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INFANT BEHAVIOR AND DEVelOPMENT 11305-318 (1988)
Behavioral Differences Between Preterm and Full-Term Newborns
as Measured with the APIB System Scores I
HEIDELISE ALS FRANK H DuFFY AND GLORIA B MCANULTY
Harvard Medical School and
Childrens Hospital Boston
This study investigates the association between gestational age at birth and behavioral functioning 2 weeks after due date Ninety-eight healthy newborns were stratified into three gestational age groups---early-born preterms (PPT) Z7 to 32 weeks middle-group preterms (PT) 33 to 37 weeks and full-terms (FT) 38 to 41 weeks--and their behavior was examined using the system scores of the Assessment of Preterm Infants Behavior (APIS) All infants were free of medical complications The PPTs (n=33) and the PTs (n=31) showed significantly more autonomic motoric state ottentional and self-regulatory disorganization and reactivity and required substantially more examiner facilitation than the FTs (n=34) The differences between PPTs and PTs ware less pronounced and did not reach significance Prospective classification of a second sample of 20 full-terms and 20 preterms under 3J --eeks gestation using discrimination rules based upon the first sample hod an overall success of 925 This study suggests that healthy preterm infants show significantly more disorganized behavior than healthy fullmiddot terms at 2 weeks after due date The APIB appears to be a robust measure of such preterm-fullmiddotterm differences
APIS behavior preterrn-ful-term behavioral differences
This study investigates whether or not healthy preterm infants of varying gesshytational age at birth catch up behaviorally to full-term infants by the time they reach 2 weeks after expected due date Behavioral differences between preterms and full-terms have been variously attributed to the medically more
This research was supponed by NICHD grants ROIHDl86S4 to H Als and ROIHDI8761 to FH Duffy NIDRR grant 0008720110 to H Als and the Mental Retardation Grant P30HDl86SS to CF Barlow Data used for replication werecoUCCled with suppon from NIMH grant HDI0889 to T B Brazelton whom we thank together with his coUaborators BM Lester and MW Yogman We thank our Department Chairmen S Walzer (Psychiatry) and CF Barlow (Neurology) for their suppon and MF Epstein Director Joint Program in Neonatology and his medical and nursing staff for their continued facilitation of our research efforts We also thank our assistants D Moir S Phillips S Gillis and A Rossow our research secretaries C Murray and C Taymor and our editor D McAnulty for their supponive efforts Foremost we thank all families for their generous panicipation
Correspondence and requests for reprints should be sent to H Als Enders M-29 The Chilshydrens Hospital 320 Longwood Avenue Boston MA 02115
305
306 AlS DUFFY AND McANULTY
compromised status of the preterm infant and to the expectations of the parents for their infants functioning (Minde Perrotta amp Marton 1985) Paludetto and his associates (Pa(udetto et aI 1982) reported using the Brazelshyton Neonatal Behavioral Assessment Scale (NBAS Brazelton 1973) that preshyterm infants without any serious disorder reaching term do as well as full-term infants These results are based on 20 healthy preterms with a wide range of gestational age at birth and 20 healthy full-terms In contrast Ferrari Grosoli Fontana and Cavazzuti (1983) reported that a group of 20 healthy preterms of equal to or less than 33 weeks gestation at birth when compared at term to 20 healthy full-term infants of 5 days post delivery performed consistently more poorly on the NBAS in terms of orientation motor performance and regulashytion of state and autonomic functioning Previously Sell and her coworkers (Sell Luick Poisson amp Hill 1980) had confirmed this finding on a sample of 188 very low birth-weight laquo 1500 gms) infants using the NBAS with additional descriptive scales specifically designed for the behavioral repertoire of preshyterms that is a prepublication version of the Assessment of Preterm Infants Behavior (APIB A1s Lester Tronick amp Brazelton 1982a 1982b) Thus it appears that the status of preterms 33 weeks or less gestational age at birth may well be associated with behavioral differences at term even in the absence of medical complications It is not clear from these studies whether or not gesshytational age of greater than 33 weeks is also associated with behavioral differshyences Furthermore the choice of assessment instrument appears to influence the results obtained
Our study consisted of two pans First we examined three groups of infants (total N =98) selected to be free of all medical complications and spanning the gestational age continuum from 27 to 41 weeks at birth We used as a behavshyioral assessment instrument the APIB which was specifically developed for the better documentation of preterm-full-term differences and focuses on the threshold to disorganized performance from modulated performance (Als et albullbull 1982a 1982b) We investigated whether or not this assessment reliably difshyferentiates healthy preterms from full-terms and what the functional differshyences between preterms and full-terms are Second we examined how consistent these group differences are across populations by applying the discrimination rules developed from the first sample to a second smaller sample of preterms and full-terms
STUDY 1 EXAMINATION OF PRETERM-FIJLL TERM DIFFERENCES
Method
Subjects Our sample included 98 appropriate-for-gestational age in weight (AGA) newborns who were selected to be free of (a) known neurological comshypromise (b) medical problems in infant and mother (c) documented social
307 APIB PRETERM BEHAVIOR
hardships in the family and (d) drug and alcohol abuse All infants were to have a high likelihood of normal development The infants spanned the gestashytional age continuum in approximately equal numbers as follows
1 Thirty-three infants were between 27 and 32 weeks gestational age at binh and were referred to as PPTs (very early preterms) The infants were selected to be healthy and specifically free of intraventricular hemorrhage (assessed by double-blind head ultrasound [US] review of on the average four consecutive USs at approximately day 2 day 10-14 day 30 and day 60) perinatal asphyxia seizures bronchopulmonary dysplasia necrotizing enJerocolitis and unresolved retinopathy of prematurity-the major medical conditions associated with early prematurity Founeen infants had been intubated with a mean duration on the respirator of 224 days (SD = 538 days) All 14 were judged to have had mild hyaline membrane disease by lung x-ray review
2 Thiny-one infants were between 33 and 37 weeks gestational age at birth and were referred to as PTs (middle preterms) They met all the criteria that the PPTs met except that none of them was intubated although four needed supplemental oxygen with a mean of 053 days (SD = 188) and one had mild hyaline membrane disease They were healthy preterms
3 Thirty-four infants were between 38 and 41 weeks gestational age at birth and were referred to as Frs (full-terms) They were selected to have Apgar ratings of 7 or better at 1 min of age and 8 or better at 5 min and were healthy full-term newborns
All twins were excluded as were any infants with any kind of congenital or chromosomal abnormalities or intrauterine infections Gestational age was assessed by routinely performed Dubowitz examination within the frrst 6 hours after delivery (Dubowitz Dubowitz amp Goldberg 1970) and was confrrmedby mothers report of her expected date of confinement (EDC) In cases of disshycrepancy (maximum discrepancy was 2 weeks) mothers dates were used
All infants were inborn in the same hospital which has a large maternity service and a level III neonatal intensive care unit (NICU) All infants were at home with their parents by 41 weeks postconception and were considered medshyically healthy Table 1 shows the perinatal medical and socioeconomic characshyteristics of the three gestational age groups studied As expected there were significant differences in binh weight gestational age at birth and Apgar ratings between the three groups (Note that because of the unequal variances of several of the parameters as tested by Levenes Test [Levene 1960] instead of a simple analysis of variance F test the Brown-Forsythe Test of Equality of Means (P) [Brown amp Forsythe 19741 which does not assume variances to be equal was used Subsequent pair-wise t tests with pooled variance were pershyformed for all variables with significant Ps To adjust for the fact that a large number of tests was made Bonferronis probabilities were used [Abt 1983 Feller 1957] The BMDP program 7D was utilized for these analyses) The inshy
bullbullbull
bullbullbull
bullbullbull
~
TABLE 1 Perinatal Characteristics of Geltational Age Groups Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
Perinatal Variables FT n=~
PT n=31
PPT n=33
Significance Test FTPT FTPPT PTlPPT
Geltatlonal age (weeks)
Birth weight (gms)
Apgar l-mln
5-mln
Gestational age at discharge from hospital (weeks)
Maternal age (years)
Parity
Ethnicity blacklother Gender malefemale Social cia I 1I1111IV V
3950 (119) 34SO ( 98)
81 (07)
906 (02) 3988 (112) 3018 (564)
171 (09) 628 1618
211103
34904 (137) 2258 (55) 752
(139) 855
(081) 3698 (19 ) 2897 (609)
190 (189) 8123 1912
71717
3021 (158) 1392 (SO) 555
(259) 72
(170) 3665 (195) 2767 (586)
12 (075) 825 1 19
13137
Fmiddot=37605middotmiddotmiddot
Fmiddot=l133middot
F = 232middot
F= 2361
F= 35704middot
Fmiddot= 153
F= 110
X= 071 X= 26 X= 1081middot
ns
ns
nl
ns
bullbullbull bull bullbull bullbullbull
bullbullbull bullbullbull ns
ns ns
nl ns
Nole FT=full-term 38 to l weeks PT=preterm 33 to 37 weeks PPT=prepreterm 27 to 32 weeks bull plt05 pltOOl pltOOOO1
309 APIB PRETERM BEHAVIOR
fants also differed in age at hospital discharge with both preterm groups being younger that is discharged before expected due date reflecting their good health status There were no maternal age parity ethnicity or gender differshyences between the three gestational age groups
Social class was assessed using the five Hollingshead (HoHingshead 1975) categories collapsed into three categories as follows Class I and II Class III and Class IV and V Chi-square test showed a significant distribution differshyence with more Class I and II families in the FT group although recruitment was not purposefully biased in this direction
Procedure AIl infants were brought by one or both parents to a specially designed quiet darkened examination room at Childrens Hospital and exshyamined with the APIB at 42 weeks postconception Testing at the hospital was chosen rather than testing at home because it allows for control and standardishyzation of the testing environment including temperature lighting and other interfering variables There were no significant differences in age at testing between the three groups The examinations were scheduled so that the infant had been fed approximately 2Yz hours prior to the examination and was comshyfortably asleep at the beginning of the examination Parents were present durshying the examination The examinations were performed by an experienced APIB examiner who had been trained to reliability by the first author or they were performed by the first author herself Both examiners were unfamiliar with the gestational age group status of the infants at testing AIl parents were specifically instructed at recruitment and when scheduled for the visit not to reveal the gestational age status of their child to the examiners Every fifth examination was conducted with the first author present and was scored indeshypendently by both examiners in order to assure continued maintenance of high interrater reliability
Measure The infants behavioral functioning was assessed with the APIB As previously described this assessment was developed in order to quantify not only the skill repenoire of the preterm and full-term infant but foremost to measure the infants reactivity and threshold of disorganization and stress to environmental input (Als 1982 1983 1985 AIs amp Brazelton 1981) The inshystrument focuses on six primary areas of newborn behavioral functioning
(1) the autonomic system (2) the motor system (3) the state system (4) the attentioninteractive system (5) the self-regulation system and (6) the degree of examiner or environmental facilitation needed to help the inshy
fant maintain or regain an integrated balanced stale
The assessment attempts to quantify the differences between for instance the infant who can muster altemess and show visual following to animate and inshy
310 ALS DUFFY AND McANULTY
animate stimuli but only with extreme stress to his autonomic and m010r sysshytem and the infant who has leeway and modulation to do so with animation and without autonomic and motoric stress
The APIB uses the maneuvers of the NBAS as a graded sequence of increasshyingly demanding environmental inputs or packages moving from distal stimulation presented during sleep to tactile stimulation which is gradually paired with vestibular stimulation The social interactive attentional package is administered at the point in the examination when the infanCs behavioral organization indicates his readiness for this sequence and before he or she is exhausted by the tactile inputs During each of the six examination packages the examiner monitors the infants reactions and behaviors along the six systems of functioning listed above
The system parameters are unique to the APIB and go beyond the NBAS assessment They are behavioraHy defined and scaled from i (well-modulated performance) to 9 (disorganized performance) Per package three scores are given for the autonomic motor state organizational and self-regulation sysshytems a baseline score (B) for the infants functioning prior to the adminisshytration of the maneuvers of the package a response score (R) capturing the infants functioning during the administration of the maneuvers of the packshyage and a post package status score (P) describing the infants functioning after the administration of the tasks and before facilitation for the next baseshyline The attentional capacity of the infant is scored in terms of B R and P only during the maneuvers of package VI which are specifically geared to elicit attention and orientation Necessary examiner facilitation is given one score per package The autonomic motor state and self-regulatory systems thus are quantified by 18 scores each (one B R and P score per package) the attentional system by 3 scores (one B R and P score for package VI only) and examiner facilitation by 6 scores one per package yielding a total 0pound 81 scores These 81 scores are reduced to 6 summary scores by forming the mean of the B R and P scores per package for each system These 6 scores are reshyferred to as the system scores and are thought to identify the differential subsystem stability of the infant They are considered to be the key parameters of the APIB and are the measures used in this study
Extensive experience with preterms and specific training is necessary in order to administer and score the APIB reliably Specific reliability criteria are applied They demand above 9800 agreement of all the 9-point scales to within 1 point that is not more than 2 of the 81 scores may be off by 2 points The I-point agreement is set at 9000 that is of the 81 scores 72 must agree to the point For the current study 20 examinations were scored independently by two examiners The overall Pearsons r was 99 Rs ranged from 98 for exshyaminer facilitation to 99 for the five other parameters thus readily meeting the specified interrater reliability criteria In addition to the six system paramshyeters the APIB yields 204 specific scores on detailed aspects of autonomic motor (including reflex performance) state organizational orientation and
311 APIB PRETERM BEHAVIOR
self-regulation functioning of the infant These can be reduced to 26 operashytionally mutually exclusive summary scores (Als 1987) These variables will not be considered in this report
The three gestational age (GA) groups were compared on the six APIB sysshytem parameters Because several of the APIB parameters showed unequal varishyances by Levenes Test for Variances the Brown-Forsythe Equality of Means Test (F$) which does not assume variances to be equal was again employed as it had been for the perinatal background variable exploration described above For all comparisons with significant F$ tests pair-wise I tests with pooled variance were performed between the gestational groups IT and PT IT and PPT and PT and PPT To adjust for the fact that a large number of tests was made these tests were again accompanied by Bonferronis probabilities
Results Table 2 shows the results for the six APIB system variables autonomic organishyzation motoric organization state organization attentional organization self-regulation and examiner facilitation All six system parameters show proshynounced GA group differences The pattern of results across variables is conshysistent On all parameters the full-term group is the most well-modulated well-functioning group The middle-preterm group (PT) takes a middle posishytion and the early-born preterms (PPT) show the most disorganized perforshymance with low threshold to stress and hypersensitive reaction The differshyences are most pronounced between the IT group and the PPT group next between the FT group and the PT group The differences between the PTs and the PPTs do not reach significance Our results indicate that there are consisshytent organizational differences between healthy full-terms and their medically healthy preterm peers when examined at 2 weeks post-term
To delineate specifically the areas of difference the earliest born group (~ 32 weeks GA) shows the greatest difference from the full-term group The PPTs
still show moderate autonomic instability and reactivity moderate motoric disorganization moderate difficulties in self-regulation and considerable difficulties in maintaining alenness They require moderate to considerable facilitation from the examiner in order to regain stabilization In contrast the full-terms show very mild autonomic reactivity and only very mild or occasional motoric disorganization with intermittent difficulty in state regulation and moderate difficulty in maintaining flexible modulated alertness yet quite adeshyquate self-regulation requiring only mild to moderate facilitation from the examiner The middle-group preterms (33-37 weeks GA) show significantly more stress than the Frs on all parameters and are more like the PPTs The APIB system parameters thus are very sensitive to preterm-full-term differshyences in functioning which appear to be still present at 2 weeks beyond due date
Because social-class membership showed significant GA group differences the contribution of social-class status to the APIB results was examined by pershy
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
306 AlS DUFFY AND McANULTY
compromised status of the preterm infant and to the expectations of the parents for their infants functioning (Minde Perrotta amp Marton 1985) Paludetto and his associates (Pa(udetto et aI 1982) reported using the Brazelshyton Neonatal Behavioral Assessment Scale (NBAS Brazelton 1973) that preshyterm infants without any serious disorder reaching term do as well as full-term infants These results are based on 20 healthy preterms with a wide range of gestational age at birth and 20 healthy full-terms In contrast Ferrari Grosoli Fontana and Cavazzuti (1983) reported that a group of 20 healthy preterms of equal to or less than 33 weeks gestation at birth when compared at term to 20 healthy full-term infants of 5 days post delivery performed consistently more poorly on the NBAS in terms of orientation motor performance and regulashytion of state and autonomic functioning Previously Sell and her coworkers (Sell Luick Poisson amp Hill 1980) had confirmed this finding on a sample of 188 very low birth-weight laquo 1500 gms) infants using the NBAS with additional descriptive scales specifically designed for the behavioral repertoire of preshyterms that is a prepublication version of the Assessment of Preterm Infants Behavior (APIB A1s Lester Tronick amp Brazelton 1982a 1982b) Thus it appears that the status of preterms 33 weeks or less gestational age at birth may well be associated with behavioral differences at term even in the absence of medical complications It is not clear from these studies whether or not gesshytational age of greater than 33 weeks is also associated with behavioral differshyences Furthermore the choice of assessment instrument appears to influence the results obtained
Our study consisted of two pans First we examined three groups of infants (total N =98) selected to be free of all medical complications and spanning the gestational age continuum from 27 to 41 weeks at birth We used as a behavshyioral assessment instrument the APIB which was specifically developed for the better documentation of preterm-full-term differences and focuses on the threshold to disorganized performance from modulated performance (Als et albullbull 1982a 1982b) We investigated whether or not this assessment reliably difshyferentiates healthy preterms from full-terms and what the functional differshyences between preterms and full-terms are Second we examined how consistent these group differences are across populations by applying the discrimination rules developed from the first sample to a second smaller sample of preterms and full-terms
STUDY 1 EXAMINATION OF PRETERM-FIJLL TERM DIFFERENCES
Method
Subjects Our sample included 98 appropriate-for-gestational age in weight (AGA) newborns who were selected to be free of (a) known neurological comshypromise (b) medical problems in infant and mother (c) documented social
307 APIB PRETERM BEHAVIOR
hardships in the family and (d) drug and alcohol abuse All infants were to have a high likelihood of normal development The infants spanned the gestashytional age continuum in approximately equal numbers as follows
1 Thirty-three infants were between 27 and 32 weeks gestational age at binh and were referred to as PPTs (very early preterms) The infants were selected to be healthy and specifically free of intraventricular hemorrhage (assessed by double-blind head ultrasound [US] review of on the average four consecutive USs at approximately day 2 day 10-14 day 30 and day 60) perinatal asphyxia seizures bronchopulmonary dysplasia necrotizing enJerocolitis and unresolved retinopathy of prematurity-the major medical conditions associated with early prematurity Founeen infants had been intubated with a mean duration on the respirator of 224 days (SD = 538 days) All 14 were judged to have had mild hyaline membrane disease by lung x-ray review
2 Thiny-one infants were between 33 and 37 weeks gestational age at birth and were referred to as PTs (middle preterms) They met all the criteria that the PPTs met except that none of them was intubated although four needed supplemental oxygen with a mean of 053 days (SD = 188) and one had mild hyaline membrane disease They were healthy preterms
3 Thirty-four infants were between 38 and 41 weeks gestational age at birth and were referred to as Frs (full-terms) They were selected to have Apgar ratings of 7 or better at 1 min of age and 8 or better at 5 min and were healthy full-term newborns
All twins were excluded as were any infants with any kind of congenital or chromosomal abnormalities or intrauterine infections Gestational age was assessed by routinely performed Dubowitz examination within the frrst 6 hours after delivery (Dubowitz Dubowitz amp Goldberg 1970) and was confrrmedby mothers report of her expected date of confinement (EDC) In cases of disshycrepancy (maximum discrepancy was 2 weeks) mothers dates were used
All infants were inborn in the same hospital which has a large maternity service and a level III neonatal intensive care unit (NICU) All infants were at home with their parents by 41 weeks postconception and were considered medshyically healthy Table 1 shows the perinatal medical and socioeconomic characshyteristics of the three gestational age groups studied As expected there were significant differences in binh weight gestational age at birth and Apgar ratings between the three groups (Note that because of the unequal variances of several of the parameters as tested by Levenes Test [Levene 1960] instead of a simple analysis of variance F test the Brown-Forsythe Test of Equality of Means (P) [Brown amp Forsythe 19741 which does not assume variances to be equal was used Subsequent pair-wise t tests with pooled variance were pershyformed for all variables with significant Ps To adjust for the fact that a large number of tests was made Bonferronis probabilities were used [Abt 1983 Feller 1957] The BMDP program 7D was utilized for these analyses) The inshy
bullbullbull
bullbullbull
bullbullbull
~
TABLE 1 Perinatal Characteristics of Geltational Age Groups Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
Perinatal Variables FT n=~
PT n=31
PPT n=33
Significance Test FTPT FTPPT PTlPPT
Geltatlonal age (weeks)
Birth weight (gms)
Apgar l-mln
5-mln
Gestational age at discharge from hospital (weeks)
Maternal age (years)
Parity
Ethnicity blacklother Gender malefemale Social cia I 1I1111IV V
3950 (119) 34SO ( 98)
81 (07)
906 (02) 3988 (112) 3018 (564)
171 (09) 628 1618
211103
34904 (137) 2258 (55) 752
(139) 855
(081) 3698 (19 ) 2897 (609)
190 (189) 8123 1912
71717
3021 (158) 1392 (SO) 555
(259) 72
(170) 3665 (195) 2767 (586)
12 (075) 825 1 19
13137
Fmiddot=37605middotmiddotmiddot
Fmiddot=l133middot
F = 232middot
F= 2361
F= 35704middot
Fmiddot= 153
F= 110
X= 071 X= 26 X= 1081middot
ns
ns
nl
ns
bullbullbull bull bullbull bullbullbull
bullbullbull bullbullbull ns
ns ns
nl ns
Nole FT=full-term 38 to l weeks PT=preterm 33 to 37 weeks PPT=prepreterm 27 to 32 weeks bull plt05 pltOOl pltOOOO1
309 APIB PRETERM BEHAVIOR
fants also differed in age at hospital discharge with both preterm groups being younger that is discharged before expected due date reflecting their good health status There were no maternal age parity ethnicity or gender differshyences between the three gestational age groups
Social class was assessed using the five Hollingshead (HoHingshead 1975) categories collapsed into three categories as follows Class I and II Class III and Class IV and V Chi-square test showed a significant distribution differshyence with more Class I and II families in the FT group although recruitment was not purposefully biased in this direction
Procedure AIl infants were brought by one or both parents to a specially designed quiet darkened examination room at Childrens Hospital and exshyamined with the APIB at 42 weeks postconception Testing at the hospital was chosen rather than testing at home because it allows for control and standardishyzation of the testing environment including temperature lighting and other interfering variables There were no significant differences in age at testing between the three groups The examinations were scheduled so that the infant had been fed approximately 2Yz hours prior to the examination and was comshyfortably asleep at the beginning of the examination Parents were present durshying the examination The examinations were performed by an experienced APIB examiner who had been trained to reliability by the first author or they were performed by the first author herself Both examiners were unfamiliar with the gestational age group status of the infants at testing AIl parents were specifically instructed at recruitment and when scheduled for the visit not to reveal the gestational age status of their child to the examiners Every fifth examination was conducted with the first author present and was scored indeshypendently by both examiners in order to assure continued maintenance of high interrater reliability
Measure The infants behavioral functioning was assessed with the APIB As previously described this assessment was developed in order to quantify not only the skill repenoire of the preterm and full-term infant but foremost to measure the infants reactivity and threshold of disorganization and stress to environmental input (Als 1982 1983 1985 AIs amp Brazelton 1981) The inshystrument focuses on six primary areas of newborn behavioral functioning
(1) the autonomic system (2) the motor system (3) the state system (4) the attentioninteractive system (5) the self-regulation system and (6) the degree of examiner or environmental facilitation needed to help the inshy
fant maintain or regain an integrated balanced stale
The assessment attempts to quantify the differences between for instance the infant who can muster altemess and show visual following to animate and inshy
310 ALS DUFFY AND McANULTY
animate stimuli but only with extreme stress to his autonomic and m010r sysshytem and the infant who has leeway and modulation to do so with animation and without autonomic and motoric stress
The APIB uses the maneuvers of the NBAS as a graded sequence of increasshyingly demanding environmental inputs or packages moving from distal stimulation presented during sleep to tactile stimulation which is gradually paired with vestibular stimulation The social interactive attentional package is administered at the point in the examination when the infanCs behavioral organization indicates his readiness for this sequence and before he or she is exhausted by the tactile inputs During each of the six examination packages the examiner monitors the infants reactions and behaviors along the six systems of functioning listed above
The system parameters are unique to the APIB and go beyond the NBAS assessment They are behavioraHy defined and scaled from i (well-modulated performance) to 9 (disorganized performance) Per package three scores are given for the autonomic motor state organizational and self-regulation sysshytems a baseline score (B) for the infants functioning prior to the adminisshytration of the maneuvers of the package a response score (R) capturing the infants functioning during the administration of the maneuvers of the packshyage and a post package status score (P) describing the infants functioning after the administration of the tasks and before facilitation for the next baseshyline The attentional capacity of the infant is scored in terms of B R and P only during the maneuvers of package VI which are specifically geared to elicit attention and orientation Necessary examiner facilitation is given one score per package The autonomic motor state and self-regulatory systems thus are quantified by 18 scores each (one B R and P score per package) the attentional system by 3 scores (one B R and P score for package VI only) and examiner facilitation by 6 scores one per package yielding a total 0pound 81 scores These 81 scores are reduced to 6 summary scores by forming the mean of the B R and P scores per package for each system These 6 scores are reshyferred to as the system scores and are thought to identify the differential subsystem stability of the infant They are considered to be the key parameters of the APIB and are the measures used in this study
Extensive experience with preterms and specific training is necessary in order to administer and score the APIB reliably Specific reliability criteria are applied They demand above 9800 agreement of all the 9-point scales to within 1 point that is not more than 2 of the 81 scores may be off by 2 points The I-point agreement is set at 9000 that is of the 81 scores 72 must agree to the point For the current study 20 examinations were scored independently by two examiners The overall Pearsons r was 99 Rs ranged from 98 for exshyaminer facilitation to 99 for the five other parameters thus readily meeting the specified interrater reliability criteria In addition to the six system paramshyeters the APIB yields 204 specific scores on detailed aspects of autonomic motor (including reflex performance) state organizational orientation and
311 APIB PRETERM BEHAVIOR
self-regulation functioning of the infant These can be reduced to 26 operashytionally mutually exclusive summary scores (Als 1987) These variables will not be considered in this report
The three gestational age (GA) groups were compared on the six APIB sysshytem parameters Because several of the APIB parameters showed unequal varishyances by Levenes Test for Variances the Brown-Forsythe Equality of Means Test (F$) which does not assume variances to be equal was again employed as it had been for the perinatal background variable exploration described above For all comparisons with significant F$ tests pair-wise I tests with pooled variance were performed between the gestational groups IT and PT IT and PPT and PT and PPT To adjust for the fact that a large number of tests was made these tests were again accompanied by Bonferronis probabilities
Results Table 2 shows the results for the six APIB system variables autonomic organishyzation motoric organization state organization attentional organization self-regulation and examiner facilitation All six system parameters show proshynounced GA group differences The pattern of results across variables is conshysistent On all parameters the full-term group is the most well-modulated well-functioning group The middle-preterm group (PT) takes a middle posishytion and the early-born preterms (PPT) show the most disorganized perforshymance with low threshold to stress and hypersensitive reaction The differshyences are most pronounced between the IT group and the PPT group next between the FT group and the PT group The differences between the PTs and the PPTs do not reach significance Our results indicate that there are consisshytent organizational differences between healthy full-terms and their medically healthy preterm peers when examined at 2 weeks post-term
To delineate specifically the areas of difference the earliest born group (~ 32 weeks GA) shows the greatest difference from the full-term group The PPTs
still show moderate autonomic instability and reactivity moderate motoric disorganization moderate difficulties in self-regulation and considerable difficulties in maintaining alenness They require moderate to considerable facilitation from the examiner in order to regain stabilization In contrast the full-terms show very mild autonomic reactivity and only very mild or occasional motoric disorganization with intermittent difficulty in state regulation and moderate difficulty in maintaining flexible modulated alertness yet quite adeshyquate self-regulation requiring only mild to moderate facilitation from the examiner The middle-group preterms (33-37 weeks GA) show significantly more stress than the Frs on all parameters and are more like the PPTs The APIB system parameters thus are very sensitive to preterm-full-term differshyences in functioning which appear to be still present at 2 weeks beyond due date
Because social-class membership showed significant GA group differences the contribution of social-class status to the APIB results was examined by pershy
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
307 APIB PRETERM BEHAVIOR
hardships in the family and (d) drug and alcohol abuse All infants were to have a high likelihood of normal development The infants spanned the gestashytional age continuum in approximately equal numbers as follows
1 Thirty-three infants were between 27 and 32 weeks gestational age at binh and were referred to as PPTs (very early preterms) The infants were selected to be healthy and specifically free of intraventricular hemorrhage (assessed by double-blind head ultrasound [US] review of on the average four consecutive USs at approximately day 2 day 10-14 day 30 and day 60) perinatal asphyxia seizures bronchopulmonary dysplasia necrotizing enJerocolitis and unresolved retinopathy of prematurity-the major medical conditions associated with early prematurity Founeen infants had been intubated with a mean duration on the respirator of 224 days (SD = 538 days) All 14 were judged to have had mild hyaline membrane disease by lung x-ray review
2 Thiny-one infants were between 33 and 37 weeks gestational age at birth and were referred to as PTs (middle preterms) They met all the criteria that the PPTs met except that none of them was intubated although four needed supplemental oxygen with a mean of 053 days (SD = 188) and one had mild hyaline membrane disease They were healthy preterms
3 Thirty-four infants were between 38 and 41 weeks gestational age at birth and were referred to as Frs (full-terms) They were selected to have Apgar ratings of 7 or better at 1 min of age and 8 or better at 5 min and were healthy full-term newborns
All twins were excluded as were any infants with any kind of congenital or chromosomal abnormalities or intrauterine infections Gestational age was assessed by routinely performed Dubowitz examination within the frrst 6 hours after delivery (Dubowitz Dubowitz amp Goldberg 1970) and was confrrmedby mothers report of her expected date of confinement (EDC) In cases of disshycrepancy (maximum discrepancy was 2 weeks) mothers dates were used
All infants were inborn in the same hospital which has a large maternity service and a level III neonatal intensive care unit (NICU) All infants were at home with their parents by 41 weeks postconception and were considered medshyically healthy Table 1 shows the perinatal medical and socioeconomic characshyteristics of the three gestational age groups studied As expected there were significant differences in binh weight gestational age at birth and Apgar ratings between the three groups (Note that because of the unequal variances of several of the parameters as tested by Levenes Test [Levene 1960] instead of a simple analysis of variance F test the Brown-Forsythe Test of Equality of Means (P) [Brown amp Forsythe 19741 which does not assume variances to be equal was used Subsequent pair-wise t tests with pooled variance were pershyformed for all variables with significant Ps To adjust for the fact that a large number of tests was made Bonferronis probabilities were used [Abt 1983 Feller 1957] The BMDP program 7D was utilized for these analyses) The inshy
bullbullbull
bullbullbull
bullbullbull
~
TABLE 1 Perinatal Characteristics of Geltational Age Groups Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
Perinatal Variables FT n=~
PT n=31
PPT n=33
Significance Test FTPT FTPPT PTlPPT
Geltatlonal age (weeks)
Birth weight (gms)
Apgar l-mln
5-mln
Gestational age at discharge from hospital (weeks)
Maternal age (years)
Parity
Ethnicity blacklother Gender malefemale Social cia I 1I1111IV V
3950 (119) 34SO ( 98)
81 (07)
906 (02) 3988 (112) 3018 (564)
171 (09) 628 1618
211103
34904 (137) 2258 (55) 752
(139) 855
(081) 3698 (19 ) 2897 (609)
190 (189) 8123 1912
71717
3021 (158) 1392 (SO) 555
(259) 72
(170) 3665 (195) 2767 (586)
12 (075) 825 1 19
13137
Fmiddot=37605middotmiddotmiddot
Fmiddot=l133middot
F = 232middot
F= 2361
F= 35704middot
Fmiddot= 153
F= 110
X= 071 X= 26 X= 1081middot
ns
ns
nl
ns
bullbullbull bull bullbull bullbullbull
bullbullbull bullbullbull ns
ns ns
nl ns
Nole FT=full-term 38 to l weeks PT=preterm 33 to 37 weeks PPT=prepreterm 27 to 32 weeks bull plt05 pltOOl pltOOOO1
309 APIB PRETERM BEHAVIOR
fants also differed in age at hospital discharge with both preterm groups being younger that is discharged before expected due date reflecting their good health status There were no maternal age parity ethnicity or gender differshyences between the three gestational age groups
Social class was assessed using the five Hollingshead (HoHingshead 1975) categories collapsed into three categories as follows Class I and II Class III and Class IV and V Chi-square test showed a significant distribution differshyence with more Class I and II families in the FT group although recruitment was not purposefully biased in this direction
Procedure AIl infants were brought by one or both parents to a specially designed quiet darkened examination room at Childrens Hospital and exshyamined with the APIB at 42 weeks postconception Testing at the hospital was chosen rather than testing at home because it allows for control and standardishyzation of the testing environment including temperature lighting and other interfering variables There were no significant differences in age at testing between the three groups The examinations were scheduled so that the infant had been fed approximately 2Yz hours prior to the examination and was comshyfortably asleep at the beginning of the examination Parents were present durshying the examination The examinations were performed by an experienced APIB examiner who had been trained to reliability by the first author or they were performed by the first author herself Both examiners were unfamiliar with the gestational age group status of the infants at testing AIl parents were specifically instructed at recruitment and when scheduled for the visit not to reveal the gestational age status of their child to the examiners Every fifth examination was conducted with the first author present and was scored indeshypendently by both examiners in order to assure continued maintenance of high interrater reliability
Measure The infants behavioral functioning was assessed with the APIB As previously described this assessment was developed in order to quantify not only the skill repenoire of the preterm and full-term infant but foremost to measure the infants reactivity and threshold of disorganization and stress to environmental input (Als 1982 1983 1985 AIs amp Brazelton 1981) The inshystrument focuses on six primary areas of newborn behavioral functioning
(1) the autonomic system (2) the motor system (3) the state system (4) the attentioninteractive system (5) the self-regulation system and (6) the degree of examiner or environmental facilitation needed to help the inshy
fant maintain or regain an integrated balanced stale
The assessment attempts to quantify the differences between for instance the infant who can muster altemess and show visual following to animate and inshy
310 ALS DUFFY AND McANULTY
animate stimuli but only with extreme stress to his autonomic and m010r sysshytem and the infant who has leeway and modulation to do so with animation and without autonomic and motoric stress
The APIB uses the maneuvers of the NBAS as a graded sequence of increasshyingly demanding environmental inputs or packages moving from distal stimulation presented during sleep to tactile stimulation which is gradually paired with vestibular stimulation The social interactive attentional package is administered at the point in the examination when the infanCs behavioral organization indicates his readiness for this sequence and before he or she is exhausted by the tactile inputs During each of the six examination packages the examiner monitors the infants reactions and behaviors along the six systems of functioning listed above
The system parameters are unique to the APIB and go beyond the NBAS assessment They are behavioraHy defined and scaled from i (well-modulated performance) to 9 (disorganized performance) Per package three scores are given for the autonomic motor state organizational and self-regulation sysshytems a baseline score (B) for the infants functioning prior to the adminisshytration of the maneuvers of the package a response score (R) capturing the infants functioning during the administration of the maneuvers of the packshyage and a post package status score (P) describing the infants functioning after the administration of the tasks and before facilitation for the next baseshyline The attentional capacity of the infant is scored in terms of B R and P only during the maneuvers of package VI which are specifically geared to elicit attention and orientation Necessary examiner facilitation is given one score per package The autonomic motor state and self-regulatory systems thus are quantified by 18 scores each (one B R and P score per package) the attentional system by 3 scores (one B R and P score for package VI only) and examiner facilitation by 6 scores one per package yielding a total 0pound 81 scores These 81 scores are reduced to 6 summary scores by forming the mean of the B R and P scores per package for each system These 6 scores are reshyferred to as the system scores and are thought to identify the differential subsystem stability of the infant They are considered to be the key parameters of the APIB and are the measures used in this study
Extensive experience with preterms and specific training is necessary in order to administer and score the APIB reliably Specific reliability criteria are applied They demand above 9800 agreement of all the 9-point scales to within 1 point that is not more than 2 of the 81 scores may be off by 2 points The I-point agreement is set at 9000 that is of the 81 scores 72 must agree to the point For the current study 20 examinations were scored independently by two examiners The overall Pearsons r was 99 Rs ranged from 98 for exshyaminer facilitation to 99 for the five other parameters thus readily meeting the specified interrater reliability criteria In addition to the six system paramshyeters the APIB yields 204 specific scores on detailed aspects of autonomic motor (including reflex performance) state organizational orientation and
311 APIB PRETERM BEHAVIOR
self-regulation functioning of the infant These can be reduced to 26 operashytionally mutually exclusive summary scores (Als 1987) These variables will not be considered in this report
The three gestational age (GA) groups were compared on the six APIB sysshytem parameters Because several of the APIB parameters showed unequal varishyances by Levenes Test for Variances the Brown-Forsythe Equality of Means Test (F$) which does not assume variances to be equal was again employed as it had been for the perinatal background variable exploration described above For all comparisons with significant F$ tests pair-wise I tests with pooled variance were performed between the gestational groups IT and PT IT and PPT and PT and PPT To adjust for the fact that a large number of tests was made these tests were again accompanied by Bonferronis probabilities
Results Table 2 shows the results for the six APIB system variables autonomic organishyzation motoric organization state organization attentional organization self-regulation and examiner facilitation All six system parameters show proshynounced GA group differences The pattern of results across variables is conshysistent On all parameters the full-term group is the most well-modulated well-functioning group The middle-preterm group (PT) takes a middle posishytion and the early-born preterms (PPT) show the most disorganized perforshymance with low threshold to stress and hypersensitive reaction The differshyences are most pronounced between the IT group and the PPT group next between the FT group and the PT group The differences between the PTs and the PPTs do not reach significance Our results indicate that there are consisshytent organizational differences between healthy full-terms and their medically healthy preterm peers when examined at 2 weeks post-term
To delineate specifically the areas of difference the earliest born group (~ 32 weeks GA) shows the greatest difference from the full-term group The PPTs
still show moderate autonomic instability and reactivity moderate motoric disorganization moderate difficulties in self-regulation and considerable difficulties in maintaining alenness They require moderate to considerable facilitation from the examiner in order to regain stabilization In contrast the full-terms show very mild autonomic reactivity and only very mild or occasional motoric disorganization with intermittent difficulty in state regulation and moderate difficulty in maintaining flexible modulated alertness yet quite adeshyquate self-regulation requiring only mild to moderate facilitation from the examiner The middle-group preterms (33-37 weeks GA) show significantly more stress than the Frs on all parameters and are more like the PPTs The APIB system parameters thus are very sensitive to preterm-full-term differshyences in functioning which appear to be still present at 2 weeks beyond due date
Because social-class membership showed significant GA group differences the contribution of social-class status to the APIB results was examined by pershy
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
bullbullbull
bullbullbull
bullbullbull
~
TABLE 1 Perinatal Characteristics of Geltational Age Groups Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
Perinatal Variables FT n=~
PT n=31
PPT n=33
Significance Test FTPT FTPPT PTlPPT
Geltatlonal age (weeks)
Birth weight (gms)
Apgar l-mln
5-mln
Gestational age at discharge from hospital (weeks)
Maternal age (years)
Parity
Ethnicity blacklother Gender malefemale Social cia I 1I1111IV V
3950 (119) 34SO ( 98)
81 (07)
906 (02) 3988 (112) 3018 (564)
171 (09) 628 1618
211103
34904 (137) 2258 (55) 752
(139) 855
(081) 3698 (19 ) 2897 (609)
190 (189) 8123 1912
71717
3021 (158) 1392 (SO) 555
(259) 72
(170) 3665 (195) 2767 (586)
12 (075) 825 1 19
13137
Fmiddot=37605middotmiddotmiddot
Fmiddot=l133middot
F = 232middot
F= 2361
F= 35704middot
Fmiddot= 153
F= 110
X= 071 X= 26 X= 1081middot
ns
ns
nl
ns
bullbullbull bull bullbull bullbullbull
bullbullbull bullbullbull ns
ns ns
nl ns
Nole FT=full-term 38 to l weeks PT=preterm 33 to 37 weeks PPT=prepreterm 27 to 32 weeks bull plt05 pltOOl pltOOOO1
309 APIB PRETERM BEHAVIOR
fants also differed in age at hospital discharge with both preterm groups being younger that is discharged before expected due date reflecting their good health status There were no maternal age parity ethnicity or gender differshyences between the three gestational age groups
Social class was assessed using the five Hollingshead (HoHingshead 1975) categories collapsed into three categories as follows Class I and II Class III and Class IV and V Chi-square test showed a significant distribution differshyence with more Class I and II families in the FT group although recruitment was not purposefully biased in this direction
Procedure AIl infants were brought by one or both parents to a specially designed quiet darkened examination room at Childrens Hospital and exshyamined with the APIB at 42 weeks postconception Testing at the hospital was chosen rather than testing at home because it allows for control and standardishyzation of the testing environment including temperature lighting and other interfering variables There were no significant differences in age at testing between the three groups The examinations were scheduled so that the infant had been fed approximately 2Yz hours prior to the examination and was comshyfortably asleep at the beginning of the examination Parents were present durshying the examination The examinations were performed by an experienced APIB examiner who had been trained to reliability by the first author or they were performed by the first author herself Both examiners were unfamiliar with the gestational age group status of the infants at testing AIl parents were specifically instructed at recruitment and when scheduled for the visit not to reveal the gestational age status of their child to the examiners Every fifth examination was conducted with the first author present and was scored indeshypendently by both examiners in order to assure continued maintenance of high interrater reliability
Measure The infants behavioral functioning was assessed with the APIB As previously described this assessment was developed in order to quantify not only the skill repenoire of the preterm and full-term infant but foremost to measure the infants reactivity and threshold of disorganization and stress to environmental input (Als 1982 1983 1985 AIs amp Brazelton 1981) The inshystrument focuses on six primary areas of newborn behavioral functioning
(1) the autonomic system (2) the motor system (3) the state system (4) the attentioninteractive system (5) the self-regulation system and (6) the degree of examiner or environmental facilitation needed to help the inshy
fant maintain or regain an integrated balanced stale
The assessment attempts to quantify the differences between for instance the infant who can muster altemess and show visual following to animate and inshy
310 ALS DUFFY AND McANULTY
animate stimuli but only with extreme stress to his autonomic and m010r sysshytem and the infant who has leeway and modulation to do so with animation and without autonomic and motoric stress
The APIB uses the maneuvers of the NBAS as a graded sequence of increasshyingly demanding environmental inputs or packages moving from distal stimulation presented during sleep to tactile stimulation which is gradually paired with vestibular stimulation The social interactive attentional package is administered at the point in the examination when the infanCs behavioral organization indicates his readiness for this sequence and before he or she is exhausted by the tactile inputs During each of the six examination packages the examiner monitors the infants reactions and behaviors along the six systems of functioning listed above
The system parameters are unique to the APIB and go beyond the NBAS assessment They are behavioraHy defined and scaled from i (well-modulated performance) to 9 (disorganized performance) Per package three scores are given for the autonomic motor state organizational and self-regulation sysshytems a baseline score (B) for the infants functioning prior to the adminisshytration of the maneuvers of the package a response score (R) capturing the infants functioning during the administration of the maneuvers of the packshyage and a post package status score (P) describing the infants functioning after the administration of the tasks and before facilitation for the next baseshyline The attentional capacity of the infant is scored in terms of B R and P only during the maneuvers of package VI which are specifically geared to elicit attention and orientation Necessary examiner facilitation is given one score per package The autonomic motor state and self-regulatory systems thus are quantified by 18 scores each (one B R and P score per package) the attentional system by 3 scores (one B R and P score for package VI only) and examiner facilitation by 6 scores one per package yielding a total 0pound 81 scores These 81 scores are reduced to 6 summary scores by forming the mean of the B R and P scores per package for each system These 6 scores are reshyferred to as the system scores and are thought to identify the differential subsystem stability of the infant They are considered to be the key parameters of the APIB and are the measures used in this study
Extensive experience with preterms and specific training is necessary in order to administer and score the APIB reliably Specific reliability criteria are applied They demand above 9800 agreement of all the 9-point scales to within 1 point that is not more than 2 of the 81 scores may be off by 2 points The I-point agreement is set at 9000 that is of the 81 scores 72 must agree to the point For the current study 20 examinations were scored independently by two examiners The overall Pearsons r was 99 Rs ranged from 98 for exshyaminer facilitation to 99 for the five other parameters thus readily meeting the specified interrater reliability criteria In addition to the six system paramshyeters the APIB yields 204 specific scores on detailed aspects of autonomic motor (including reflex performance) state organizational orientation and
311 APIB PRETERM BEHAVIOR
self-regulation functioning of the infant These can be reduced to 26 operashytionally mutually exclusive summary scores (Als 1987) These variables will not be considered in this report
The three gestational age (GA) groups were compared on the six APIB sysshytem parameters Because several of the APIB parameters showed unequal varishyances by Levenes Test for Variances the Brown-Forsythe Equality of Means Test (F$) which does not assume variances to be equal was again employed as it had been for the perinatal background variable exploration described above For all comparisons with significant F$ tests pair-wise I tests with pooled variance were performed between the gestational groups IT and PT IT and PPT and PT and PPT To adjust for the fact that a large number of tests was made these tests were again accompanied by Bonferronis probabilities
Results Table 2 shows the results for the six APIB system variables autonomic organishyzation motoric organization state organization attentional organization self-regulation and examiner facilitation All six system parameters show proshynounced GA group differences The pattern of results across variables is conshysistent On all parameters the full-term group is the most well-modulated well-functioning group The middle-preterm group (PT) takes a middle posishytion and the early-born preterms (PPT) show the most disorganized perforshymance with low threshold to stress and hypersensitive reaction The differshyences are most pronounced between the IT group and the PPT group next between the FT group and the PT group The differences between the PTs and the PPTs do not reach significance Our results indicate that there are consisshytent organizational differences between healthy full-terms and their medically healthy preterm peers when examined at 2 weeks post-term
To delineate specifically the areas of difference the earliest born group (~ 32 weeks GA) shows the greatest difference from the full-term group The PPTs
still show moderate autonomic instability and reactivity moderate motoric disorganization moderate difficulties in self-regulation and considerable difficulties in maintaining alenness They require moderate to considerable facilitation from the examiner in order to regain stabilization In contrast the full-terms show very mild autonomic reactivity and only very mild or occasional motoric disorganization with intermittent difficulty in state regulation and moderate difficulty in maintaining flexible modulated alertness yet quite adeshyquate self-regulation requiring only mild to moderate facilitation from the examiner The middle-group preterms (33-37 weeks GA) show significantly more stress than the Frs on all parameters and are more like the PPTs The APIB system parameters thus are very sensitive to preterm-full-term differshyences in functioning which appear to be still present at 2 weeks beyond due date
Because social-class membership showed significant GA group differences the contribution of social-class status to the APIB results was examined by pershy
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
309 APIB PRETERM BEHAVIOR
fants also differed in age at hospital discharge with both preterm groups being younger that is discharged before expected due date reflecting their good health status There were no maternal age parity ethnicity or gender differshyences between the three gestational age groups
Social class was assessed using the five Hollingshead (HoHingshead 1975) categories collapsed into three categories as follows Class I and II Class III and Class IV and V Chi-square test showed a significant distribution differshyence with more Class I and II families in the FT group although recruitment was not purposefully biased in this direction
Procedure AIl infants were brought by one or both parents to a specially designed quiet darkened examination room at Childrens Hospital and exshyamined with the APIB at 42 weeks postconception Testing at the hospital was chosen rather than testing at home because it allows for control and standardishyzation of the testing environment including temperature lighting and other interfering variables There were no significant differences in age at testing between the three groups The examinations were scheduled so that the infant had been fed approximately 2Yz hours prior to the examination and was comshyfortably asleep at the beginning of the examination Parents were present durshying the examination The examinations were performed by an experienced APIB examiner who had been trained to reliability by the first author or they were performed by the first author herself Both examiners were unfamiliar with the gestational age group status of the infants at testing AIl parents were specifically instructed at recruitment and when scheduled for the visit not to reveal the gestational age status of their child to the examiners Every fifth examination was conducted with the first author present and was scored indeshypendently by both examiners in order to assure continued maintenance of high interrater reliability
Measure The infants behavioral functioning was assessed with the APIB As previously described this assessment was developed in order to quantify not only the skill repenoire of the preterm and full-term infant but foremost to measure the infants reactivity and threshold of disorganization and stress to environmental input (Als 1982 1983 1985 AIs amp Brazelton 1981) The inshystrument focuses on six primary areas of newborn behavioral functioning
(1) the autonomic system (2) the motor system (3) the state system (4) the attentioninteractive system (5) the self-regulation system and (6) the degree of examiner or environmental facilitation needed to help the inshy
fant maintain or regain an integrated balanced stale
The assessment attempts to quantify the differences between for instance the infant who can muster altemess and show visual following to animate and inshy
310 ALS DUFFY AND McANULTY
animate stimuli but only with extreme stress to his autonomic and m010r sysshytem and the infant who has leeway and modulation to do so with animation and without autonomic and motoric stress
The APIB uses the maneuvers of the NBAS as a graded sequence of increasshyingly demanding environmental inputs or packages moving from distal stimulation presented during sleep to tactile stimulation which is gradually paired with vestibular stimulation The social interactive attentional package is administered at the point in the examination when the infanCs behavioral organization indicates his readiness for this sequence and before he or she is exhausted by the tactile inputs During each of the six examination packages the examiner monitors the infants reactions and behaviors along the six systems of functioning listed above
The system parameters are unique to the APIB and go beyond the NBAS assessment They are behavioraHy defined and scaled from i (well-modulated performance) to 9 (disorganized performance) Per package three scores are given for the autonomic motor state organizational and self-regulation sysshytems a baseline score (B) for the infants functioning prior to the adminisshytration of the maneuvers of the package a response score (R) capturing the infants functioning during the administration of the maneuvers of the packshyage and a post package status score (P) describing the infants functioning after the administration of the tasks and before facilitation for the next baseshyline The attentional capacity of the infant is scored in terms of B R and P only during the maneuvers of package VI which are specifically geared to elicit attention and orientation Necessary examiner facilitation is given one score per package The autonomic motor state and self-regulatory systems thus are quantified by 18 scores each (one B R and P score per package) the attentional system by 3 scores (one B R and P score for package VI only) and examiner facilitation by 6 scores one per package yielding a total 0pound 81 scores These 81 scores are reduced to 6 summary scores by forming the mean of the B R and P scores per package for each system These 6 scores are reshyferred to as the system scores and are thought to identify the differential subsystem stability of the infant They are considered to be the key parameters of the APIB and are the measures used in this study
Extensive experience with preterms and specific training is necessary in order to administer and score the APIB reliably Specific reliability criteria are applied They demand above 9800 agreement of all the 9-point scales to within 1 point that is not more than 2 of the 81 scores may be off by 2 points The I-point agreement is set at 9000 that is of the 81 scores 72 must agree to the point For the current study 20 examinations were scored independently by two examiners The overall Pearsons r was 99 Rs ranged from 98 for exshyaminer facilitation to 99 for the five other parameters thus readily meeting the specified interrater reliability criteria In addition to the six system paramshyeters the APIB yields 204 specific scores on detailed aspects of autonomic motor (including reflex performance) state organizational orientation and
311 APIB PRETERM BEHAVIOR
self-regulation functioning of the infant These can be reduced to 26 operashytionally mutually exclusive summary scores (Als 1987) These variables will not be considered in this report
The three gestational age (GA) groups were compared on the six APIB sysshytem parameters Because several of the APIB parameters showed unequal varishyances by Levenes Test for Variances the Brown-Forsythe Equality of Means Test (F$) which does not assume variances to be equal was again employed as it had been for the perinatal background variable exploration described above For all comparisons with significant F$ tests pair-wise I tests with pooled variance were performed between the gestational groups IT and PT IT and PPT and PT and PPT To adjust for the fact that a large number of tests was made these tests were again accompanied by Bonferronis probabilities
Results Table 2 shows the results for the six APIB system variables autonomic organishyzation motoric organization state organization attentional organization self-regulation and examiner facilitation All six system parameters show proshynounced GA group differences The pattern of results across variables is conshysistent On all parameters the full-term group is the most well-modulated well-functioning group The middle-preterm group (PT) takes a middle posishytion and the early-born preterms (PPT) show the most disorganized perforshymance with low threshold to stress and hypersensitive reaction The differshyences are most pronounced between the IT group and the PPT group next between the FT group and the PT group The differences between the PTs and the PPTs do not reach significance Our results indicate that there are consisshytent organizational differences between healthy full-terms and their medically healthy preterm peers when examined at 2 weeks post-term
To delineate specifically the areas of difference the earliest born group (~ 32 weeks GA) shows the greatest difference from the full-term group The PPTs
still show moderate autonomic instability and reactivity moderate motoric disorganization moderate difficulties in self-regulation and considerable difficulties in maintaining alenness They require moderate to considerable facilitation from the examiner in order to regain stabilization In contrast the full-terms show very mild autonomic reactivity and only very mild or occasional motoric disorganization with intermittent difficulty in state regulation and moderate difficulty in maintaining flexible modulated alertness yet quite adeshyquate self-regulation requiring only mild to moderate facilitation from the examiner The middle-group preterms (33-37 weeks GA) show significantly more stress than the Frs on all parameters and are more like the PPTs The APIB system parameters thus are very sensitive to preterm-full-term differshyences in functioning which appear to be still present at 2 weeks beyond due date
Because social-class membership showed significant GA group differences the contribution of social-class status to the APIB results was examined by pershy
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
310 ALS DUFFY AND McANULTY
animate stimuli but only with extreme stress to his autonomic and m010r sysshytem and the infant who has leeway and modulation to do so with animation and without autonomic and motoric stress
The APIB uses the maneuvers of the NBAS as a graded sequence of increasshyingly demanding environmental inputs or packages moving from distal stimulation presented during sleep to tactile stimulation which is gradually paired with vestibular stimulation The social interactive attentional package is administered at the point in the examination when the infanCs behavioral organization indicates his readiness for this sequence and before he or she is exhausted by the tactile inputs During each of the six examination packages the examiner monitors the infants reactions and behaviors along the six systems of functioning listed above
The system parameters are unique to the APIB and go beyond the NBAS assessment They are behavioraHy defined and scaled from i (well-modulated performance) to 9 (disorganized performance) Per package three scores are given for the autonomic motor state organizational and self-regulation sysshytems a baseline score (B) for the infants functioning prior to the adminisshytration of the maneuvers of the package a response score (R) capturing the infants functioning during the administration of the maneuvers of the packshyage and a post package status score (P) describing the infants functioning after the administration of the tasks and before facilitation for the next baseshyline The attentional capacity of the infant is scored in terms of B R and P only during the maneuvers of package VI which are specifically geared to elicit attention and orientation Necessary examiner facilitation is given one score per package The autonomic motor state and self-regulatory systems thus are quantified by 18 scores each (one B R and P score per package) the attentional system by 3 scores (one B R and P score for package VI only) and examiner facilitation by 6 scores one per package yielding a total 0pound 81 scores These 81 scores are reduced to 6 summary scores by forming the mean of the B R and P scores per package for each system These 6 scores are reshyferred to as the system scores and are thought to identify the differential subsystem stability of the infant They are considered to be the key parameters of the APIB and are the measures used in this study
Extensive experience with preterms and specific training is necessary in order to administer and score the APIB reliably Specific reliability criteria are applied They demand above 9800 agreement of all the 9-point scales to within 1 point that is not more than 2 of the 81 scores may be off by 2 points The I-point agreement is set at 9000 that is of the 81 scores 72 must agree to the point For the current study 20 examinations were scored independently by two examiners The overall Pearsons r was 99 Rs ranged from 98 for exshyaminer facilitation to 99 for the five other parameters thus readily meeting the specified interrater reliability criteria In addition to the six system paramshyeters the APIB yields 204 specific scores on detailed aspects of autonomic motor (including reflex performance) state organizational orientation and
311 APIB PRETERM BEHAVIOR
self-regulation functioning of the infant These can be reduced to 26 operashytionally mutually exclusive summary scores (Als 1987) These variables will not be considered in this report
The three gestational age (GA) groups were compared on the six APIB sysshytem parameters Because several of the APIB parameters showed unequal varishyances by Levenes Test for Variances the Brown-Forsythe Equality of Means Test (F$) which does not assume variances to be equal was again employed as it had been for the perinatal background variable exploration described above For all comparisons with significant F$ tests pair-wise I tests with pooled variance were performed between the gestational groups IT and PT IT and PPT and PT and PPT To adjust for the fact that a large number of tests was made these tests were again accompanied by Bonferronis probabilities
Results Table 2 shows the results for the six APIB system variables autonomic organishyzation motoric organization state organization attentional organization self-regulation and examiner facilitation All six system parameters show proshynounced GA group differences The pattern of results across variables is conshysistent On all parameters the full-term group is the most well-modulated well-functioning group The middle-preterm group (PT) takes a middle posishytion and the early-born preterms (PPT) show the most disorganized perforshymance with low threshold to stress and hypersensitive reaction The differshyences are most pronounced between the IT group and the PPT group next between the FT group and the PT group The differences between the PTs and the PPTs do not reach significance Our results indicate that there are consisshytent organizational differences between healthy full-terms and their medically healthy preterm peers when examined at 2 weeks post-term
To delineate specifically the areas of difference the earliest born group (~ 32 weeks GA) shows the greatest difference from the full-term group The PPTs
still show moderate autonomic instability and reactivity moderate motoric disorganization moderate difficulties in self-regulation and considerable difficulties in maintaining alenness They require moderate to considerable facilitation from the examiner in order to regain stabilization In contrast the full-terms show very mild autonomic reactivity and only very mild or occasional motoric disorganization with intermittent difficulty in state regulation and moderate difficulty in maintaining flexible modulated alertness yet quite adeshyquate self-regulation requiring only mild to moderate facilitation from the examiner The middle-group preterms (33-37 weeks GA) show significantly more stress than the Frs on all parameters and are more like the PPTs The APIB system parameters thus are very sensitive to preterm-full-term differshyences in functioning which appear to be still present at 2 weeks beyond due date
Because social-class membership showed significant GA group differences the contribution of social-class status to the APIB results was examined by pershy
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
311 APIB PRETERM BEHAVIOR
self-regulation functioning of the infant These can be reduced to 26 operashytionally mutually exclusive summary scores (Als 1987) These variables will not be considered in this report
The three gestational age (GA) groups were compared on the six APIB sysshytem parameters Because several of the APIB parameters showed unequal varishyances by Levenes Test for Variances the Brown-Forsythe Equality of Means Test (F$) which does not assume variances to be equal was again employed as it had been for the perinatal background variable exploration described above For all comparisons with significant F$ tests pair-wise I tests with pooled variance were performed between the gestational groups IT and PT IT and PPT and PT and PPT To adjust for the fact that a large number of tests was made these tests were again accompanied by Bonferronis probabilities
Results Table 2 shows the results for the six APIB system variables autonomic organishyzation motoric organization state organization attentional organization self-regulation and examiner facilitation All six system parameters show proshynounced GA group differences The pattern of results across variables is conshysistent On all parameters the full-term group is the most well-modulated well-functioning group The middle-preterm group (PT) takes a middle posishytion and the early-born preterms (PPT) show the most disorganized perforshymance with low threshold to stress and hypersensitive reaction The differshyences are most pronounced between the IT group and the PPT group next between the FT group and the PT group The differences between the PTs and the PPTs do not reach significance Our results indicate that there are consisshytent organizational differences between healthy full-terms and their medically healthy preterm peers when examined at 2 weeks post-term
To delineate specifically the areas of difference the earliest born group (~ 32 weeks GA) shows the greatest difference from the full-term group The PPTs
still show moderate autonomic instability and reactivity moderate motoric disorganization moderate difficulties in self-regulation and considerable difficulties in maintaining alenness They require moderate to considerable facilitation from the examiner in order to regain stabilization In contrast the full-terms show very mild autonomic reactivity and only very mild or occasional motoric disorganization with intermittent difficulty in state regulation and moderate difficulty in maintaining flexible modulated alertness yet quite adeshyquate self-regulation requiring only mild to moderate facilitation from the examiner The middle-group preterms (33-37 weeks GA) show significantly more stress than the Frs on all parameters and are more like the PPTs The APIB system parameters thus are very sensitive to preterm-full-term differshyences in functioning which appear to be still present at 2 weeks beyond due date
Because social-class membership showed significant GA group differences the contribution of social-class status to the APIB results was examined by pershy
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
()
TABLE 2 APIB System Variables Means and Standard Deviations (in Parentheses)
Gestational Age Groups Pairwise Comparison p
APIB Variables FT
n=3lt4 PT
n=31 PPT
n=33 Significance
Test P FTPT FTPPT PTPPT
Autonomic organization 267 19 73 3798 bullbullbullbullbull bullbullbullbullbull ns (092) (098) (110)
Matorlc organization 264 418 98 2597 bullbullbullbullbull bullbullbullbullbull ns (131 ) (156) (1 14)
State organization 322 444 475 1471 bullbullbullbullbull bullbullbullbullbull ns
AUentional organization
(142) c87
(126) 583
(094) 668 793 bullbullbull ns ns
Self regulatlon
(210) 377
( 196) 513
(14)
558 1313 bullbullbull ns
Examiner facilitation
(183) c 11
( 150) 538
(111) 576 723middotmiddotmiddotmiddot bullbull shy ns
(1 92) (199) (1 67)
Note FT=fullmiddotterm 38 tocl weeks PT=preterm 33 to 37 weeks PPT=premiddotpreterm 27 to 32 weeks plt05 - plt01 pltOO5bull__ pltOO1 pltOCKlOl
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
313 APia PRETERM BEHAVIOR
forming an analysis of variance with Social Class used as a grouping variable in addition to Gestational Age None of the six APIB parameters showed a significant Social Class effect or a significant Social Class by Gestational Age interaction effect whereas aU six showed strong Gestational Age effects essenshytially identical to those described above It can thus be concluded that social class is not a variable contributing to the APIB differences found by gestational age group
STUDY 2 PROSPECTIVE CLASSIFICATION TEST
Because it is important to establish consistency of the GA group differences across populations we examined an earlier APIB data set of 40 previously studied infants Full-terms numbered 20 and met the medical and demographic selection criteria of the 34 full-terms in Study 1 There were 20 healthy preshyterms with a gestational age of lt 34 weeks They were thus most comparable to the 33 early preterms (PPT) from Study 1 Table 3 shows an overview of their background variables
There were again no differences in maternal age parity or sex distribushytion between the two groups All infants that were selected were Caucasian These 40 infants had been examined with the APIB at both 40 weeks and 44 weeks post conceptional age Table 4 shows the means and standard deviations of the APIB system variables for the two examinations and the results of a repeated-measures ANOVA Given the marked differences between means and the robustness of the F distributions with respect to the influence of non homoshygeneity of population error variances provided that the number of observashytions in the samples is equal (Cochran 1947Kirk 1968) we have chosen the F statistic for repeated-measures design
TABLE 3 Perinatai CharaCteristics of Study 2 Infants Means and Standard Deviations (in Parentheses)
Gestational Age Groups I
FT PT Significance Test Perinatal Variables n=20 n=20 (twotailed)
Gestational age (weeks) 021 3081 197 (059) (275)
Birth weight (gms) 338950 155930 1266 ( 121) (5000)
Apgar I-min 870 530 540 (07) (277)
S-min 915 735 00 (037) (198)
Gestational age ot discharge 4065 3633 87 from hospital (weeks) (057) (221 )
Note FT=fullterm 38 to 1 weeks PT=preterm lt34 weeks bull pltOO1
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
Co)- TABLE 4
APIB System Variables of Study 2 Infonls Meons and Standard Deviations (in Parentheses) of E)(aminations at 40 and 44 Weeks Poslconceplion
ANOVA
0 Weeks Gestational Age Groups
44 Weeks Gestational Age Groups Group Effect Time Effect
Group X Time Interaction Effect
APIB Variables FT
n=20 PT
n=20 FT
n=20 PT
n=20 F F F
Autonomic organization 223 64 209 427 3813middot nI nS (068) (153) (072) (174)
Motor organization 26 55 229 509 6140middot ns ns (089) (138) (084) ( 172)
Stole organization 39 586 271 482 3812 4073middot ns (128) (102) (114) (121)
Attentional organization 642 817 347 642 2481 5398 nS (192) (079) (1 98) (218)
Selfmiddotregulatlon 36 564 293 537 3009 ns ns (126) (151 ) ( 143) (208)
E)(omlner facilitation 353 600 334 6Q4 3183 ns ns (135) (154) (156) (1 98)
Notbull FT=fullmiddoterm 38 to 41 weeks PT=preterm ltM weeks bull pltOOOOI
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
315 APIB PRETERM BEHAVIOR
As for the large sample of Study I all six APIB systems parameters show significant Group effects at both data points Furthermore two of the paramshyeters namely State and Attentional Organization show significant change over time as one might expect (Als 1978) Because the Study I sample was studied at 42 weeks postconception yet data from that age point were not available for the Study 2 infants the mean of the 40- and 44-week data points was formed and utilized as the approximate equivalent of Study 1 The gestashytionaJ age groupings of Study 2 were named FTMN (full-term group mean of two examinations) and PTMN (preterm group mean of two examinations) Table 5 shows the mean values utilized As expected all six showed highly sigshynificant FTIPT differences The plan was to initiate a prospective classificashytion test to see if discrimination rules based upon groups FT and PPT from Study 1 could accurately classify members of groups FTMN and PTMN A training-set test-set procedure was employed Diagnostic rules were generated by the multi group classification aJgorithm CLASIF which uses Geissers equaJ dispersions small samples procedure (Cooley amp Lohnes 1971) This program develops rules and thereby assigns subjects to one of severaJ cateshygories based upon probabilistic measures derived from considerations of varishyance and covariance matrices The six system sheet APIB summary features were used The training-set consisted of FT and PPT and the test-set FfMN and PTMN Surprisingly 100070 of the FTMN (2020) and 90070 of the PTMN (1820) were correctly identified for an overall test-set classification success of 95070 (3840) To be sure the choice of PPT did not overly bias our results we repeated the anaJysis using PPPT (aJl preterms from Study 1 ie PTs and
TABLE 5 APIB System Variables of Study 2 Infants
Means and Standard Deviations (in Parentheses) for the Means of the Examinations at 40 and laquo Weeks Postconception
Gestational Age Groups
FT PT Significance Test APIB Variables n=20 n=20 t (two-tailed)
Autonomic organization
Motoric organization
State organization
AHentional organization
Self-regulation
Examiner focilitation
216 (064) 238
(078) 333
(107) 494
(173) 322
(114) 3laquo
(129)
446 (154)
526 (146) 534
(097) 746
(095) 561
(1laquo) 602
(157)
617middot
779middot
623middot
569middot
584middot
567middot
Note FT=full-term 38 to 41 weeks PT=preterm lt3-4 weeks bull pltOOl
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
316 ALS DUFFY AND McANULTY
PPTs) along with Frs as the training-set Once again prospective test-set classishyfication was successful with FTMN classified 100070 correctly (2020) and PTMN classified 85 correctly (1720) for an overall success of 925070 (3740) It can be concluded that APIB-derived classification rules generated to discriminate full-terms from preterms on one population can accurately disshycriminate on another population The results speak to consistent behavioral differences between full-term and preterm infants as well as the sensitivity of the APIB in measurement of these differences
DISCUSSION
The results of this study lend support to the conclusion that when healthy preshyterm infants reach 2 weeks post-term they are still behaviorally recognizable as preterm infants in contrast to their healthy full-term peers The behavioral difshyferences are strongest with the very early-born preterms (s 32 weeks GA) yet are also apparent between full-terms and 33- to 37-week preterms The APIB system scores which are unique to this newborn assessment appear to be senshysitive to these differences and reliably document them The areas of greatest behavioral difference are in autonomic and motoric functioning next in state organization and self-regulation and then in attentional organization and amount of examiner facilitation needed The differences between the earlyshyborn (ppn and the middle-born (pn preterms are not as pronounced as those between the full-terms and either of the preterm groups The results thus inshydicate the continued reactivity and low threshold to disorganization of the preshyterm groups in responding to their environment that is to a very sensitively administered examination which requires extensive training The earliest-born group showed the most reactivity and sensitivity In contrast the full-terms at 42 weeks were autonomically and motorically stable had good state control were better able to maintain themselves in balance stayed well organized and required much less help from the examiner in doing so They showed relatively greater difficulty in alerting These findings are in keeping with earlier results on full-term newborns (Als 1978) The preterms at 42 weeks still had moderate difficulty with autonomic motor and state organization and considerable difficulty coming to a steady focused alert state They displayed much more autonomic lability motoric stress signals and an inability to come to a robust crying state and needed much more facilitation from the examiner This is in keeping with the results reported by Ferrari et ale (1983) and Sell et ale (1980) and it stands in contrast to the fmdings by Paludetto et ale (1982) The use of the APIB system variables appears to yield robust preterm-full-term differshyences as was shown in the successful prospective classification test with a secshyond set of data The results point to the usefulness of the APIB in identifying reliably the continued differences in neurobehavioral organization of preterm and full-term infants and in highlighting the hypersensitivity of the preterm
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
317 APIB PRETERM BEHAVIOR
infants even beyond term and even when selected to be medically noncom proshymised
The etiology of the behavioral differences in healthy preterm and full-term newborns is uncertain at this point The immaturity of the early-born brain in exposure to the sensory environment of the intensive care unit and the extrashyuterine world at large may be at least a partial cause for the differences obshyserved in early behavioral functioning (Duffy Mower Jensen amp Als 1984) This hypothesis is currently being investigated further Differences in brain structure due to early subtle fetal insults also cannot be ruled out at this point
The implications of these findings are that preterms even after a benign hospital course will present different behavioral pictures to their interactors and make different demands on their caregivers than full-term infants These differences appear to be due to gestational age at birth per se and not due to social class This needs to be kept in mind in providing anticipatory guidance to the parents and caregivers of preterms who are often encouraged to think of their preterm infants as having caught up when they have reached the exshypected due date It appears that catching up has not happened by 2 weeks after due date and may in fact be a misleading expectation The APIB might be a useful instrument in helping parents gain confidence in the reading of their infants cues and staying aware of their continued fragility and low threshshyold of reactivity
REFERENCES
Abt K (1983) Significance testing of many variables-Problems and solutions Neuropsychoshybiology 9 47-51
Als H (1978) Assessing an assessment In A Sameroff (Ed) Organization and stability of newshyborn behavior A commentary on the Brazelton Neonatal Behavioral Assessment Scale Monograph oj the Society jor Research in Child Development 4] 14-29
Als H (1982) Towards a synactive theory of development Promise for the assessment of infant individuality Infant Mental Health Journal 3 229-243
Als H (1983) Infant individuality Assessing patterns of very early development In F Call E Galenson amp RL Tyson (Eds) Frontiers in infant psychiatry New York Basic Books
Als H (1985) Patterns of infant behavior Analogs of later organizational difficulties In FH Duffy amp N Geschwind (Eds) Dyslexia A neuroscientific approach to clinical evaluation Boston Little Brown
Als H (1987) APIBjeatures Summary variables (rev cd) Unpublished manuscript ChildrenS Hospital Boston
Als H t amp Brazelton TB (1981) A new model of assessing the behavioral organization in preshyterm and full-term infants Two case studies Journal oj the American Academy ojChild Psychiatry 20 239-269
Als H bull Lester BM Tronick EC amp Brazelton TB (l982a) Manual for the assessment of preterm infants behavior (APIB) In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics (Vol J) New York Plenum
Als H bull Lester BM Tronick E amp Brazelton TB (1982b) Towards a research instrument for the assessment of preterm infants behavior In HE Fitzgerald BM Lester amp MW Yogman (Eds) Theory and research in behavioral pediatrics New York Plenum
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
318 ALS DUFFY AND McANULTY
Brazelton TB (1973) Neonatal Behavioral Assessment Scale Clinics in developmental medicine No 50 Philadelphia Lippincott
Brown MB bull amp ForsYthe AB (1974) The small sample behavior of some statistics which leSI the equality of several means Tlaquohnometrics 16 J29-132
Cochran WG (1947) Some consequences when the assumptions for the analysis of variance areshynot satisfied Biomefrics J 22-38
Cooley WWbull amp Lohnes PR (1971) Multivariate data analysis New York Wiley Dubowitz L bullbull Dubowitz V amp Goldberg C (1970) Clinical assessment of gestational age- in the
newborn infant Journal oJ Pediatrics 77 1-10 Duffy FH Mower GDbull Jensen F bull amp Als H (1984) Neural plasticity A new frontier for
infant development In HE Fitzgerald BM Lester amp M W Yogman (Eds) Theory and research in behavioral pediatrics (Vol II) New York Plenum
Feller W (1957) An introduction to probability theory and its applications New York Wiley Ferrari F Grosoli M V bull Fontana Gbull amp Cavazzuti GB (1983) Neurobehavioral comparison
of low-risk pretenn and full-tenn infants at term conceptual age Developmental Medicine ad Child Neurology 25 450-458
Hollingshead AB (1975 June) Four-Jactor index oJsocial status Working paper Yale Univer- sity New Haven CT
Kirk RE (1968) Experimental design Proceduresor the social sciences Belmont CA Brooksl Cole
Levene H (1960) Robust tests for equality of variance In I OIkin (Ed) Contributions to probshyability statistics Palo Alto CA Stanford University Press
Minde K Perroua M amp Manon P (1985) Maternal caretaking and play with full-tenn and premature infants Journal 0 Child Psychology and Psychiatry 26 231-244
Paludetto R Mansi G Rinaldi P DeLuca T bullbull Corchia G bull De-Curtis M bull amp Andolfi M (1982) Behavior of preterm newborns reaching tenn without any serious disorder Early Human Development 6 357-363
Sell EJ Luick A bull Poisson SS bull amp Hill S (1980) Outcome of very low binhweight (VLBW) infants I Neonatal behavior of 188 infants Developmental and Behavioral Pediatrics I 78-85
1 February 1988 Revised 25 April 1988 bull
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