development of swallowing and feeding

7/29/2019 Development of Swallowing and Feeding

1/13

DEVELOPMENT OF SWALLOWING AND FEEDING:

PRENATAL THROUGH FIRST YEAR OF LIFE

Amy L. Delaney1* and Joan C. Arvedson2

1Childrens Hospital of Wisconsin-Milwaukee, University of Wisconsin-Madison, Madison, Wisconsin2Childrens Hospital of Wisconsin-Milwaukee, Medical College of Wisconsin-Milwaukee, Milwaukee, Wisconsin

The development of feeding and swallowing involves a highly com-plex set of interactions that begin in embryologic and fetal periods andcontinue through infancy and early childhood. This article will focus onswallowing and feeding development in infants who are developing nor-

mally with a review of some aspects of prenatal development that providea basis for in utero sucking and swallowing. Non-nutritive sucking inhealthy preterm infants, nipple feeding in preterm and term infants, andselected processes of continued development of oral skills for feedingthroughout the first year of life will be discussed. Advances in researchhave provided new information in our understanding of the neurophysiol-ogy related to swallowing, premature infants sucking and swallowingpatterns, and changes in patterns from preterm to near term to terminfants. Oral skill development as texture changes are made throughoutthe second half of the first year of life is an under studied phenomenon.Knowledge of normal developmental progression is essential for profes-sionals to appreciate differences from normal in infants and children withfeeding and swallowing disorders. Additional research of infants and chil-dren who demonstrate overall typical development in oral skills for feed-ing is encouraged and will provide helpful reference points in increasingunderstanding of children who exhibit differences from typical develop-ment. It is hoped that new technology will provide noninvasive means of

delineating all phases of sucking and swallowing from prenatal throughinfancy. Further related topics in other articles of this issue provide a com-prehensive review of factors influencing oral intake, growth, nutrition,and neurodevelopmental status of children. '2008 Wiley-Liss, Inc.Dev Disabil Res Rev 2008;14:105117.

Key Words: infant; child; development; feeding; swallowing; sucking;

neurobiology

DEVELOPMENT OF SWALLOWING ANDFEEDING: PRENATAL THROUGH FIRST

YEAR OF LIFE

Adequate respiration and nutrition are essential for allliving creatures. Successful and safe oral feeding inneonates and young infants requires well coordinated

sucking, swallowing, and breathing sequencing. Breathing typ-ically does not require active effort by infants except for thosewith complicating factors that may include, but are not limitedto, bronchopulmonary dysplasia, upper airway obstruction asin Pierre Robin sequence and other craniofacial anomalies,and severe laryngotracheomalacia. Swallowing or deglutitionincludes the entire act from food placement in the mouthuntil the material enters into the stomach [Dodds, 1989;Dodds et al., 1989; Logemann, 1998]. Logemann [1998]

stressed that feeding (or eating) is distinct from swallowing.Eating is primarily an oral phase function that includes oralpreparation and oral transit of a bolus. Feeding is described as

specific to anticipatory reactions, food getting, the placementof food in the mouth, and bolus management, includingchewing (mastication) if necessary and the transfer of the boluswith the tongue into the pharynx. In addition, feeding is abroader term that includes the interactions between childrenand their caregivers. Eating/feeding requires active effort byinfants who must have exquisite timing and coordination ofsucking, swallowing, and breathing to be efficient. Adequategrowth, defined by appropriate weight gain in early infancy andfor the first few years of life, is a primary measure of successfulfeeding. An infant should take feedings efficiently in about 20to no more than 30 min without stress to infant or feeder sothat the infant consumes sufficient volume to gain weightappropriately. It is expected that infants feed at intervals of at

least 23 hr from the start of one feeding to the start of thenext feeding. This time interval is an important factor in thefacilitation of hunger, satiation at end of the feeding period,digestion, and promotion of the next cycle. Infants need tofeed efficiently and safely to maintain stable respiratory healthand to make appropriate developmental gains over time.

Professionals involved with assessment and treatment ofinfants and children with feeding and swallowing deficits musthave a thorough understanding of embryologic and develop-mental anatomy of the upper aerodigestive tract and the nor-mal physiology of deglutition [e.g., Miller, 1982, 1999; Arved-son and Brodsky, 2002]. Research in recent years has added tothe understanding of the development of feeding and swallow-ing in utero and continuing through infancy [e.g., Ross and

Nyland, 1998; Gewolb et al., 2001a,b,c; Qureshi et al., 2002;Miller et al., 2003, 2006].

Normal sucking, swallowing, and breathing sequencingrequires integration of multiple afferent and efferent systems inthe central nervous system (CNS). The most complex human

*Correspondence to: Amy L. Delaney, Childrens Hospital of Wisconsin, 9000 W.Wisconsin Ave, PO Box 1997, MS #785, Milwaukee, WI 53201-1997.E-mail: [email protected] 23 May 2008; Accepted 23 May 2008Published online in Wiley InterScience (www.interscience.wiley.com).DOI: 10.1002/ddrr.16

DEVELOPMENTAL DISABILITIES

RESEARCH REVIEWS 14: 105117 (2008)

' 2008 Wiley -Liss, Inc.


2/13

neuromuscular unit in the body is theupper aerodigestive tract that acts as aconduit for passage of air and food.Feeding and swallowing are the activ-ities through which parents and careproviders first assess the overall healthand neurodevelopmental well-being ofneonates and young infants. In addition,normal feeding patterns reflect the early

developmental pathways that are thebasis for later communication skills. Theinterrelationship between feeding (in allliving beings) and complex verbal com-munication (unique to humans) is mul-tifactorial and in need of continuedresearch. The study of comparativeanatomy and its implications for humancommunication are well described[Laitman and Reidenberg, 1993] andwill not be discussed further here. Theneurobiology of deglutition is discussedby Arthur Miller and the neurophysiol-ogy of hunger and satiety is discussed

by Pauline Smith and Alastair Fergusonin this issue.

The purpose of this review is todescribe some aspects of developmentof normal feeding and swallowing fromprenatal periods through infancy. Topicsinclude the following: (1) prenatal de-velopment of sucking, swallowing, andbreathing coordination that is an impor-tant underpinning for oral feeding inpreterm and term infants; (2) develop-mental progression of oral feeding skillsat the breast or by bottle and nipple inneonates and young infants; (3) oral

feeding skill development in the secondhalf of the first year of life. Transitionfeeding skills emerge in typically devel-oping infants by about 6 months of age,at which time spoon feeding may beintroduced. Overall developmental skilllevels, not chronologic age, must betaken into account when one considersexpectations for advancement of tex-tures [e.g., Rogers and Arvedson,2005]. The critical need for understand-ing the anatomy of the oral/pharyn-geal/laryngeal/esophageal mechanism

and the physiology of deglutition can-not be overstated, although that is not amajor focus for this review. Pediatricspecialists working with infants andchildren with diverse feeding and swal-lowing problems must keep develop-mental milestones of typically develop-ing infants and children in mind inorder to carry out evaluations that result

in optimal management decisions foreach unique child.

PRENATAL DEVELOPMENT OFSUCK, SWALLOW, ANDRESPIRATION

The development of sucking andswallowing can be appreciated first byunderstanding the context of develop-mental changes in the embryonic (first8 weeks of gestation) and fetal (week 9to birth) periods. The neurodevelop-mental maturation of cerebral andbrainstem pathways involved in swal-

lowing underlie and contribute to thereadiness for oral feeding. The processeswill be discussed in relation to healthypreterm and term infants.

Prenatal Age Estimations (AdjustedAge)

Professionals need to keep prena-tal age estimations in mind when settingskill level expectations for preterminfants readiness to feed orally and toadvance textures over time, given thatages of preterm infants are typicallyadjusted to the prenatal age estimate for

the first 24 months of life. It is commonto refer to the number of weeks in fetaldevelopment as postconceptual age(PCA) relating to the estimated day offertilization (fertilization age) or as post-menstrual age (PMA) relating to thefirst day of the last normal menstrualperiod (gestational age) [Moore andPersaud, 2003]. PCA is expected to be2 weeks shorter than PMA. Theremay be confusion when age is describedin months, especially when it is notknown whether calendar months

(2831 days) or lunar months (28 days)are meant. However, it is more com-mon for these ages to be described inmonths.

Relevant Embryologic and FetalDevelopment

Embryonic period (weeks 18)All major organs and systems

form from three germ layers beginningthe fourth through the eighth week ofgestation making this the most criticalperiod of prenatal development. Theanatomy of the oral cavity, pharynx,larynx, and esophagus is the result ofembryologic processes that begin at fer-tilization of the ovum and continue af-ter birth. The beginnings of most essen-tial external and internal structures areformed during this period. Table 1describes a few key processes relevant to

swallowing development. A humanappearance is evident by the end of the8th week. Disturbances during this pe-riod may give rise to major congenitalanomalies.

Fetal period (week 9 to birth)The fetal period is marked by

rapid body growth from the 9th weekto birth. Head growth is relatively slowcompared to growth in the rest of thebody. Differentiation of tissues andorgans continues [e.g., Moore and Pre-saud, 2003]. During this period, the fe-

tus undergoes dramatic development ofswallowing, sucking, and oral sensori-motor function. The oral cavity, phar-

ynx, and esophagus are three distinctanatomic regions that can function sep-arately but, in swallowing, they inte-grate their functions via a neuronal net-work. The anatomy and physiology ofnormal swallowing is well described ina number of resources [e.g., Bosma,1986; Miller, 1999; Arvedson andBrodsky, 2002]. A highly complex andintegrated sensorimotor system provides

Table 1. Selected Processes in Embryologic Period Relevant to Swallow Development

Number of Weeks Gestation Process Role in Swallowing

45 Endoderm of yolk sac incorporated into embryo toform primordial gut

Basis for separate esophagus and trachea

4 Mandible via 1st branchial arch Growth important for tongue position and soft palate fusion6 Oropharyngeal membrane ruptures to form

primitive choanae allowing for nasal breathingNasal breathing critical for efficient nipple feeding (breast or

bottle)67 Separation of esophagus and trachea from the

primitive foregutAllows for liquid to move through esophagus without

aspiration

Adapted from Moore and Persaud, 2003.

106 Dev Disabil Res Rev

DEVELOPMENT OF SWALLOWING AND FEEDING

DELANEY AND ARVEDSON


3/13

the foundation for functional sucking,swallowing, and breathing.

Neurobiology of Oral Feeding andSwallowing

Cerebral and brainstem pathwaysinvolved in oral sensorimotor functionand swallowing [e.g., Yakovlev andLecours, 1967; Brody et al., 1987; Kinneyet al., 1988] as well as respiration

[Carroll, 2003] undergo developmentalmaturation during the fetal period,which continues after birth. Control ofswallowing occurs via multiple levels ofthe nervous system [Miller, 1999].

Brainstem and cranial nerve developmentThe brain stem shows myelination

at 1824 weeks gestation. Roots of anumber of cranial nerves (CN) are my-elinated during 2024 weeks gestation:III (oculomotor), IV (trochlear), VI(abducens), as well as the intramedullaryroots of cranial nerves VII (facial), IX

(glossopharyngeal), and XII (hypo-glossal). These changes correspond withthe appearance of opening and closingof the jaw, anterior tongue movements,and suckling seen on ultrasound imag-ing after 18 weeks gestation [Milleret al., 2003].

Peak synaptogenesis of the me-dulla is seen at 3436 weeks gestation.By 3538 weeks, the nervous systemmatures sufficiently to carry out someintegrative functions to include nipplefeeding as term approaches.

Sensory systems relevant to oral feedingSensory (afferent) cranial nerve

input to the brain-stem swallowing cen-ters is provided primarily by CN V,VII, IX, and X. The oral-pharyngealregion has one of the richest and mostdiverse sensory inputs of the entirebody [Miller, 1999]. Oral sensationoccurs via a range of modalities thatinclude taste, somesthetic sensitivity,two-point discrimination, oral stereog-nosis, vibrotactile detection, proprio-ception, nociception, and chemical andthermal sensitivity. Detailed descriptions

of each modality with its neural inner-vation and function can be found inMiller [1999 pp 1333]. A variety ofsensory attributes are integral to oral-motor function to prepare liquid andfood for swallowing.

Taste is one of the most complexsensations evoked from the oral-pharyn-geal region. Miller [1999] suggests thatperception of taste may be more a flavorthan true taste since different modalitiescontribute to taste perception. Thesemodalities include smell, touch, texture,

temperature, and the chemical sense oftaste [Linden, 1993]. Taste and tactilesensation in oral regions is well devel-oped in fetal rats and sheep [Mistretta,1972; Bradley and Mistretta, 1973].Sensory fibers responding to taste syn-apse in the rostral nucleus tractus soli-tarius (NTS). Taste buds develop duringweeks 1113 in the human fetus, mostforming on the dorsal surface of the

tongue, with some on the palatoglossalarches, palate, posterior surface of theepiglottis, and the posterior wall of theoropharynx. Stimulation of variousnerve branches that innervate thetongue, including glossopharyngealnerve, along with the lingual branch andthe chorda tympani branch of the tri-geminal nerve, evokes potentials in therostral region of the NTS [Blomquistand Antem, 1965]. Neurons respondingto gustatory stimulation in the rat arealso found in the rostral region of theNTS [Travers and Norgren, 1986]. Gus-

tatory neurons are organized topograph-ically. The majority of the NTS inter-neurons discharge to stimulation of tastebuds in specific regions.

The oral, pharyngeal, and esopha-geal regions are innervated by fibers thatrespond to noxious stimuli. In humans,the highest density of neural receptorsthat respond to noxious stimuli islocated around the mouth and nose[Miller, 1999]. Myelinated to unmyeli-nated fiber ratio is relatively high in thetrigeminal nerve, which suggests thatmore myelinated fibers are involved in

innervating these receptors than in otherparts of the body [Miller, 1999]. Like-wise, the oral and pharyngeal regionshave numerous sensory fibers respondingto changes in temperature [e.g., Storey,1968a,b; Poulos and Lende 1970a,b].Mechanical stimuli (touch and pressure)are perceived over many more regionsof the oral cavity than are thermal stim-uli with the tongue having a high den-sity of mechanosensitive neurons.

Motor systems relevant to oral feedingPrimary motor (efferent) cranial

nerve input to the brain-stem swallowingcenters is provided primarily by CN V,VII, IX, X, XII, and the upper cervical(C1C3) nerves. Central pattern genera-tors in specific regions of the brain stemappear to control movements of mastica-tion, respiration, and swallowing.

Development of the brain stemnetwork of interneurons controlling thepharyngeal phase of swallowing appearsto reach a functional level in the fetus[Miller, 1999]. Pharyngeal swallowing isone of the first motor responses that

uses pharyngeal muscles and appears inthe fetal lamb [Bradley and Mistretta,1973], in the fetal monkey [Minei andSuzuki, 1976], and in the human fetusby the 11th week [Hooker, 1954]. Thehuman fetus shows activity in thetongue at about the same time as the

jaw-opening reflex.Central pattern generators are

modulated by suprabulbar regions and

sensory feedback [Miller, 1999]. Swal-lowing can be evoked by multiple cen-tral pathways even after removal of theentire cortical and subcortical regionsabove the brain stem, which indicatesthat the cerebral cortex is not essentialto the pharyngeal and esophageal phases[Miller, 1982]. The cerebral cortex doesappear to facilitate the oral phase andthe initiation of the pharyngeal phase,which requires exquisite timing of res-piration and swallowing.

The relationship between the tim-ing of respiration and swallowing has

been studied via transynatic neural trac-ers (cholera toxin horseradish peroxidase[CT-HRP] and pseudorabies virus[PRV]) that effectively label afferent ter-minal fields within the nucleus of thesolitary tract (NTS) as well as swallow-ing motor neurons and their dentriticfields within the nucleus ambiguous(NA), dorsal motor nucleus (DMN),and the hypoglossal nucleus (XII)[Broussard and Altschuler, 2000a,b;Altschuler, 2001]. These authors statedthat their data provide an anatomic basisfor interaction of swallowing motoneur-

ons with premotor neurons located inthe area of NA. Motoneurons that in-nervate all levels of the esophagus areconfined to the compact formation(NAc). While the motoneurons projec-ting to the pharynx and cricothyroidmuscles are located in the semicompactformation (NAsc), extensive bundlingof motoneuronal dendrites within theNA supports the hypothesis that thesestructures serve as networks for the gen-eration of complex motor activities,such as swallowing [Broussard andAltschuler, 2000b]. A subpopulaton of

neurons in intermediate and interstitialsubnuclei of the NTS projects to pha-ryngeal motoneurons and buccophar-

yngeal PMNs and is synaptically linkedto esophageal peripheral motor neurons(PMNs). This link between buccophar-

yngeal and esophageal PMNs provides apotential anatomic substrate within theNTS for the central integration ofesophageal peristalsis with the pharyn-geal phase of swallowing and airway-protective reflexes. Both human studiesand animal models that investigate

Dev Disabil Res Rev


DELANEY AND ARVEDSON 107


4/13

esophagoglottal closure and pharyngo-upper esophageal sphincter (pharyngo-UES) contractile reflexes have locatedthe neural pathways that mediate airwayprotective reflexes. Additional researchusing this same paradigm may help todemonstrate the central integration ofswallowing and airway protectivereflexes in infants and young children aswell as adults [Broussard and Altschuler,

2000a].

Effect of decreased sensory input on motorfunction

Short-term decrease in oropha-ryngeal sensory input to adults has beenshown to impede cortical control forswallowing through magnetoencepha-lography (MEG) [Teismann et al.,2007]. Teismann et al. found decreasedmotor activation apart from a stronglyreduced sensory representation. Signifi-cantly increased swallowing relatedmuscle activation during an anesthesia

was found compared to swallowingwithout anesthesia. Up to about 10

years ago many thought that swallowingwas coordinated only by the brainstem.Functional brain imaging methods haveproved the influence of several corticalareas on deglutition [Hamdy et al.,1999; Mosier et al., 1999; Dziewaset al., 2003]. Although this line ofresearch is with adults, it is hoped thatsimilar research paradigms may aid inincreasing understanding of the devel-oping brain.

Sensory input for infants. Breathing, suck-ing, and swallowing activities occur inthe upper aerodigestive tract and areorchestrated by specific areas in theCNS. When pharyngeal and laryngotra-cheal sensation is reduced, aspiration islikely to occur with no overt manifesta-tions, that is, silent aspiration. Researchfindings have challenged the assumptionthat healthy newborn infants coughwith aspiration [Perkett and Vaughan,1982; Pickens et al., 1988]. Predomi-nant responses of sleeping infants stimu-lated by introduction of a small bolus

(0.1 ml) of water or saline into thepharynx via a nasal catheter are swal-lowing, apnea, and laryngeal closure.Coughing is rare [Pickens et al., 1988].Research on neonatal development ofcough involves studies of the laryngealchemoreflexes (LCR) that are stimu-lated by fluid contacting the mucosa ofthe larynx. These reflexes are initiatedin the fetus and newborn when hypo-chloremic or strongly acidic solutionscontact the epithelium that surroundsthe entrance to the laryngeal airway

[Thach, 2001]. The LCRs include star-tle, rapid swallowing, apnea, laryngealconstriction, hypertension, and brady-cardia. Several responses make up theLCR reflex. The most commonresponse is one or more swallows,slightly less common is apnea that mayor may not be accompanied by laryn-geal closure as inspiratory efforts areobstructed. The probability of a cough

response increases in frequency withmaturation. As the infant matures, rapidswallowing and apnea become less pro-nounced, whereas cough and possiblylaryngeal constriction become moreprominent. This transformation relatesprimarily to central neural processingrather than to changes in the airwaymucosal water receptors that initiatethe reflex [Thach, 2001, 2007]. Clini-cians must keep these findings in mindduring interpretation of instrumentalswallow examinations for young infantsduring which there may be occasional

trace silent aspiration. In some instances,this may not necessarily be a majorproblem. Further data are needed, par-ticularly outcomes data on infants whocontinue to feed orally.

Prenatal Sucking, Swallowing,and Breathing

Ultrasound studies of fetuses haverevealed early development of swallow-ing and oral sensorimotor function[e.g., Ross and Nyland, 1998; Milleret al., 2003]. Fetal swallowing is impor-tant for the regulation of amniotic fluid

volume and composition, recirculationof solutes from the fetal environment,and maturation of the fetal gastrointesti-nal tract [Ross and Nyland, 1998]. Thepharyngeal swallow is one of the firstmotor responses in the pharynx and hasbeen reported between 10 and 14weeks gestation [Humphrey, 1967;Devries et al., 1985; Cajal, 1996].Ultrasound studies reveal non-nutritivesucking and swallowing in most fetusesby 15 weeks gestation. The fetusabsorbs some amniotic fluid after swal-lowing it. A suckling response may be

elicited at this stage as reported in spon-taneously aborted fetuses [Moore andPersaud, 2003]. Forward tongue thrust-ing has been reported by 21 weeks ges-tation, tongue cupping at 28 weeks ges-tation, and suckling (anterior-posteriortongue movements) between 18 and 24weeks gestation. Self oral-facial stimula-tion is shown to precede suckling andswallowing [Miller et al., 2003]. Con-sistent swallowing is seen by 2224weeks gestation [Miller et al., 2003].The near term fetus swallows amniotic

fluid at a volume of about 5001,000ml/day [Ross and Nyland, 1998].

Substantial weight gain occursfrom 21 to 25 weeks. By 24 weeks, sur-factant is being secreted to maintain thepatency of the developing alveoli of thelungs. The respiratory system is stillimmature and may not be viable (viabil-ity is defined as the ability of a fetus tosurvive in the extrauterine environ-

ment).By 2629 weeks, the lungs are ca-

pable of breathing air. The CNS candirect rhythmic breathing movementsand control body temperature by thisperiod. Fetal responses can be inducedby bitter-tasting substances at 2628weeks, indicating that reflex pathwaysare established between taste buds andfacial muscles. [Moore and Persaud,2003]. Taste can alter frequency ofsuckling motions.

Sex-related differences across 2ndand 3rd trimesters are found for early

oral, lingual, pharyngeal, and laryngealmotor activities via sonographic imagesof 85 healthy fetuses at 24 weeks 3 days(SD 0.69) [Miller et al., 2006]. Males(N5 43) and females (N5 42) dem-onstrated statistically similar patterns ofgeneral physical growth, but significantdifferences were found in developmentof specific lingual and pharyngeal struc-tures, laryngeal and pharyngeal motoractivity, and oral-lingual movements.Complex oral-motor and upper airwayskills emerged earlier in females, sug-gesting a sex-specific trajectory of

motor development [Miller et al.,2006]. Pharyngeal and laryngeal move-ments in males were less rhythmic andcomplete than in females throughoutthe second trimester. By the third tri-mester, these movements became moresimilar. Overall, females attained oral-motor skills at earlier stages of prenatalmaturation. These authors concludedthat differential patterns of prenatalmotor development may be importantin defining sex-specific indices of oralskill maturation. Additional data areneeded.

Preterm infant feedingA normal-weight fetus born at 32

weeks is premature by date asopposed to premature by weight[Moore and Persaud, 2003]. A healthypreterm delivery may result in total oralfeeding by 34 weeks gestation. Growthslows as the fetus nears term. Infantsdelivered in this near-term period aretypically total oral feeders, althoughsome show evidence of mild disorgani-zation of sucking, swallowing, and





5/13

breathing coordination for the first cou-ple weeks of life. The course towardoral feeding is different in preterminfants delivered at shorter gestation.

Preterm infant feeding developmentThe first concerns following pre-

term delivery relate to stabilization ofrespiration to support life. Infants with-

out major cardiorespiratory or GI tractdeficits are appropriate for introductionto non-nutritive sucking, usually viapacifier, as early as 2829 weeks PCA.Some infants who are intubated orallyare noted on ulstrasound to suck on thetube, likely a continuation of suckingthat is noted in utero as the fetus can beseen to suck fingers or suck on thetongue.

Non-nutritive sucking: Indicator of oralfeeding readiness in preterm infants

One of the most complicated

tasks required of a newborn infant isoral feeding that involves complex inte-gration of anatomic structures toinclude lips, jaw, cheeks, tongue, palate,pharynx, and larynx. Coordinatedrhythmic sequences of sucking, swal-lowing, and breathing are required ofinfants whether they are breast- or bot-

tle-fed. The survival rates of preterminfants have improved significantly inrecent years, but one of the most com-mon and urgent care issue that contin-ues, is the subject of when and how toinitiate and to advance oral feedings.The ability to make a transition fromgavage to oral feeding depends on neu-rodevelopmental status related to behav-

ioral organization (Table 2), to cardio-respiratory regulation, and to the abilityto produce a rhythmic suck-swallow-breathe pattern. Healthy term infantshave that ability, but preterm infants lessthan 32 weeks PCA are neurologicallyimmature and rarely they are capable ofthat coordination. Preterm infants canbecome stressed with bottle feeding forseveral reasons to include, but not lim-ited to, (1) neurological immaturity, (2)difficulty regulating autonomic func-tions, and (3) difficulty achieving be-havioral state organization when they

are presented with stimuli [Als andBrazelton, 1981; Brazelton and Nugent,1995]. Oral feeding is usually optimalwhen an infant is drowsy, in a quietawake and alert state, or actively awakeand aroused. When an infant is in deepsleep (seldom seen in preterm infants)or in light sleep, on one hand, or highly

aroused or agitated on the other hand,feedings do not typically go smoothlyand easily because the behaviors inter-fere with suck, swallow, and breathesequencing.

Non-nutritive sucking (NNS)success is commonly used as one of themarkers of readiness for an infant tofeed by bottle [Pinelli and Symington,2001], although only a few studies have

examined the relationships between thecharacteristics of NNS and nutritivesucking (NS). Most infants are givenNNS experiences via pacifier. Studieshave demonstrated positive effects of NNSvia pacifier in multiple ways (Table 3).Fucile et al. [2002] reported that theirexperimental group of preterm infantsreached independent oral feeding 1week earlier than a sham group with nointervention when specific stimulationof oral structures was carried out for 15min once per day for 10 days starting48 hr after discontinuation of CPAP.

However, there was no difference inlength of stay between the two groups.Similarly, Bragelien et al. [2008] re-ported that a stimulation program didnot result in earlier weaning from NGtube feedings in premature infants orearlier discharge when compared tosimilar infants with no intervention. Itwould be of interest to have a compari-son group receiving some other type ofhands on intervention, e.g., soothingtouch to other body parts with a ques-tion of potential for facilitating oralfeeding. This comparison has been

shown for reducing pain during heelstick with saturation levels maintainedsignificantly better in Yakson (a tradi-tional Korean touching method) andNNS group compared to control groupneonates [Im et al., 2008]. Theseauthors found no difference among thegroups with regard to heart rate and

Table 2. Infant Readiness for Oral Feeding on Basis ofBehavioral Organization States

State Behavioral Organization State Related to Feeding Readiness

1 Deep sleep, seldom seen in a preterm infant2 Light sleep3a Drowsy4a Quiet awake and/or alert5a Actively awake and aroused6 Highly aroused, agitated, upset and/or crying

aBehavioral organization states optimal for oral feeding. Adapted from Als, 1985, 1986; Brazelton and Nugent, 1995.

Table 3. Outcomes Associated with NNS via Pacifier for Preterm Infants

Authors Outcome

Pa ludetto et a l., 1984 Increased transcutaneous oxygen tension bet ween 32 and 35 weeks gestationBurroughs et al., 1978 Promoting oxygenationTreloar, 1994 Higher transcutaneous oxygen tensions [tcPO2s] after crying induced by heelstickField and Goldson, 1984; South et al., 2005; Im et al.,

2008Soothing during invasive procedures (less fussing and crying); Pain reduction during heel

stick procedureField et al., 1982; Gaebler and Hanzlik, 1996 Shorter transition from tube to oral feeding; shorter hospital stayBernbaum et al., 1983 Matur ing suck pattern, enhanced growth and maturationMeasel and Anderson, 1979 Improved digestion by s imulating the natural way nutrients are ingestedField et al., 1982 Weight gainDiPietro et al., 1994; McCain, 1995 Regulating state and facilitating optimal behavioral state for feedingStandley, 2003 NNS with music significantly increased feeding ratePickler and Reyna, 2004 Prefeeding NNS had no effect on NS, breathing during feeding, or select behavioral

characteristics of feeding

Dev Disabil Res Rev




6/13

pain measured by the Neonatal InfantPain Scale, but they did not use anymeasures to compare oral feedingaspects.

Comparison of non-nutritive and nutritivesucking in a preterm infant

In contrast to previously heldbeliefs, Miller and Kang [2007] reportedthat lingual patterns on ultrasound

showed significantly greater displace-ments and excursions when a preterminfant was sucking for nutritive pur-poses (NS) compared to NNS on a pac-ifier. The angle of the hyoid movementwas significantly greater with NS thanwith NNS. Vertical tongue body excur-sions occurred similar to those previ-ously considered at 69 month develop-mental skill levels. These authors sug-gested that technical advances innoninvasive ultrasound imaging techni-ques with integration of semiautomaticcomputerized analyses of tongue surface

configurations and hyoid activity pro-vide means to enhance knowledge oforal swallowing function in early phasesof preterm infant development.

Facilitation of oral feeding (breast and bottle)The movements of non-nutritive

sucking and swallowing in preterminfants are characterized by organizedbursts of lingual movement separated bybrief pauses in motor activity [Wolff,1968; Daniels et al., 1986]. Thesemovements represent ontogenetic matu-ration of morphologic and neurological

systems [Hafstrom and Kjellmer, 2000;Miller et al., 2003]. The readiness fororal feeding is related to behavioral stateorganization [Als, 1985, 1986] (Table2), to a rhythmic suck-swallow-breathepattern, and to cardiorespiratory regula-tion [McCain, 2003]. Some infants doappear ready to begin oral feeding at3233 weeks gestation [Cagan, 1995;McCain, 2003], although 34 weeks ges-tation is often used as the lower limit ofexpectations for full oral intake to meetnutrition and hydration needs.

Developmental patterns of rhyth-

mic sucking and swallowing in preterminfants have been outlined by Gewolbet al. [2001a] who used intranipple andpharyngeal pressure recordings. Theyfound that swallow rhythm is establishedas early as 32 weeks PMA and does notchange through 40 weeks PMA.Although the swallow rhythm does notchange, the stability of the suck rhythmincreases steadily from 32 to 40 weeksPMA. At 32 weeks PMA, sucking israpid and of low amplitude, not linkedto swallowing. By 33 weeks PMA,

sucking is irregular with an average of23 sucks per sec and not linked withswallowing. Transitions occur duringweek 34. From 35 to 40 weeks PMA,infants have well-defined sucks occur-ring at 1 suck per sec and suck/swallowsequences appear well established. Theratio of 1 suck to 1 swallow predomi-nates in infants until they are beyond 40weeks PMA. At that age it is not un-

usual for 23 sucks per swallow tooccur [Qureshi et al., 2002]. Thesechanges may reflect a pattern of matura-tion representing the process of enceph-alization with infants maturing to altertheir feeding strategies qualitatively froma pattern that has had some reflexivefeeding rhythm characteristics [Bosma,1986]. The maturation of sucking andswallowing from preterm to term andbeyond is characterized by increasedsucking and swallowing rates, longersucking bursts, and larger volumes persuck [Mathew, 1991; Schrank et al.,

1998; Lau et al., 2000, 2003; Gewolbet al., 2001a,c; Qureshi et al., 2002;Mizuno and Ueda, 2003; Gewolb andVice, 2006].

Feeding experience appears to bethe best predictor of feeding outcomes[Pickler et al., 2005, 2006], with thenumber of sucks in the first suck burstalso contributing significantly to feedingoutcomes [Pickler et al., 2006]. Picklerand Reyna [2003] suggest that achieve-ment of full bottle feedings may befacilitated by increased bottle-feedingopportunities, given the inverse rela-

tionship found via number of bottlefeedings received per day during transi-tion from the first bottle feeding to fullbottle feedings and length of transitionto full bottle feedings in 25 preterminfants. Crosson and Pickler [2004]reviewed the literature on demand feed-ings for preterm infants. They foundthat the seven studies in the previous 50

years used a variety of research methodswith interpretation difficulties becauseof inadequate sample sizes and incom-plete descriptions of methodology insome studies. They concluded that

overall findings support cautious con-tention that demand feeding mightprove to be the feeding approach ofchoice for most healthy preterm infants.In contrast, Tosh and McGuire [2006]concluded following a standard searchstrategy of the Cochrane NeonatalReview Group that there are insuffi-cient data to guide clinical practice as ofthe date of their review. They urged alarge randomized controlled trial tofocus on infants in the transition phasefrom gavage to oral feeding that should

be of sufficient duration to assess effectson growth and time to oral feeding andhospital discharge.

Oral feeding at term and during first fewmonths of life. Healthy premature infantsat their expected delivery date andinfants delivered at term during the firstweek of nipple feeding are likely tohave intermittent decreased minute ven-

tilation, respiratory rate, and tidal vol-ume during oral feeding. During thenext few months, infants refine theirskills and increase efficiency so that theymaintain feeding durations while theyconsume a greater volume appropriatefor their weight gain and growth.Regardless of age, the majority ofinfants swallows are followed by expira-tion [Kelly et al., 2007].

The anatomy of oral and pharyn-geal structures in the first few monthsof life underlies and facilitates nipplefeeding. The mandible is disproportion-

ately small compared to the skull. Thetongue fills the oral cavity and contactsall surfaces leaving little space for varia-tion in tongue movements. The fat padsin the cheeks narrow the oral cavity inthe lateral dimension [Kennedy andKent, 1985; Bosma, 1986; Arvedsonand Brodsky, 2002]. The posterior one-third of the tongue lies within the oralcavity as the larynx is positioned muchhigher in the pharynx than in the adultstructure without the 908 angle separat-ing the oral and pharyngeal cavities andthe approximation of the soft palate and

epiglottis. This positioning of the larynxhigh and under the tongue base affordsthe infant some protection, but nottotal protection, from aspiration of liq-uid into the lungs. This anatomic con-figuration supports the act of suckling,defined as backwardforward tonguemovement to extract liquid from thebreast or bottle [Bosma, 1986; Arvedsonand Brodsky, 2002].

Infants delivered at term typicallytake only breast milk or formula vianipple during the first few months oflife. According to the American Acad-

emy of Pediatrics (AAP) [Samour andKing, 2006], infants in the first monthof life average 75 ml (2.5 oz) formulaor breast milk per 450 g (pound) ofbody weight per day over 78 feedingslasting 1520 min at 23 hr intervals.Typical infants increase the amount ofbreast milk or formula by 30 ml (1 oz)per month until 69 months when theytake 240 ml (8 oz) per feeding 34times per day [Samour and King, 2006](Table 4). By 6 months of age, theseinfants taking smooth pureed food by





7/13

spoon are still getting 80% of nutritionneeds met by formula or breast milkwith decrease to 50% by 10 months ofage [e.g., Samour and King, 2006]. Effi-cient infants and children spend 30 minor less at mealtimes [Reau et al., 1996].

The AAP Committee on Nutri-tion recommends that infants are giveniron-fortified formula or breast milkuntil 12 months of age for optimalnutrition status [AAP, 1999]. Cows

milk before 12 months of age increasesthe risk for iron deficiency anemia,milk protein allergy, gastrointestinalblood loss, and inadequate nutrition.

No nutrition supplement isrequired until 6 months of age as terminfants usually have adequate iron storesuntil then, whether they are breast orbottle fed [Griffin and Abrams, 2001;Samour and King, 2006]. By 6 monthsof age, caloric requirements are notalways satisfied with formula or breastmilk alone. Total breast-fed infantsrequire iron and zinc supplements, usu-

ally by introduction of iron-fortifiedinfant cereal and pureed meats by spoon[Fomon, 2001; Samour and King, 2006;Krebs, 2006]. The transition to spoonfeeding is an important milestone fordevelopmental skill purposes and nutri-tion well-being.

Preterm infant age adjustments after birthPreterm infants should be given

the benefit of their adjusted ages for thefirst 24 months of life. In addition,functional levels relating to gross and

fine motor skills, cognitive skills, andlanguage and speech skills, must all betaken into account when determiningexpectations for oral feeding recom-mendations. The expectations for feed-ing skills and swallowing safety are esti-mated in relation to both adjusted ageand overall developmental status. Differ-ences become particularly importantwhen determining readiness for advanc-ing textures. When overall developmen-tal skill levels (gross and fine motorskills as well as cognitive and speech/

language skills) are below chronologicage (or adjusted age for children bornprematurely), feeding and swallowingspecialists should guide parents andother professionals in ways that helpthem to appreciate fully the relationshipof oral feeding skills and global develop-mental levels. For example, a child at 12months chronologic age, 9 monthsadjusted age (born at 26 weeks gesta-tion) and not yet sitting independently

(expected by 6 months), is not expectedto chew and swallow solid food. Thischild realistically would be expected tohave oral feeding and swallowing skillsequivalent to a typically developinginfant at about 6 months of age. At thatage, nipple feeding continues to be theprimary means of meeting nutrition andhydration needs with spoon feeding forpractice and developmental skilladvancement. In addition to the skill de-velopment that infants experience dur-ing the first year of life, they also partici-pate in reciprocal feeding or mealtime

relationships that change over time.

Relationship changes relevant to feedingdevelopment

Feeding during infancy is a recip-rocal process that depends on specificabilities and characteristics of caregiversand infants with a give-and-takeexchange. Normal feeding developmentincludes the following three stages: ho-meostasis (02 months), attachment(36 months), and separation/individua-tion (636 months) [Chatoor et al.,

1984]. A healthy positive feeding rela-tionship is critical for successful feeding.Caregivers need to understand the pro-cess in the young infants achievementof some degree of self-regulation duringthe stage of homeostasis. Caregiversmust recognize and respond promptly tohunger cues, and they should assist theinfant in regaining an organized state af-ter becoming overstimulated or upset.During the stage of attachment, infantsbegin to engage interest of other peoplein interactional patterns [Greenspan and

Lourie, 1981] with feeding becoming asocial time. Pauses after sucking burstsduring nipple feedings become moreobvious. Feeders may interpret thosepauses as the infant signaling a need toburp or indicating satiety, whereas theinfant may be pausing as a cue forsocialization. Infants begin to exertmore control over their environment byabout 6 months of age at the beginning

of the separation/individuation period.From 6 months to 36 months, the pri-mary behavioral development is a strug-gle to attain a sense of self. Caregiversprovide boundaries, structure, and limitsthat allow a child to explore safely. Acommon challenge at meal times duringthis time involves a balance betweenautonomy and dependency.

Although this article focuses onthe infant and young child for oral skilldevelopment while stressing the impor-tance of swallowing efficiently withoutrisks for aspiration, successful feeding

also requires appropriate reciprocal rela-tionships among caregivers and children.The complexities of feeding in typicalchildren and those with feeding andswallowing problems involve multiplefactors, all of which must be consideredfor caregivers to make decisions regard-ing optimal facilitation of safe and non-stressful feeding. The need for knowl-edge of normal development continuesto be important as typical children reachthe second half of the first year of lifeand become ready for transition feeding.

Changes in second half of first year: Transi-tion feeding. Infants demonstrate readi-ness for transition feeding when theyare 6 months of age, or when theiroverall developmental skills are at thatlevel, usually including the ability tomaintain an upright posture for a shorttime when placed in a sitting position.

Anatomic changes have occurredas growth of the oral cavity and lower-ing of laryngeal structures providesmore space in the oral cavity. Withelongation of the pharynx and descentof the larynx, a 908 angle of the oral-

pharyngeal complex occurs as the pos-terior 1/3 of the tongue descends intothe pharynx. The fat pads are absorbedand disengagement of the soft palateand epiglottis occurs. These anatomicchanges allow for increased movementof the oral structures that aid in thetransition from the early pattern ofsuckling to sucking and the introduc-tion of spoon feeding. Sucking is char-acterized by the tongue showing verti-cal movement to extract liquid withonly small vertical movement of the jaw

Table 4. Typical Number of Bottle/Breast Feedings per Day andRange of Formula Intake

Age (months) Number of Feeds per Day Range of Intake per Feeding


8/13

and firmer approximation of the lips[Bosma, 1986; Arvedson and Brodsky,2002]. With the change in direction oftongue movement during sucking, thechild is ready for transition to foodsother than liquids. As additionalresearch is carried out, perhaps the casestudy report with vertical tongue actionnoted in a preterm infant on ultrasoundmay provide added support for that

finding [Miller and Kang, 2007].

Critical and sensitive periods affectingexpansion of diet textures

Critical periods have beendescribed for chewing and for taste.The critical period for chewing is thattime following the disappearance of thetongue protrusion reflex that shouldoccur around 6 months of age [Illing-worth and Lister, 1964]. The tongueprotrusion reflex is characterized bypushing food out of the mouth when itis placed on the anterior tongue. Most

children have difficulty in learning spe-cific oral movements if these new tex-tures are introduced after the criticalperiod has passed. When textured foodsare introduced after 10 months of age,children are more likely to refuse solids.They consume inadequate volumes offood and are choosy about the foodsthey accept at 15 months of age[Northstone et al., 2001].

Critical periods have also beenreported for introduction of tastes.Newborn infants detect sweet solutions,reject sour flavors, and are indifferent to

the taste of salt [Mennella and Beau-champ, 1998]. By 4 months of age,infants recognize salt water relative toplain water and over the next 2 yearschanges in taste response occur. By 18months, children begin rejecting saltwater in preference for salt in tablefoods [Mennella and Beauchamp, 1998].Children first introduced to fruitsshowed preference for fruits over vege-tables. However, multiple exposures tovaried foods increased their overall ac-ceptance and intake [Sullivan and Birch,1994; Forestell and Mennella, 2007].

Breast-fed children have been reportedto have less prominent food selectivitythan formula-fed due to exposure tomultiple flavors from the breast milk ifthe mother frequently consumed thosefoods [Forestell and Mennella, 2007].Likewise difficulties in introducingunpleasant tasting protein hydrolysateformulas during older infancy (at 7months of age) may relate to early lim-ited experiences with multiple flavorsfor infants on milk based formulas[Mennella et al., 2004].

Anatomic and sensory changesEruption of teeth is an important

anatomic change in late infancy. Theteeth assist in biting and grinding ofmore textured foods.

Dentition is thought to play acrucial role as sensory receptors duringbiting and chewing [Bosma, 1986;Arvedson and Brodsky, 2002]. Onset oftooth eruption is expected for mandib-ular incisors (68 to 1213 months),molars (1224 months), and canines(1620 months) [Bosma, 1986; Arved-

son and Brodsky, 2002].

Introduction of spoon feedingThe introduction of spoon feed-

ing of thin smooth pureed food occursonce a child reaches about a 6-monthlevel developmentally. Foods are intro-duced one at a time in a specific orderper guidelines by dietitians that permitobservations for potential food allergies[Fomon, 2001; Fiocchi et al., 2006;Samour and King, 2006]. The AmericanDietetics Association recommends athin rice infant cereal as the first food

because it is an unlikely allergen. Singleingredient foods (such as commercialStage one thin pureed food in the U.S.or well blended smooth food) should beintroduced one at a time after cereal totest for food allergies. Combinationfoods that are smooth pureed foods(e.g., Stage two baby foods in the U.S.)can be introduced after all single ingre-dient foods have been offered usuallybetween 7 and 9 months of age. Gradu-ally food with texture are added, suchas, dissolvable solids (e.g., soft cracker at

69 months), textured puree foods(e.g., mashed banana, cottage cheese at69 months), ground solids at 69months, soft diced solids (e.g., fruits andvegetables at 912 months), and eventu-ally a general toddler diet of table foodsby 1218 months of age.

In the U.S. and some other coun-tries, a spout cup is introduced between6 and 9 months as a beginning step inweaning from the breast or bottle. Chil-dren are more likely to be successfulwith cup drinking if a spill-proof valve

is not used until a child has learned tosuck actively to extract liquid. By 12months, children are generally receivingtheir fluids through a combination ofbottle or breast feeding and cup with avalve or a straw. Children are expectedto drink independently from a spoutcup or straw, usually by their first birth-day. Independent drinking from anopen cup usually occurs later.

With these feeding transitions, gen-eral motor development and oral feed-ing ability are shown to relate closelyalthough a one-to-one relationship has

not been established (Table 5) [Carruthand Skinner, 2002; Koda et al., 2006].With broad developmental gains ingross motor function, children canimprove stability through the trunk,neck, and shoulder musculature toincrease mobility of extremities for self-feeding activities These gains aid in thestability of respiratory muscles, laryngealand oral-pharyngeal structures impor-tant to achieve feeding milestones [e.g.,Alexander, 1987; Larnett and Ekberg,1995; Morris and Klein, 2000].

Table 5. Selected Motor Skills (Gross, Fine, and Oral) inChildren During Transition Feeding Development

Mean age (mont hs) Mot or Skill

45 Sit on caregivers lap without helpReach for spoon when hungryOpen mouth when spoon approaches or touches lipsMove tongue gently back and forth as food enters mouthUse tongue to move food to back of mouth to swallowKeep food in mouth; no refeeding

68 Transfer toys and foods from one hand to the other Feed self cracker or cookie

810 Crawl on hands and kneesTurn upper body from sitting to crawlingEat finger foods without gaggingUse fingers to rake food toward selfPut fingers in mouth to move food and keep it in the mouthEat foods with tiny lumps without gaggingChew softer foods, keeping most in mouth

1012 Walk without helpPoke food with index fingerChew firmer foods, keeping most in mouth

Adapted from Carruth and Skinner, 2002.





9/13

Oral-Motor Development for Earlyand Advanced Transitional Feeders

Growth patterns, progression oftexture advancement, and mealtime du-ration are factors in the feeding devel-opment of young children. Disruptionsin these factors are common in childrenwith feeding and swallowing problemswhen they should be transitioning tonew skills that are needed to reach agoal for table food and cup drinking.These disruptions do not define under-lying oral sensorimotor difficulties.Understanding of the typical oral-motor

development related to feeding enablesclinicians to sort out delayed advance ofdiet from disorders of feeding and swal-lowing. Observation and description oforal-motor behaviors in typically devel-oping children have been primarymeans for reaching conclusions regard-ing oral-motor development and func-tion. These descriptions of oral-motordevelopment form a basis for diagnosingfeeding disorders. Developmental hier-archies of oral-motor skill acquisitionthat have been described for transitionalfeeders are found primarily in reviews

and based on expert opinion throughinformal observations [e.g., Bosma,1986; Pridham, 1990; Stevenson andAllaire, 1991; Alexander et al., 1993;Pinder and Faherty, 1999; Morris andKlein, 2000; Arvedson and Brodsky,2002]. Empirically based systematic andformal observations for typically devel-oping transition feeders are limited(Table 6). Formal and informal descrip-tions have limitations that include thefollowing: (1) inconsistent operationaldefinitions for observational normative

data, (2) lack of agreement of terminol-ogy among researchers, (3) variability inages reported for skill acquisition, (4)subjectivity required by observer tointerpret skills, and (5) overall limitednumber of typically developing childrenstudied. The current state of normativedata leads to concerns regarding thewide range of ages reported for acquisi-tion of any specific oral skill. Thesereports based on small number of typi-cally developing children may inflatethe influence of individual variability.The reported range of onset of oral

motor skills across typically developingchildren varied from as little as 6months to as high as 26 months for anygiven skill [Morris, 1982; Carruth andSkinner, 2002]. Descriptions of oral-motor development commonly used toevaluate and to make management deci-sions for children with feeding andswallowing deficits are based primarilyon descriptions of six children followedover time [Morris, 1982]. The expectedage of onset for all oral-motor behaviorswas reported when two-thirds of theparticipants (four of the six children)

demonstrated that particular skill.Detailed descriptions were presented.However, normal variability is notlikely accounted for with that limitedsample. Most descriptions of normaloral-motor development for feeding arebased on Morris [1982].

Observation of children whilethey are eating and drinking offers clini-cians opportunities to note some oralskills, but some oral movements are notvisible during these kinds of evaluations.It is not possible to define pharyngeal,

laryngeal, and upper esophageal musclemovements by observation. In instanceswhere concerns include possible pha-ryngeal phase swallowing problems, toinclude risks for aspiration with oralfeeding, instrumental examinationsbecome important.

Instrumental Examinations of OralSensorimotor Skills and Swallowing

Instrumental methods that supple-ment observations of feeding includeelectromyography (EMG) and kinematicanalyses [Green et al., 1997; Wilson,

2005]. However, these methods havelimitations. For example, EMG meas-ures muscle activation patterns but itdoes not provide relevant observationalmovement patterns. Kinematic analyses

yield movement patterns of the jaw intwo- and three-dimensions by tracingreflective markers placed on the chin,but they give no indication of bolusposition.

Other examinations that focus onpharyngeal phase of swallowing includevideofluoroscopic swallow study (VFSS)and flexible endoscopic evaluation of

swallowing (FEES) with sensory testing(FEESST). VFSS provides visualizationof oral, pharyngeal, laryngeal, and upperesophageal structures in two-dimen-sions. The primary focus for that exam-ination is to define pharyngeal physiol-ogy for swallowing. The FEES withsensory testing (FEESST) does not pro-vide visualization of the oral phase ofswallowing, although it visualizestongue base, soft palate, laryngeal, andpharyngeal structures. Details regardingthese instrumental examinations can be

Table 6. Typical Oral-Motor Development with Clinical Relevance for Transition Feeders

SourceN; Age Groups(months) Method Normative Data

Gesell and Ilg, 1937 N5 10; Birth to 12months

Longitudinal clinical feeding observation;Cine recording;

Descriptions of oral-motor behaviors

No standardized feeding proceduresGisel, 1991 N5 143; 6, 8, 10,

12, 18, 24 monthsCross-sectional clinical feeding observation; Chewing duration, number of chewing

cycles, time/cycle ratios per texturesaveraged across 10 trials

Video recording of 10 trials of differenttextures (puree, small piece viscous, large

piece viscous, solid).Morris, 1982 N5 6; Birth to 36

monthsLongitudinal clinical feeding observation;

Video recording; No standardized feedingprocedures

Descriptions of oral-motor behaviors

Stolovitz and Gisel,1991

N5 143; 6, 8, 10,12, 18, 24 months

Cross-sectional clinical feeding observation; Frequency of occurrence of: anticipation offood, food removal with lips, reactionafter spoon removal, tongue movementsaveraged across 10 trials

Video recording of 10 trials of differenttextures (puree, small piece viscous, largepiece viscous, solid)

Wilson, 2005 N5 48; 4, 7, 12, 35months

Cross-sectional kinematic feedingassessment, five trials of each food texturein childs current diet.

Analyses:3-dimension volume;2-dimension horizontal excursion;Rate/frequency of chewing.

Dev Disabil Res Rev




10/13

found in several sources [e.g., Willging,1995; Willging et al., 1996; Arvedsonand Lefton-Greif, 1998; Willging andThompson, 2005].

Developmental Progression ofOral-Motor and Feeding Skills

Movements of the jaw, lips, andtongue serve as the foundation skillsrequired during oral feeding. The jaw

supports and positions the tongue andlips and opens and closes to accept andchew food [Kennedy and Kent, 1985].The lips open to accept food, close tocontain food within the oral cavity andmay retrieve food outside the oral cavity.The tongue curves around the food tocontrol it within the oral cavity, reposi-tions and changes shape to manipulatethe bolus, retrieves food outside the oralcavity and moves upward to contact thehard palate to propel the bolus into thepharynx [Kennedy and Kent, 1985;Hiiemae and Palmer, 2003]. Overall,

early transition feeders demonstrate in-accurate and inconsistent control of oralstructures during feeding developmentas they advance textures, but the oral-motor movements for feeding becomemore accurate and less variable with ex-perience, similar to experience withother oral-motor movements [Robbinsand Klee, 1987; Clark et al., 2001].

Jaw movement developmentJaw movement development has

been the focus of considerable scrutinyin feeding development research, likely

due to easy access during direct obser-vation and instrumental measures. Theamount and type of jaw movement usedduring feeding provides meaningful in-formation about the motor control ofthis structure. Accepted descriptions ofthe developmental progression of jawmovement from a vertical opening andclosing movement described by Bosma[1986] eventually developing into a cir-cular-rotary chewing pattern [Morris,1982] may be dispelled with recent ki-nematic analyses of chewing develop-ment [Wilson, 2005]. More specifically,

early transition feeders are described asusing wide and ungraded jaw move-ments during spoon feeding. Openingmovements of the jaw to accept thebolus are inaccurate and overshoot theintended target, which is ascribed tolack of experience [Morris, 1982]. Wilson[2005] supported the descriptions ofinaccurate movements as she stated thatthe 4- and 7-month old children used agreater range of jaw movement forpureed foods than older children andadults. However, kinematic analyses

reveal that the movements of the jawduring chewing do not follow thepredictable pattern previously described.Kinematic analyses have expandedunderstanding of the complexities of

jaw movement during feeding develop-ment that cannot be discerned by visualinspection alone.

The initial stage of chewing de-velopment established between 6 and 9

months consists primarily of vertical jawmovement (munching) with a sucklingmotion by the tongue while chewingsolids has been agreed upon [e.g., Mor-ris, 1982; Gisel, 1991]. The complexityof jaw movements seems to increasesimultaneously with lateral movementsof the tongue to transfer the bolus tothe molar or chewing surfaces. Thesekinematic data also suggest that overallrange of jaw movement increases aschildren make advances with textures.These findings suggest that movementpatterns are different for different tex-

tures resulting in the consensus thatchildren should be observed as they takefood of varying textures [Gisel, 1991;Wilson, 2005].

The coordinative organization forchewing measured by EMG is estab-lished by 12 months of age but contin-ues to be refined into childhood [Greenet al., 1997]. Overall, chewing effi-ciency increases with age and is texturespecific. As children gain chewing effi-ciency, they use fewer chewing cycles(each cycle consists of one down andup movement of the jaw) for overall

shorter duration than when they werefirst introduced to chewing [Gisel,1988]. Chewing duration for solids sig-nificantly decreases across the transitionfeeding period [Gisel, 1991] and doesnot stabilize until sometime after 3 yearsof age [Gisel, 1988].

Children take more time to chewsolids than pureed food, which is to beexpected since pureed foods typicallyrequire little or no chewing. The onlygender difference occurs with girls tak-ing more time to chew solids than boys[Gisel, 1991]. Time/cycle ratios were

generally between 1.0 and 1.5 for alltextures and no significant differenceswere found by age or texture [Gisel,1991; Wilson 2005]. Collectively, stud-ies suggest that infants move their jawwith similar range of movement asadults. Infants just learning to chewproduce the same chewing rate as adultsacross textures [Wilson, 2005].

Lip movement developmentLip movement during oral feed-

ing is readily observable. Children use

the lips to remove food from the spoon,to stabilize the rim of the cup to extractliquid, and to maintain a bolus insidethe oral cavity. Poor lip strength isthought to interfere with lip functionduring feeding.

Achievement of lip closure toremove a bolus from the spoon or toretain a bolus within the oral cavityvaries by texture and age. Visual obser-

vation of circumoral (lip) movementsduring feeding reveal differences in 6-to 24-month-old childrens ability touse full lip closure on a spoon for foodremoval and to retain a bolus in the oralcavity after removal of a spoon [Stolo-vitz and Gisel, 1991]. Most of the 143children achieved lip closure on thespoon to remove a bolus of pureed foodand maintained lip closure to retain abolus in the mouth. By 12 months ofage, all children achieved lip closure forat least 80% of trials for all consistenciesfor both removal and retention.

Normative midline lip closingpressure during feeding of puree wasdetermined for 104 typically developingchildren using a strain gauge transducerembedded in a spoon [Chigira et al.,1994]. The mean lip closing pressure onthe spoon steadily increased from 5months to 3 years of age (from 25 g/cm2 stabilizing at 75 g/cm2) whilevariability decreased with age. Lip clos-ing pressure increased only slightlybetween 3 and 5 years of age [Chigiraet al., 1994]. Strength cannot be judgedaccurately from clinical assessments of

oral feeding [Clark, 2003], but logicalestimations may be made from observ-able findings.

Tongue movement developmentThe tongue has important func-

tions during oral feeding. The tongue ishighly visible when a child opens themouth to accept a bolus or when onelicks the lips. On the other hand, thetongue is difficult to observe when achild is chewing or swallowing withclosed lips. The tongue is expected toremain in the oral cavity during feeding

except for retrieval of food from thelips. However, early transition feedersare likely to protrude the tongue out-side of the oral cavity during feeding.This protrusion decreases with experi-ence. Children gradually minimize asuckling pattern from 6 to 10 month ofage for viscous consistency and from 6to 12 months of age for puree. As chil-dren shift to sucking patterns with thetongue by 6 months of age, gross roll-ing movements in a lateral direction canbe noted. Over time, children advance





11/13

to distinct lateral shifting of the bolusfrom midline to the molar surfaces andback to midline [Morris and Klein,2000]. Eventually children lateralize thebolus with the tongue from one molarsurface to the other in smooth andcoordinated movements [Alexanderet al., 1993; Morris and Klein, 2000]with significant increase from 6 to 24months of age for solids but not for vis-

cous consistencies [Stolovitz and Gisel,1991]. Only 7% of 2-year-old childrenand 15% of 5-year-old children moveda solid food from side to side precisely.Instead, they tend to use slow and roll-ing tongue movements to lateralize thefood [Gisel, 1988].

Children from 12 to 36 monthsof age continue to refine their oralskills, expand the kinds of foods theyaccept, become more efficient at chew-ing foods that require more extensiveoral manipulation, and handle liquidsvia open cup. Their eating is basically

functional for regular table food withtheir peers and the rest of their family.

Primary areas of oral-motor de-velopment for feeding have beendescribed. These skills should be con-sidered in the general context of nutri-tion needs and general motor develop-ment. Oral-motor development forfeeding is described in varied sources.However, data-based references are lim-ited. High levels of variability arereported in expected onset of most ofthese skills but a general progression hasbeen established. Careful consideration

is needed when professionals use thesedescriptions. More systematic normativedata are needed for adequate under-standing of normal oral-motor develop-ment for feeding.

SUMMARYClinicians evaluating feeding and

swallowing skills of infants and youngchildren make their observations basedheavily on extensive knowledge of nor-mal development, to include embryol-ogy and fetal development. Althoughmultiple sources contain descriptions of

oral-motor behaviors in infants andyoung children, there is a need for ob-jectivity with quantitative measures toaid clinicians in decision making formanagement of infants and childrenwith feeding and swallowing disorders.Additional research findings are neededthat will assist clinicians in confirming,expanding, or refuting observationalreports. With increased data, ages of ac-quisition of oral skills may be narrowedand refined to provide the most usefulinformation to clinicians involved in

evaluating infants and children withcomplex feeding and swallowing issues.Instrumental examinations of swallow-ing and oral skills, although discussedonly briefly, must be considered whenthere are signs of possible aspirationwith oral feeding, along with possiblepharyngeal or upper esophageal swallowdeficits. Procedures and observationsmay differ from one child to another,

but the ultimate goal is the same for ev-ery infant and child: a stable airway andadequate nutrition/hydration. n

REFERENCESAlexander R. 1987. Oral-motor treatment for

infants and young children with cerebralpalsy (CP). Semin Speech Lang 8:87100.

Alexander R, Boehme R, Cupps B. 1993. Nor-mal development of functional motor skills.San Antonio: Therapy Skill Builders.

Als H. 1985. Observation of newborn behavior(NIDCAP). Boston: Brigham and WomensHospital.

Als H. 1986. A synactive model of neonatal be-havioral development in the prematureinfant and for support of infants and parentsin the neonatal intensive care environment.Phys Occ Ther Pediatr 6:354.

Als H, Brazelton TB. 1981. A new model ofassessing the behavioral organization in pre-term and fullterm infants: two case studies.

J Am Acad Child Psychiatry 20:239263.Altschuler SM. 2001. Laryngeal and respiratory

protective reflexes. Am J Med 111(Suppl8A):90S94S.

American Academy of Pediatrics Committee onNutrition. 1999. Iron fortification of infantformulas. Pediatrics 104(Part 1):119123.

Arvedson JC, Brodsky L. 2002. Pediatric swallow-ing and feeding: assessment and manage-ment, 2nd ed. Albany: Singular PublishingGroup, Division of Thomson Learning.

Arvedson JC, Lefton-Greif MA. 1998. Pediatricvideofluoroscopic swallow studies: a profes-sional manual with caregiver guidelines. SanAntonio, TX: Harcourt Assessment.

Bernbaum JC, Pereira GR, Watkins JB, et al.1983. Nonnutritive sucking during gavagefeeding enhances growth and maturation inpremature infants. Pediatrics 71:4145.

Blomquist AJ, Antem A. 1965. Localization of theterminal of the tongue afferents in the nu-cleus of the solitary tract. J Comp Neurol124:127130.

Bosma JF. 1986. Development of feeding. ClinNutr 5:210218.

Bradley RM, Mistretta CM. 1975. Fetal sensoryreceptors. Physiol Rev 55:352358.Bradley RM, Mistretta CM. 1973. Swallowing in

fetal sheep. Science 179:10161017.Bragelien R, Rokke W, Markestad T. 2008. Stim-

ulation of sucking and swallowing to pro-mote oral feeding in premature infants. ActaPaediatr 96:14301432.

Brazelton TB, Nugent JK. 1995. Neonatal behav-ioral assessment scale, 3rd ed. London:MacKeith Press. Clinics in DevelopmentMedicine No. 137

Brody BA, Kinney HC, Kloman AS, et al. 1987.Sequence of CNS myelination in humaninfancy. I. An autopsy study of myelination.

J Neuropathol Exp Neurol 46:283301.

Broussard DL, Altschuler SM. 2000a. Centralintegration of swallow and airway-protectivereflexes. Am J Med 108(Suppl 4a):62S67S.

Broussard DL, Altschuler SM. 2000b. Brainstemviscerotopic organization of afferents andefferents involved in the control of swallow-ing. Am J Med108(Suppl 4a):79S86S.

Burroughs AK, Asonye UO, Anderson-ShanklinGC, et al. 1978. The effect of nonnutritivesucking on transcutaneous oxygen tension innoncrying, preterm neonates. Res NursHealth 1:6975.

Cagan J. 1995. Feeding readiness behavior inpreterm infants (Abstract). Neonatal Netw14:82.

Cajal CLR. 1996. Description of human fetallaryngeal function: phonation. Early HumDev 45:6372.

Carroll JL. 2003. Developmental plasticity inrespiratory control. J Appl Physiol 94:375389.

Carruth BR, Skinner JD. 2002. Feeding behaviorsand other motor development in healthychildren (224 months). J Am Coll Nutr21:8896.

Chatoor I, Schaefer S, Dickson L, et al. 1984.Non-organic failure to thrive: a develop-mental perspective. Pediatr Ann 13:829843.

Chigira A, Kazuhiko O, Mukai Y, et al. 1994.

Lip closing pressure in disabled children: acomparison with normal children. Dyspha-gia 9:193198.

Clark HM. 2003. Neuromuscular treatment forspeech and swallowing: a tutorial. Am JSpeech Lang Pathol 12:400415.

Clark HM, Robin DA, McCullagh G, et al.2001. Motor control in children and adultsduring a non-speech oral task. J SpeechLang Hear Res 44:10151025.

Crosson DD, Pickler RH. 2004. An integratedreview of the literature on demand feedingsfor preterm infants. Adv Neonatal Care 2:216225.

Daniels H, Hevlieger H, Casaer P, et al. 1986.Nutritive and non-nutritive sucking in pre-term infants. J Dev Physiol 8:117121.

Devries JIP, Visser GHA, Prechtl HFR. 1985.The emergence of fetal behavior. II. Quanti-tative aspects. Early Hum Dev 12:99120.

DiPietro JA, Cusson RM, Caughy MO, et al.1994. Behavioral and physiologic effectsof nonnutritive sucking during gavage feed-ing in preterm infants. Pediatr Res 36:207214.

Dodds WJ. 1989. The physiology of swallowing.Dysphagia 3:171179.

Dodds WJ, Stewart ET, Logemann JA. 1989.Physiology and radiology of the normal oraland pharyngeal phases of swallowing. Am JRadiol 154:953963.

Dziewas R, Soros P, Ishii R, et al. 2003. Neuroi-maging evidence for cortical involvement in

the preparation and in the act of swallowing.Neuroimage 20:135144.Field T, Goldson E. 1984. Pacifying effects of

nonnutritive sucking on term and pretermneonates during heelsticks. Pediatrics 74:10121015.

Field T, Ignatoff E, Stringer S, et al. 1982. Non-nutritive sucking during tube feedings:effects on preterm neonates in an intensivecare unit. Pediatrics 70:381384.

Fiocchi A, Assaad A, Bahna S, et al. 2006. Foodallergy and the introduction of solid foods toinfants: a consensus document. Adverse reac-tions to Foods Committee, American Col-lege of allergy, asthma and immunology.Ann Allergy Asthma Immunol 97:1020.

Dev Disabil Res Rev




12/13

Fomon SJ. 2001. Feeding normal infants: rationalefor recommendations. J Am Diet Assoc 101:10021005.

Forestell CA, Mennella JA. 2007. Early determi-nants of fruit and vegetable acceptance.Pediatrics 129:12471254.

Fucile S, Gisel EG, Lau C. 2002. Oral stimulationaccelerates the transition from tube to oralfeeding in pre-term infants. J Pediatr 141:230236.

Gaebler CP, Hanzlik JR. 1996. The effects of aprefeeding stimulation program on preterm

infants. Am J Occup Ther 50:184192.Gesell A, Ilg FL. 1937. Feeding behavior of

infants. Philadelphia, PA: J.B. LippincottCompany.

Gewolb IH, Vice FL. 2006. Maturational changesin the rhythms, patterning, and coordinationof respiration and swallow during feeding inpreterm and term infants. Dev Med ChildNeurol 48:589594.

Gewolb IH, Vice FL, Schwietzer-Kenney EL,et al. 2001a. Developmental patterns ofrhythmic suck and swallow in preterminfants. Dev Med Child Neurol 43:2227.

Gewolb IH, Bosma JF, Taciak VL, et al. 2001b.Abnormal developmental patterns of suckand swallow rhythms during feeding in pre-term infants with and without bronchopul-

monary dysplasia. Dev Med Child Neurol43:454459.

Gewolb IH, Bosma JF, Vice FL. 2001c. Integra-tion of suck and swallow rhythms duringfeeding in preterm infants with and with-outBPD. Pediatr Res 49:315. (Abstract).

Gisel EG. 1988. Chewing cycles in 2- to 8-year-old normal children: a developmental pro-file. Am J Occup Ther 42:4046.

Gisel EG. 1991. Effect of food texture on the de-velopment of chewing of children betweensix months and two years of age. Dev MedChild Neurol 33:6979.

Green JR, Moore CA, Ruark JL, et al. 1997. De-velopment of chewing in children from 12 to48 months: longitudinal study of EMG pat-terns. J Neurophysiol 77:27042716.

Greenspan S, Lourie RS. 1981. Developmentalstructuralist approach to the classification ofadaptive and pathologic personality organiza-tions: infancy and early childhood. Am JPsychiatry 138:725735.

Griffin IJ, Abrams SA. 2001. Iron and breastfeed-ing. Pediatr Clin North Am 48:401413.

Hafstrom M, Kjellmer I. 2000. Non-nutritivesucking in the healthy pre-term infant. EarlyHum Dev 60:1324.

Hamdy S, Rothwell JC, Brooks DJ, et al. 1999.Identification of the cerebral loci processinghuman swallowing with H2(15)O PET acti-vation. J Neurophysiol 81:19171926.

Hiiemae KM, Palmer JB. 2003. Tongue move-ments in feeding and speech. Crit Rev Oral

Biol Med 14:413429.Hooker D. 1954. Early human fetal behavior, witha preliminary note on double simultaneousfetal stimulation. Res Publ Assoc Res NervMent Dis 33:98113.

Humphrey T. 1967. Reflex activity in the oraland facial area of the human fetus. In:Bosma JF, editor. Second Symposium onoral sensation and perception. Springfield,IL: Charles C. Thomas.

Illingworth RS, Lister J. 1964. The critical or sen-sitive period, with special reference to cer-tain feeding problems in infants and chil-dren. J Pediatr 65:839848.

Im H, Kim E, Park E, et al. 2008. Pain reductionof heel stick in neonates: yakson compared

to non-nutritive sucking. J Trop Pediatr54:3135.

Kelly BN, Huckabee M, Jones RD, et al. 2007.The first year of human life: coordinatingrespiration and nutritive swallowing. Dys-phagia 22:3743.

Kennedy JG, Kent RD. 1985. Anatomy and phys-iology of deglutition and related functions.Semin Speech Lang 6:257273.

Kinney HC, Brody BA, Kloman AS, et al. 1988.Sequence of CNS myelination in humaninfancy. II. Patterns of myelination in autop-

sied infants. J Neuropathol Exp Neurol47:217234.

Koda N, Tachibana Y, Hirose T, et al. 2006. De-velopment of eating behavior by Japanesetoddlers in a nursery school: relation to in-dependent walking. Percept Mot Skills103:145.

Krebs N. 2006. Meat as a first complementaryfood for breastfed infants: feasibility andimpact on zinc intake and status. J PediatrGastroenterol Nutr 42:207214.

Laitman J, Reidenberg J. 1993. Specializations ofthe human upper respiratory and upper di-gestive systems as seen through comparativeand developmental anatomy. Dysphagia8:318325.

Larnett G, Ekberg O. 1995. Positioning improves

the oral and pharyngeal swallowing functionin children with CP. Acta Pediatr 84:689692.

Lau C, Alagugurusamy R, Schanler RJ, et al.2000. Characterization of the developmentalstages of sucking in preterm infants duringbottle feeding. Acta Paediatr 89:846852.

Lau C, Smith EO, Schanler RJ. 2003. Coordina-tion of suck-swallow and swallow respirationin preterm infants. Acta Pediatr 92:721727.

Linden R. 1993. Taste. Br Dent J 175:243253.Logemann JA. 1998. Evaluation and treatment of

swallowing disorders, 2nd ed. Austin, TX:Pro-Ed.

Mathew O. 1991. Science of bottle feeding. Disa-bil Rehabil 119:511519.

McCain GC. 1995. Promotion of preterm infant

nipple feeding with nonnutritive sucking.J Pediatr Nurs 10:38.

McCain GC. 2003. An evidence-based guidelinefor introducing oral feeding to healthy pre-term infants. Neonatal Netw 22:4550.

Measel CP, Anderson GC. 1979. Nonnutritivesucking duringtube feedings: effect on clini-cal course in premature infants. J ObstetGynecol Neonatal Nurs 8:265272.

Mennella JA, Beauchamp GK. 1998. Develop-ment and bad taste. Pediatr Asthma AllergyImmunol 12:161164.

Mennella JA, Griffin CE, Beauchamp GK. 2004.Flavor programming during infancy. Pedia-trics 113:840845.

Miller AJ. 1982. Deglutition. Physiol Rev 62:

129184.Miller AJ. 1999. The neuroscientific principles ofswallowing and dysphagia. San Diego: Sin-gular Publishing Group.

Miller JL, Kang SM. 2007. Preliminary ultrasoundobservation of lingual movement patternsduring nutritive versus non-nutritive suckingin a premature infant. Dysphagia 22:150160.

Miller JL, Macedonia C, Sonies BC. 2006. Sexdifferences in prenatal oral-motor functionand development. Dev Med Child Neurol48:465470.

Miller JL, Sonies BC, Macedonia C. 2003. Emer-gence of oropharyngeal, laryngeal, and swal-lowing activity in the developing fetal upper

aerodigestive tract: an ultrasound evaluation.Early Hum Dev 71:6187.

Minei LJ, Suzuki K. 1976. Role of fetal degluti-tion and micturition in the production andturnover of amniotic fluid in the monkey.Obstet Gynecol 48:177181.

Mistretta CM. 1972. Topographical and histologi-cal study of the developing rat tongue, palateand taste buds. In Bosma JF, editor. Oralsensation and perception. Springfield, IL:Charles C. Thomas. p 163187.

Mizuno K, Ueda BS. 2003. The maturation and

coordination of sucking, swallowing, andespiration in preterm infants. J Pediatr 142:3640.

Moore KL, Persaud RVN. 2003. The developinghuman: clinically oriented embryology, 7thed. Philadelphia: Saunders.

Morris SE. 1982. Pre-speech assessment scale.Clifton, NJ: J.A. Preston Corporation.

Morris SE, Klein MD. 2000. Pre-feeding skills,2nd ed. San Antonio, TX: Therapy SkillBuilders, A Harcourt Health Sciences Com-pany.

Mosier KM, Liu WC, Maldkian JA, et al. 1999.Lateralization of cortical function in swal-lowing: a functional MR imaging study.AJNR Am J Neuroradiol 20:15201526.

Northstone K, Emmett P, Nethersole F, et al.

2001. The effect of age of introduction tolumpy solids on food eaten and reportedfeeding difficulties at 6 and 15 months.

J Hum Nutr Diet 14:4354.Paludetto R, Robertson SS, Hack M, et al. 1984.

Transcutaneous oxygen tension during non-nutritive sucking in preterm infants. Pedia-trics 74:539542.

Perkett E, Vaughan R. 1982. Evidence for alaryngeal chemoreflex in some human pre-term infants. Acta Paediatr Scand 71:969972.

Pickens DL, Schefft GL, Thach BT. 1988. Pro-longed panea associated with upper airwayprotective reflexes in apnea of prematurity.Am Rev Respir Dis 137:113118.

Pickler RH, Best AM, Reyna BA, et al. 2005.

Prediction of feeding performance in pre-term infants. Newborn Infant Nurs Rev5:116123.

Pickler RH, Best AM, Reyna BA, et al. 2006.Predictors of nutritive sucking in preterminfants. J Perinatol 26:693699.

Pickler RH, Chiaranai C, Reyna BA. 2006. Rela-tionship of the first suck burst to feedingoutcomes in preterm infants. J Perinat Neo-natal Nurs 20:157162.

Pickler RH, Reyna BA. 2003. A descriptive studyof bottle-feeding opportunities in preterminfants. Adv Neonatal Care 3:139146.

Pickler RH, Reyna BA. 2004. Effects of non-nu-tritive sucking on nutritive sucking, breath-ing, and behavior during bottle feedings of

preterm infants. Adv in Neonatal Care 4:226234.Pinder GL, Faherty AS. 1999. Issues in pediatric

feeding and swallowing. In: Caruso A,Strand E, editors. Clinical management ofmotor speech disorders in children. New

York, NY: Thieme Medical Publishers. pp281318.

Pinelli J, Symington A. 2001. Non-nutritive suck-ing for promoting physiologic stability andnutrition in preterm infants. The CochraneLibrary 3:CD001071.

Poulos DA, Lende RA. 1970a. Response of tri-geminal ganglion neurons to thermal stimu-lation of oral-facial regions. I. Steady-stateresponse. J Neurophysiol 33:508517.





13/13

Poulos DA, Lende RA. 1970a. Response of trigem-inal ganglion neurons to thermal stimulationof oral-facial regions. I. Temperature changeresponse. J Neurophysiol 33:518526.

Pridham KF. 1990. Feeding behavior of 6-12month old infants: assessment of sources ofparental information. J Pediatr Nurs 117:S174S180.

Qureshi MA, Vice FL, Taciak VL, et al. 2002.Changes in rhythmic suckle feeding patternsin term infants in the first month of life.Dev Med Child Neurol 44:3439.

Reau NR, Senturia D, Lebailly SA, et al. 1996.Infant and toddler feeding patterns andproblems: normative data and a new direc-tion. J Dev Behav Pediatr 17:149153.

Robbins J, Klee T. 1987. Clinical assessment oforopharyngeal motor development in youngchildren. J Speech Hear Disord 52:271277.

Rogers B, Arvedson J. 2005. Assessment of infantoral sensorimotor and swallowing function.Ment Retard Dev Disabil Res Rev 11:7482.

Ross MG, Nyland MJM. 1998. Developmentof ingestive behavior. Am J Physiol 43:R879R893.

Samour PQ, King K. 2006. Handbook of pediat-ric nutrition. Sudbury, England: Jones andBartlett Publishers.

Schrank W, Al-Sayed LE, Beahm PH, et al. 1998.

Feeding responses to free-flow formula interm and preterm infants. Disabil Rehabil132:426430.

South MM, Strauss RA, South AP, et al. 2005.The use of non-nutritive sucking to decrease

the physiologic pain response during neona-tal circumcision: a randomized controlledtrial. Am J Obstet Gynecol 193:537542.

Standley JM. 2003. The effect of music-reinforcednonnutritive sucking on feeding rate of pre-mature infants. J Pediatr Nurs 18:169173.

Stevenson R, Allaire JH. 1991. The developmentof normal feeding and swallowing. PediatrClin North Am 38:14391453.

Storey A. 1968a. A functional analysis of sensoryunits innervating epiglottis and larynx. ExpNeurol 20:366383.

Storey A. 1968b. Laryngeal initiation of swallow-ing. Exp Neurol 20:359365.

Stolovitz P, Gisel EG. 1991. Circumoral move-ments in response to three different foodtextures in children 6 months to 2 years ofage. Dysphagia 6:1725.

Sullivan SA, Birch LL. 1994. Infant dietary expe-rience and acceptance of solid foods. Pedia-trics 93:271277.

Teismann IK, Steinstraeter O, Stoeckigt K, et al.2007. Functional oropharyngeal sensory dis-ruption interferes with the cortical controlof swallowing. BMC Neurosci 8:62. Avail-able at: http://www.biomedcentral.com/1471-2202/8/62.

Thach BT. 2001. Maturation and transformationof reflexes that protect the laryngeal airway

from liquid aspiration from fetal to adult life.Am J Med 111(Suppl 8A):69S77S.

Thach BT. 2007. Maturation of cough and otherreflexes that protect the fetal and neonatalairway. Pulm Pharmacol Ther 20:365370.

Tosh K, McGuire W. 2006. Ad litum or demand/semi-demand feeding versus scheduled inter-val feeding for preterm infants. CochraneDatabase Syst Rev 3:CD005255.

Travers JB, Norgren R. 1986. Electromyographicanalysis of the ingestion and rejection ofsapid stimuli in the rat. Behav Neurosci100:544555.

Treloar DM. 1994. The effect of nonnutritivesucking on oxygenation in healthy, cryingfull-term infants. Appl Nurs Res 7:5258.

Willging JP. 1995. Endoscopic evaluation of swal-

lowing in children. Int J Pediatr Otorhino-laryngol 32:S107S108.

Willging JP, Miller CK, Hogan MJ, et al. 1996.Fiberoptic endoscopic evaluation of swallow-ing in children: a preliminary report of 100procedures. Dysphagia 11:162.

Willging JP, Thompson DM. 2005. PediatricFEESST: fiberoptic endoscopic evaluation ofswallowing with sensory testing. Curr Gas-troenterol Rep 7:240243.

Wilson EM. 2005. Kinematic description ofchewing development. PhD Dissertation.Madison, WI: University of Wisconsin-Madison.

Wolff PH. 1968. The serial organization of suck-ing in the young infant. Pediatarics 42:943956.

Yakovlev PI, Lecours AR. 1967. The myeloge-netic cycles of regional maturation of thebrain. In: Minkowski A, editor. Regionaldevelopment of the brain in early life.Oxford, England: Blackwell. p 370.

Dev Disabil Res Rev



development of swallowing and feeding

Documents