dental enamel hypoplasias in prehistoric populations

DENTAL ENAMEL HYPOPLASIAS INPREHISTORIC POPULATIONS

A. H. GOODMANSchool of Natural Science, Hampshire College, Amherst, Massachusetts 01002

Adv Dent Res 3(2):265-271, September, 1989

ABSTRACT

I ecent years have witnessed an impressive increase in research on enamel hypoplasias in archaeological^populations. By reviewing a series of studies of enamel hypoplasias at Dickson Mounds, Illinois,

North America (950-1300 A.D.), a prehistoric site involved in the transition from gathering-hunting to agricul-ture, this paper provides an illustration of this type of research.

The location of linear hypoplasias on labial tooth surfaces of 111 adults was studied with a thin-tipped caliper,and this location was converted to an age at development. Most defects developed between two and four yearsof developmental age. Hypoplasias increased in prevalence from 45% in the pre-agriculture group to 80% inthe agricultural group (p < 0.01). The transition to agriculture occurred at a cost to infant and childhood health.Defects are associated with decreased longevity. Individuals with defects have a life expectancy of nearly tenyears fewer than those without defects, suggesting that the development of a defect marks a significant andlasting health event. Enamel hypoplasias occur most frequently on anterior teeth, polar teeth in developmentalfields, and the middle developmental thirds of teeth. Analysis of these data suggests that enamel may bedifferentially susceptible to growth disruption and that susceptibility varies both within and among teeth.

The study of enamel defects at Dickson provides insights into the health and nutritional consequences of theeconomic change from hunting and gathering to agriculture. More generally, with the availability of teeth fromgenetically homogeneous populations, studies of enamel hypoplasias in prehistory should provide a usefulcomplement to research on this condition in contemporary peoples.

INTRODUCTION

The convening of an interdisciplinary conferenceon developmental defects of dental enamel is timelyfor one studying these defects in an archaeologicalcontext. Closer connections to the increasing body ofresearch on dental defects in experimental animalsand contemporary human populations will help im-prove prehistorians' understandings of the signifi-cance of these defects in archaeological contexts.Conversely, those studying dental defects in contem-porary humans may not be aware of the impressivegrowth in research on these defects in prehistoricgroups.

Presented at the Symposium and Workshop on DevelopmentalDefects of Enamel, February 23-25, 1988, Rotorua, New Zealand,sponsored by Colgate-Palmolive (NZ) Ltd., the New Zealand Den-tal Research Foundation, and the Medical Research Council of NewZealand

The research reported in this paper was supported in part byGrant T-32-DEO7048 from the National Institute of Dental Re-search, National Institutes of Health, Bethesda, Maryland 20892.

Where skeletal remains are available for analysis,enamel hypoplasias are now very often studied asindicators of physiological perturbations (stress) ex-perienced during tooth development (Rose etai, 1985).For example, in a recent volume on health and nu-tritional changes at the transition from hunting-gath-ering to agriculture (Cohen and Armelagos, 1984), 15of the 19 (79%) regional case studies included enameldefect data. The annual meetings of the AmericanAssociation of Physical Anthropologists regularly in-clude a number of papers on enamel defects, and the1988 meeting featured a symposium devoted to thissubject.

The use of enamel hypoplasias as non-specific, sys-temic stress indicators in prehistoric studies seems tobe well-justified. On the one hand, most defects areunlikely to be due to hereditary factors or localizeddisruptions (traumas), and these few cases are usu-ally identifiable (Cook, 1980). On the other hand, thelarge number of possible causes of these defects (Cut-ress and Suckling, 1982) precludes ascribing a morespecific cause. Especially where the fluoride contentof drinking water is low, and bouts of undernutrition

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266 GOODMAN Adv Dent Res September 1989

and disease during infancy and childhood are fre-quent, most defects are likely to be secondary to thestress imposed by these factors on the developingenamel.

This use of enamel hypoplasias as indelible re-corders of stresses during a critical period of dentaldevelopment fits into prehistorians' increased con-cerns with health and nutritional status. Temporalchanges in health and nutrition are now viewed asimportant keys to our understanding of human ev-olution. Further, the distribution of disease and maL-nutrition over ecological and sociopolitical terrains isincreasingly seen as critical to our understanding ofthe human condition, past and present. Dental re-searchers may not share all the prehistorians' evo-lutionary concerns. However, most might at leastappreciate that the archaeological database providesa greater time depth and a varied set of ecologicalsettings in which to study a condition that is commontoday.

The purpose of this paper is not an exhaustive re-view of the study of dental defects in prehistoric andarchaeological populations, but rather to highlighttrends and perspectives in a way that might informthose working with contemporary populations. Thiswill be done via a review of a series of studies ofenamel defects from one archaeological site: DicksonMounds, Illinois, North America (950-1300 A.D.).

In this paper, I will first provide a brief introductionto Dickson archaeology and the methods employedfor studying enamel hypoplasias. Subsequently, re-sults of three applications of the study of enamel de-fects at Dickson are presented: (1) temporal changesin the prevalence and age at development of defects;(2) associations between enamel hypoplasias and lon-gevity; and (3) distribution of defects within and amongteeth in relationship to patterns of sensitivity to de-velopmental disruption. The chief contribution of thefirst application is to\yard understanding shifting pat-terns of health and nutrition over time. The secondapplication has implications for the validity of dentalhypoplasias as "stress indicators". An association be-tween enamel defects and mortality would suggestthat the formation of these defects is a meaningfulevent. Finally, the third application raises fundamen-tal biological questions about the nature of normalenamel formation and how differences in sensitivityto developmental disruption may help to explain thedistribution of enamel hypoplasias within and amongteeth.

MATERIALS AND METHODS

The Dickson Mounds are a multicomponent, hab-itation-burial complex located near Lewiston, Illinois.The skeletons from Dickson have been associated withthree roughly sequential cultural groups: Late Wood-land (LW), Mississippian Acculturated Late Wood-land (MALW), and Middle Mississippian (MM). The

Late Woodland group (ca. 950-1100 A.D.) is charac-terized as one involving a relatively small (74-125)and semi-sedentary gathering and hunting popula-tion, with seasonal camp sites and an economy di-rected toward the use of a broad spectrum of localfauna and flora. The MALW group (ca. 1050-1200 A.D.)reflects a transition during which local populationscame under the influence of Mississippian culturesfurther to the south and already involved in maize-based agriculture (Harn, 1978,1986). During the MMtime period {ca. 1200-1300 A.D.), the "Mississippian-ization" of local populations became complete withthe culmination of trends toward: (1) extended andintensified trade networks; (2) increased populationdensity, size, and sedentarism; and (3) greater reli-ance on maize agriculture (Goodman et al., 1984b). Insum, in a short period of time the Dickson populationexperienced a revolutionary change in lifestyle, fromnomadic and rather self-reliant gathering-hunting toagriculture, village life, and increased contact withoutside groups.

The mounds and associated cemeteries are esti-mated to include over 3000 skeletons, of which nearlya third have been excavated and made available forpaleo-epidemiological analysis. Cultural group affili-ations of these individuals were determined by as-sociation with grave goods and burial positionindicative of the different groups and locations withinthe mounds (Goodman et al., 1984b). Developmentalage of adults was based on the agreement of multiplestandard measurements, including the degree of epi-physeal closure and changes in the pubic symphysis(Goodman et al., 1984b; Moore et al., 1975).

The temporal changes at Dickson have been shownto be associated with increases in nutritional, infec-tious, degenerative, and traumatic pathologies and adecrease in growth status and life expectancy (Good-man et al., 1984b; Goodman and Armelagos, 1985a).For example, porotic hyperostosis, an indication ofiron deficiency anemia, is four times as prevalentamong MM subadults as compared with LW sub-adults (64% to 16%) (Lallo et al., 1977). Periosteal in-fections in subadults increase from 27% in the LW to81% in the MM (Lallo et al., 1978). Life expectancy islower at all age intervals in the MM when comparedwith the combined LW and MALW samples (Mooreet al., 1975).

One hundred and eleven adults and adolescentswere examined for the presence of enamel hypopla-sias so that our understanding of changes in nutritionand health would be improved (Goodman et al., 1980).Enamel hypoplasias were operationally defined ashaving circumferential pitting and lines or bands ofdecreased enamel thickness (see Fig. 1). Identificationwas aided by the cleaning of teeth and use of a dentalprobe and binocular microscope.

All teeth were studied except for third molars, whichwere considered to be too variable in developmentaltiming for estimation of age at hypoplasia formation.Loss of the tooth (pre- or post mortem), as well as loss



Vol. 3 No. 2 ENAMEL HYPOPLASIAS IN PREHISTORIC POPULATIONS 267

of enamel (due to attrition and other causes), wasrecorded so that overestimation of the enamel avail-able for study would be avoided. For approximationof the developmental ages of individuals at the timeof hypoplasia formation, the locations of defects rel-ative to the cemento-enamel junction were measuredwith a thin-tipped caliper to 0.1 mm. These locationmeasurements were then converted to a develop-mental age based on the tooth development chro-nology of Massler and co-workers (1941). Defects were"clustered" into half-year developmental periods. Forexample, the maxillary central incisor was dividedinto nine half-year periods between birth-0.5 and 4.0-4.5 years of age. Finally, defects on different teethwere "matched" to others that occurred during thesame time period so that it could be ascertained thatthe hypoplasias were due to a systemic disruption.By use of this method, a chronology of stress by half-year developmental periods was achieved for eachindividual from birth to seven years of age (Goodmanet al., 1980, 1984a).

We should caution that this chronology providesonly an estimate of developmental age at time of for-mation of enamel hypoplasias. Variation may be ex-pected among individuals, genders, and populations.Eruption may be delayed by stresses such as chronicundernutrition and parasitism (Alvarez and Navia,1989). Therefore, matrix formation and calcificationtimes might also be affected. More information isneeded on population differences in and environ-mental effects on dental matrix formation and mat-uration. Nonetheless, the chronology of Massler andco-workers (1941) has been used in all other studiesof the chronology of enamel hypoplasias (Goodman,1988) and is close to other calcification standards(Cameroon and Sims, 1974). It is a useful startingplace for the development of information on the tim-ing of enamel hypoplasias.

The first study reviewed utilizes the entire data set,while the last two use a portion of the data set. Thesecond focuses on defects occurring between 3.5 and7.0 years, a period of time that was available for studyon all individuals. The third study is based on the 30individuals who had a complete and uneroded set ofteeth.

RESULTS

Temporal Changes in Prevalenceand Age at Development

Nearly two-thirds (66%) of individuals had one ormore hypoplasias. A clear trend of increased hypo-plasias per individual is evident through prehistoricstages. The mean frequency of enamel defects in-creases from 0.90 in the LW (n = 20) to 1.18 in theMALW (n = 45) and 1.61 in the MM (n = 46). Thereis an increased frequency of individuals with one ormore hypoplasias — from 45% in the LW to 60% inthe MALW and 80% in the MM. The difference inprevalence between the LW and combined MALWand MM and the MM alone is significant (p < 0.01level, Chi-square test with Yates' correction) (Good-man etal., 1980).

The chronological pattern of enamel defects for thepre-agricultural groups (combined LW and MALW)and the agricultural group (MM) is presented in Fig.2 (Goodman et al., 1984a). The developmental pat-terns of defects in both the pre-agricultural and ag-ricultural groups follow a roughly normal distribution,with highest frequencies between two and four yearsof age. However, there is some evidence for a slightlyearlier distribution of defects in the MM comparedwith the combined LW/MALW group. The median isearlier in the MM (2.5-3.0 years) than in the LW/MALW(3.0-3.5 years). At 2.5-3.0 years, 57% of the MM's 93

Fig. 1 - Chronologic enamel hypoplasias on maxillary, anteriorpermanent teeth. Hypoplasias are observable on the right centralincisor, the right and left lateral incisors, and the right and leftcanines. All hypoplasias occur between 3.0 and 3.5 years of de-velopmental age and appear to be the result of the same systemicdisruption (stress).

• LW/MALW• MM

40-1

30-

O 20-

10-

'0- "0.5-"l.0-"l "20-"2 "3.0-"3.5- 4.0" 4 5" 5 0- 5 5" 60" 6 5"0.5 10 1.5 2.0 2.5 30 3.5 4.0 4 5 50 5.5 60 65 7.0

DEVELOPMENTAL AGE (YEARS)

Fig. 2 —Frequency distribution of enamel hypoplasias by half-yearperiods in two Dickson Mounds populations: combined LateWoodland (LW) and Mississippian Acculturated Late Woodland(MALW) and the Middle Mississippian (MM) (Goodman et al.,1984a).




defects had occurred, compared with only 34% of the50 LW/MALW's defects. This difference approachessignificance (two-tailed p < 0.10) via the Kolmogorov-Smirnov test (Goodman et al., 1984a).

Enamel Hypoplasias and LongevityThe mean age at death of individuals in the three

cultural groups and in the total sample is comparedfor those individuals with no hypoplasia-stress peri-ods between 3.5 and 7.0 years, one hypoplasia-stressperiod, and 2-3 hypoplasia-stress periods (Table, Fig.3). In the LW, no individual had more than a singledefect. Those with one hypoplasia had a slightly butnot significantly greater mean age at death (34.7 years)than individuals with no hypoplasia-stress periods(31.6 years) (F ratio = 0.35; Goodman and Armela-gos, 1988).

This association between hypoplasias and longev-ity is reversed during the MALW periods. The meanage at death of individuals without hypoplasias was36.6 years, or 5.5 years greater than those with onehypoplasia-stress period (31.1 years) and 8.0 yearsgreater than those with two or more stress periods.This inverse association between stress periods andmean age at death is most pronounced during theMM. The mean age at death of individuals withouthypoplasias was 37.5 years, or 7.3 years longer thanthose with one hypoplasia and 15.7 years longer thanthose with two or more hypoplasias. A one-way AN-OVA, testing for the statistical significance of differ-ences in ages at death among hypoplasia-stress periodgroups, yielded an F ratio of 6.52 (p < 0.01; Table).

There is also a significant decrease in longevity withchildhood stress periods in the total sample (Table;

Fig. 3). The mean age at death of individuals withouthypoplasia-stress periods was 35.8 years, or 4.4 yearsgreater than for those with one hypoplasia-stress pe-riod (31.4 years) and 10.2 years greater than for thosewith two or more hypoplasia-stress periods (25.6years). The ANOVA yields a significant F ratio (4.99,p < 0.01). The most significant a priori contrasts arebetween the no-stress-period group and the one-or-more-stress-periods and two-or-more-stress-periodsgroups (t = 3.04 and 3.08, respectively; p < 0.01;Goodman and Armelagos, 1988).

Factors Affecting the Distributionof Enamel Hypoplasias

Variations in defect frequency among teeth are pre-sented in Fig. 4. The maxillary central incisor is mosthypoplastic, followed by the mandibular canine, themaxillary canine, and the other incisors. Despite sim-ilar ages at development, the maxillary central incisorhas nearly twice the frequency of defects as the otherincisors. Furthermore, this tooth is 4-5 times as hy-poplastic as first molars, which are developing atroughly similar ages.

Although there is extreme variation in defect fre-quency across teeth, we also noted that the distri-butions of defects within teeth are remarkably similar,despite variations in age at formation (Fig. 5). Spe-cifically, when the tooth crown is divided into de-velopmental thirds (incisal/occlusal, middle, cervical),the lowest frequency of defects is invariably foundon the incisal/occlusal third, and the highest propor-tion of defects is nearly always found in the middlethird. For all 14 teeth, from zero to 25% of defects pertooth are found on the incisal/occlusal third, from 40

TABLECOMPARISON OF MEAN AGES AT DEATH FOR INDIVIDUALS BY CULTURAL HORIZON AND NUMBER OF

HYPOPLASIA-STRESS PERIODS BETWEEN 3.5 AND 7.0 YEARS OF DEVELOPMENTAL AGE

Late WoodlandNo Hypoplasias (A)One Hypoplasia (B)2-3 Hypoplasias (C)

MALWNo Hypoplasias (A)One Hypoplasia (B)2-3 Hypoplasias (C)

Middle MississippianNo Hypoplasias (A)One Hypoplasia (B)2-3 Hypoplasias (C)

Total SampleNo Hypoplasias (A)One Hypoplasia (B)2-3 Hypoplasias (C)

SampleSize

20119

-4522149

461722

7111404516

Mean33.031.634.7

-33.336.631.128.631.637.530.221.832.535.831.425.6

S.D.11.510.413.0

~13.412.814.711.711.29.0

11.08.7

12.110.112.710.8

One-way ANOVA(F Ratio)

0.35

1.44

6.52**

4.99**

A prioriA vs. B0.55

1.22

2.25**

1.84+

ContrastsA vs. C

—

1.53

3.50***

3.04**

(T-Values)Aus.B + C

0.55

1.69

3.52***

3.08**

4- = 2-tailed p < 0.10; * = 2-tailed p < 0.05; ** = 2-tailed p < 0.01; *** = 2-tailed p < 0.001.




to 80% on the middle third, and from 18 to 60% onthe cervical third (Fig. 5).

DISCUSSION

The increased frequency of enamel hypoplasias inthe MM at Dickson supports other paleopathologicaldata in suggesting that the temporal changes expe-rienced by the Dickson populations led to an increasein infant and childhood stress (Goodman et al., 1980,1984a). Although the exact cause of these defects can-not be ascertained, the peak in hypoplasias betweentwo and four years of age suggests that, along withthe associated parasitism, the weaning diet may nothave been adequate.

More generally, enamel hypoplasias are ubiquitousin prehistoric populations (Rose et al., 1985). This isconsistent with the view that these groups were ex-periencing a variety of bouts of poor health and un-dernutrition, with minimal medical intervention. Thehigh prevalence of hypoplasias suggests that they aredue to systemic perturbations secondary to stressesof undernutrition and infection (Suckling et al., 1983,1986).

The developmental distribution of defects in pre-historic samples consistently peaks between two andfour years of age (Goodman, 1988). This contrasts toSarnat and Schour's (1941) study of a modern clinicalsample from Chicago, in which a much earlier peakwas reported. The difference suggests that the pat-tern of defects is due not to universal biological fac-tors, but rather is related to patterns of stress. Inpeasant populations, it is common to have a peak ininfection and malnutrition after the first year (cf.Chavez and Martinez, 1982; Mata et al., 1971). Thehypoplasia peak found in archaeological populationsseems to follow this developmental pattern.

There are at least three processes which may ac-count for the association between enamel hypopla-sias developing between 3.5 and 7.0 years of age anddecreased life expectancy in adolescence/adulthood.First, this association may result from differential life-long patterns of biological susceptibility to physiolog-ical disruptions. An increased susceptibility to stressmay cause both an increased frequency of childhoodhypoplasias and an earlier age at death. That is, in-dividuals who are ill during childhood may continueto fall ill as adults, due to a "weak constitution".Second, individuals who were exposed to and sur-vived a period of severe childhood stress may suffera loss in ability to respond to other stresses. In asense, these individuals are "biologically damaged"by the early stress. The wear and tear of stresses dur-ing development may render them less fit to respondto and survive subsequent stresses. Third, these datamay result from differential lifelong patterns of be-havior ally and culturally based exposure to stressors.An increased lifelong potential for exposure to stres-

40

35

30

25

20

Age at Death (Years)

L. W. M. A. L. W. M. M. TOTAL

Cultural HorizonsH I No Hypoplasia8 Y//X One Hypoplasia KSS i 2-3 Hypoplasias

Fig. 3 —Mean ages at death of Dickson Mounds adolescents/adultsby number of hypoplasia-stress periods between 3.5 and 7.0 yearsof developmental age. LW = Late Woodland, MALW — Missis-sippian Acculturated Late Woodland, MM = Middle Mississippian(Goodman and Armelagos, 1988).

40 n

J3Q.oQ.X

*S 20n

I io

• Maxillary TeethB Mandibular Teeth

Fig. 4 —Comparison of the frequency of enamel defects by toothtype based on 30 individuals from the Dickson Mounds (Goodmanand Armelagos, 1985b).

11 12 Pmi Pm2 M2

Fig. 5 —The frequency of enamel hypoplasias by incisal/occlusal,middle, and cervical crown thirds of maxillary (upper row) andmandibular (lower row) permanent tooth type, II to M2 (Goodmanand Armelagos, 1985b).




sors may cause both an increased frequency of child-hood stress and earlier ages at death.

While these data have been largely unable to dis-tinguish among these mechanisms, it is suggestedthat a cultural buffering hypothesis is most congruentwith the patterns of association. The greatest differ-ence in mean longevity between those with and with-out hypoplasias/stress is in tljie MM, the horizon inwhich status differences are! likely to be greatest(Rothschild, 1979).

Although the cultural buffering hypothesis is sup-ported, this does not exclude a role for a "biologicaldamage" mechanism. Low socio-economic statusduring childhood may promote disease and under-nutrition, which leaves individuals less able to rallyfrom future insults. Most important, the data stronglysupport the notion that enamel defects are indicatorsof stress and that this stress is highly meaningful interms of life expectancy. In sum, because enamel de-fects are relatively indelible, they may provide a uniquetool for analysis of the long-term consequences ofstress during early development.

A commonly held view contends that all teeth de-veloping at the time of a disruption will be equallylikely to develop a hypoplasia (cf. Cameroon and Sims,1974; Sharawy and Yaeger, 1986). Our data, however,suggest that there are wide differences in suscepti-bility to hypoplasias among teeth developing at sim-ilar times (Goodman and Armelagos, 1985b).

A variety of unexplored factors, other than age atcrown formation, may explain this apparent differ-ence in susceptibility. The differences in frequency ofdefects among teeth developing at the same time maybe due to differences in "genetic canalization" anddevelopmental stability (cf. Waddington, 1957). Themore genetically stable or canalized teeth may be morehypoplastic because, in a sense, they are unable toalter growth by changing velocity of development.Thus, matrix apposition occurs on time, but the qual-ity of enamel suffers. Also, the polar and most stableteeth of developmental fields (cf. Butler, 1939; Dahl-berg, 1945) are generally the most hypoplastic.

The paucity of defects on the incisal/occlusal thirdsof teeth could be due to attrition. However, this pat-tern holds in this population even for the youngestindividuals with recently erupted teeth. Thus, it issuggested that all teeth display similar within-toothhypoplasia patterns due to common morphologicalor physiological factors, such as within-tooth varia-tion in rate of enamel apposition, length of prisms,prism direction and angle, and number of active se-cretory-phase ameloblasts. We have suggested thatlong prisms are most consistently associated withenamel defects (Goodman and Armelagos, 1985b).However, we are unable to determine the physiolog-ical significance of long prisms. For example, areameloblasts which secrete at a high velocity most atrisk of disruption, or is the risk of a defect simplyproportional to the amount of matrix formed by anameloblast?

The study of enamel defects in anthropology is ex-panding on many fronts. For example, Skinner (1986)has shown that enamel defects are very common inthe gorilla. However, these defects are far less com-mon in both Old and New World monkeys (Vitzthumand Wikander, 1988). This variability across speciesmay be significant to our understanding of the above-noted variations within species.

Anthropological analyses of enamel hypoplasias asindicators of stress have spread from studies of ar-chaeological to historical (Goodman, 1988) and con-temporary groups (Goodman et al., 1987). Studies ofhypoplasias in contemporary groups living undermarginal conditions may add perspective to the pre-historic data. However, since methods for the analy-sis of general stress during infancy and childhood aregenerally poor, these contemporary studies may provemost important if we find that enamel defects arehighly reflective of stress levels. This is one area ofstudy where anthropologists are beginning to workwith nutritional scientists, and where cooperation withother dental researchers is needed.

In summary, with increased interest in the ecologyand evolution of humans, enamel hypoplasia hasemerged as a frequently used indicator of dietary anddisease stress. Recent studies have effectively dis-criminated levels of stress, indicated by the frequencyof hypoplasia, between sexes, age groups, socialclasses, and time-successive populations (Rose et al.,1985). A variety of benefits can be seen in cooperationbetween prehistorians and other dental researchers.Prehistorians need more precise information on thecauses of enamel defects, while "dry skull" studiesmay provide unique research opportunities, inclu-ding an ability to study the evolution of nutrition andhealth.

ACKNOWLEDGMENT

The author wishes to acknowledge Grace Suck-ling's pioneering studies, which have inspired thiswork. All shortcomings of this paper, however, aresolely the responsibility of the author.

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dental enamel hypoplasias in prehistoric populations

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