Linear enamel hypoplasia as an indicator of physiological stress in great apes: reviewing the evidence in light of enamel growth variation

Physiological stress, such as malnutrition or illness, can disrupt normal enamel growth, resulting in linear enamel hypoplasias (LEHs). Although ecological factors may contribute to LEH expression, other factors, such as surface abrasion and enamel growth variables, are also likely to be involved. Attention to these other factors is necessary before we can begin to understand what LEH might signify in terms of ecological sources of physiological stress in non-human primates. This study focuses on assessing the contribution of these other factors to variation in LEH expression within and across great ape taxa. Here, we present LEH data from unabraded crown regions in samples of seven great ape species. We analyze these data with respect to lateral enamel formation time and the angles that striae of Retzius make with the enamel surface, as these variables are expected to affect variation in LEH expression. We find that although the duration of enamel formation is associated with sex differences in LEH expression, it is not clearly related to taxonomic variation in LEH expression, and does not explain the low frequency of LEH in mountain gorillas found in this and a previous study. Our data on striae of Retzius angles suggest that these influence LEH expression along the tooth crown and may contribute to the consistently high frequencies of LEH seen in Pongo in this and previous studies. We suggest that future work aimed at understanding species variation in these angles is crucial to evaluating taxonomic patterns of LEH expression in great apes.     

Macroscopic and microscopic analyses of linear enamel hypoplasia in Plio-Pleistocene South African hominins with respect to aspects of enamel development and morphology

This study uses macroscopic and microscopic methods to analyze the expression of linear enamel hypoplasia (LEH) in Plio-Pleistocene South African hominins. LEH is a developmental defect of enamel that is used in many anthropological contexts as a physiological stress indicator. Previous research has not settled the question as to whether differences in LEH expression exist between Paranthropus and Australopithecus and if they exist, to what extent these differences might be explained simply by taxonomic differences in enamel development and morphology rather than by differential stress experience. In this study, the analysis of LEH is conducted with respect to differences between Paranthropus and Australopithecus in aspects of enamel development and morphology that are thought to influence LEH expression. Two factors impacting LEH expression are considered: the duration of enamel formation, and the spacing of perikymata. It is predicted that if the first factor strongly influences the expression of LEH, then there should be fewer defects per tooth in Paranthropus because of its abbreviated crown formation spans (and fast extension rates) relative to Australopithecus. It is also predicted that because Australopithecus has more densely packed perikymata in comparable regions of the crown than Paranthropus, this taxon should, on average, have narrower defects than Paranthropus. To address these questions, 200 Australopithecus and 137 Paranthropus teeth were examined for LEH, and the analysis of defect width with respect to perikymata spacing was conducted on tooth impressions examined under a scanning electron microscope using INCA (Oxford Instruments) measurement software. Data support the first prediction: Australopithecus does have significantly more defects per canine tooth than Paranthropus. Data do not support the second prediction in large part because several Australopithecus specimens have wide groove defects in which perikymata are not visible and enamel is irregular. Such wide grooves are not predicted by perikymata spacing such that alternative explanations, including taxonomic differences in ameloblast sensitivity and the duration/severity of disruptions to enamel growth, must be considered.     

Missing defects? A comparison of microscopic and macroscopic approaches to identifying linear enamel hypoplasia

Linear enamel hypoplasia (LEH), the presence of linear defects of dental enamel formed during periods of growth disruption, is frequently analyzed in physical anthropology as evidence for childhood health in the past. However, a wide variety of methods for identifying and interpreting these defects in archaeological remains exists, preventing easy cross‐comparison of results from disparate studies. This article compares a standard approach to identifying LEH using the naked eye to the evidence of growth disruption observed microscopically from the enamel surface. This comparison demonstrates that what is interpreted as evidence of growth disruption microscopically is not uniformly identified with the naked eye, and provides a reference for the level of consistency between the number and timing of defects identified using microscopic versus macroscopic approaches. This is done for different tooth types using a large sample of unworn permanent teeth drawn from several post‐medieval London burial assemblages. The resulting schematic diagrams showing where macroscopic methods achieve more or less similar results to microscopic methods are presented here and clearly demonstrate that “naked‐eye” methods of identifying growth disruptions do not identify LEH as often as microscopic methods in areas where perikymata are more densely packed. Am J Phys Anthropol 153:463–472, 2014. © 2013 Wiley Periodicals, Inc.     

Brief communication: Comparison of methods for estimating chronological age at linear enamel formation on anterior dentition

Linear enamel hypoplasia (LEH) is an enamel defect that records the effects of physiological stress on tooth formation. Estimating the age at which LEH defects form is integral to the reconstruction of population health in bioarcheological studies. Two principal methods for aging LEH defects have been introduced in the literature. The conventional approach employs regression equations based on a linear model of tooth growth. The newer, Reid and Dean [Am J Phys Anthropol 113 (2000) 135-139] approach, is based upon a histologically derived curvilinear model of enamel development and therefore likely provides more accurate age estimates. However, the extent to which the Reid and Dean method produces estimated ages at defect formation differing from those of the regression equations has not, until now, been determined. This study quantifies the differences between these two methods. Evaluating the degree to which these methods differ is essential for interpreting the accuracy of LEH age estimates given in previous bioarcheological studies. Age estimates of LEH defects on 338 anterior teeth from the Hamann-Todd osteological sample were calculated using both methods. The resulting estimated ages were compared through a randomized block ANOVA. However, the mean differences between the estimated ages yielded by both methods range from 4 months or less depending on the tooth type with an overall average of 2.63 months. The discussion focuses on the degree to which this difference affects answers to bioarcheological questions.     

Plasticity and constraint in response to early‐life stressors among late/final jomon period foragers from Japan: Evidence for life history trade‐offs from incremental microstructures of enamel

This study evaluates two hypotheses that address how Late/Final Jomon period people responded to early‐life stress using linear enamel hypoplasia (LEH) and incremental microstructures of enamel. The first hypothesis predicts that Jomon people who experienced early‐life stressors had greater physiological competence in responding to future stress events (predictive adaptive response). The second hypothesis predicts that Jomon people traded‐off in future growth and maintenance when early investment in growth and survival was required (plasticity/constraint). High resolution tooth impressions were collected from intact, anterior teeth and studied under an engineer's measuring microscope. LEH were identified based on accentuated perikymata and depressions in the enamel surface profile. Age of formation for each LEH was estimated by summing counts of perikymata and constants associated with crown initiation and cuspal enamel formation times. The relationship between age‐at‐first‐defect formation, number of LEH, periodicity between LEH, and mortality was evaluated using multiple regression and hazards analysis. A significant, positive relationship was found between age‐at‐death relative to age‐at‐first‐defect formation and a significant, negative relationship was found between number of LEH relative to age‐at‐first‐defect formation. Individuals with earlier forming defects were at a significantly greater risk of forming defects at later stages of development and dying at younger ages. These results suggest that Late/Final Jomon period foragers responded to early‐life stressors in a manner consistent with the plasticity/constraint hypothesis of human life history. Late/Final Jomon period individuals were able to survive early‐life stressors, but this investment weakened responses to future stress events and exacerbated mortality schedules. Am J Phys Anthropol 155:537–545, 2014. © 2014 Wiley Periodicals, Inc.     

Preferential expression of linear enamel hypoplasia on the sectorial premolars of rhesus monkeys (Macaca mulatta)

Three hundred and sixty rhesus macaque specimens at the Caribbean Primate Research Center were examined for evidence of linear enamel hypoplasia (LEH). A previously unreported intertooth pattern in LEH was observed. Defects occur preferentially on the sectorial premolar of both males and females. Relative to other teeth, the sectorial premolar exhibits more prominent defects and is more likely to exhibit multiple defects. This pattern is unlike the human intertooth LEH pattern and unlike patterns previously reported for monkeys and apes. These observations are discussed in the context of factors thought to influence the intertooth distribution of LEH in humans and in nonhuman primates. The authors reject crown height, the timing of crown development, and the duration of crown formation as factors contributing to the observed pattern and favor an explanation involving enamel thickness, perikymata spacing, and/or prism orientation. Am J Phys Anthropol 107:179–186, 1998. © 1998 Wiley-Liss, Inc.     

Brief communication: physiological stress in the Florida Archaic-enamel hypoplasia and patterns of developmental insult in early North American hunter-gatherers

We examined the prevalence and developmental timing of linear enamel hypoplasias (LEHs) in an early Archaic Floridian population from Windover (8,120-6,980 (14)C years B.P. uncorrected). Using digital images, mandibular and maxillary canines were analyzed for defect prevalence and timing of insults. Although overall prevalence was very weakly correlated with earlier defect timing, there were significant differences in defect prevalence that varied by sex and tooth type. The mean LEH count in male mandibular canines was far higher than in male maxillary canines or in female mandibular or maxillary canines. We examined defect timing as a possible predictor of the sex differences in LEH prevalence. There were no significant sex differences in the developmental timing of the earliest defects in either tooth class. Developmental timing is not responsible for the sex differences seen in defect prevalence in mandibular canines.     

Prevalence and the duration of linear enamel hypoplasia: a comparative study of Neandertals and Inuit foragers

As a dental indicator of generalized physiological stress, enamel hypoplasia has been the subject of several Neandertal studies. While previous studies generally have found high frequencies of enamel hypoplasia in Neandertals, the significance of this finding varies with frequencies of enamel hypoplasia in comparative samples. The present investigation was undertaken to ascertain if the enamel hypoplasia evidence in Neandertals suggests a high level of physiological stress relative to a modern human foraging group, represented here by an archaeological sample of Inuit from Point Hope, Alaska. Unlike previous studies, this study focused specifically on linear enamel hypoplasia (LEH), emphasizing systemic over localized causes of this defect by considering LEH to be present in an individual only if LEH defects occur on two anterior teeth with overlapping crown formation periods. Moreover, this study is the first to evaluate the average growth disruption duration represented by these defects in Neandertals and a comparative foraging group. In the prevalence analysis, 7/18 Neandertal individuals (from Krapina and southern France) and 21/56 Neandertal anterior teeth were affected by LEH, or 38.9% and 37.5% respectively. These values do not differ significantly from those of the Inuit sample in which 8/21, or 38.1% of individuals, and 32/111, or 28.8% of anterior teeth were affected. For the growth disruption duration analysis, 22 defects representing separate episodes of growth disruption in Neandertals were compared with 22 defects in the Inuit group using three indicators of duration: the number of perikymata (growth increments) in the occlusal walls of LEH defects, the total number of perikymata within them, and defect width. Only one indicator, the total number of perikymata within defects, differed significantly between the Inuit and Neandertal groups (an average of 13.4 vs. 7.3 perikymata), suggesting that if there is any difference between them, the Inuit defects may actually represent longer growth disruptions than the Neandertal defects. Thus, while stress indicators other than linear enamel hypoplasia may eventually show that Neandertal populations were more stressed than those of modern foragers, the evidence from linear enamel hypoplasia does not lend support to this idea.     

Variation in modern human enamel formation times

Most of what we know about the timing of human enamel formation comes from radiographic studies on children of known age. Here, we present new longitudinal data derived from a histological analysis of tooth enamel. Two samples, one from southern Africa and one from northern Europe, contained all anterior and molar tooth types. Two further samples contained only one tooth type: canines from a medieval Danish sample and third molars from a modern North American sample. Data were collected on 326 molars and 352 anterior teeth. Each tooth was sectioned and prepared for polarized light microscopy. We used daily enamel cross striations to determine cuspal enamel formation time, recorded the periodicity of long-period striae in the lateral enamel, and used this value to calculate enamel formation times for each decile of crown length. We present data that reveal some of the processes whereby differences in enamel formation times arise between our samples. Mean cuspal enamel formation times were similar in southern African and northern European anterior teeth, but differed in certain molar cusps. All the southern African anterior teeth completed enamel formation earlier. The greatest difference in mean chronological age at enamel completion was 5.2 vs. 6.2 years of age in lower canines. However, enamel completion times in the molar teeth showed few differences between the samples, with mean times for the longest forming cusps all falling between 3.0 years and 3.45 years. Our data suggest fewer differences between samples and smaller ranges of variation than in many radiographic studies and present a more realistic picture of worldwide variation in enamel formation times.     

Linear enamel hypoplasia in gibbons (Hylobates lar carpenteri)

This study describes the expression of linear enamel hypoplasia (LEH), a sensitive dental indicator of physiological stress, in Thailand gibbons (Hylobates lar carpenteri). Previous studies of enamel hypoplasia in hominoids have focused on great apes, with little attention given to the expression of this stress indicator in gibbons. In that gibbons differ from both monkeys and great apes in numerous life history features, LEH expression in gibbons might be expected to show significant differences from both. In this study, 92 gibbon specimens from two sites in Thailand were compared with several samples of monkeys and great apes in their expression of LEH. The intertooth distribution of LEH in gibbons was compared to that of chimpanzees and rhesus monkeys. Gibbon populations from both sites exhibit LEH frequencies intermediate between those of the monkey samples, in which LEH prevalence is usually low, and those of the great ape samples, in which LEH prevalence is high. Gibbons differ significantly from monkeys, but not great apes, in the number of individuals whose teeth record multiple stress events. Multiple episodes of stress are rarely recorded in the teeth of monkeys, while multiple stress events occur with higher frequency in gibbons and great apes. Taxonomic variation in the duration of crown formation, the prominence and spacing of perikymata on dental crowns, life history features, and/or experience of physiological stress may explain these patterns. The intertooth distribution of LEH in gibbons is, for different reasons, unlike that of either chimpanzees or rhesus monkeys. The mandibular canines of gibbons have significantly more LEH than any of their other teeth. Aspects of crown morphology, perikymata prominence/spacing, enamel thickness, and crown formation spans are potential causes of taxonomic variation in the intertooth distribution of LEH.     

Age of linear enamel hypoplasia formation based on Massler and colleagues’ and Reid and Dean's standards in a Polish sample dated to 13th–18th century CE

In the study of enamel hypoplasia formation ages basically two standards of dental development are being applied. According to some authors, different methods produce different results, thus it is critical to decide which method to use. This study focuses on the comparison of three methods for estimating ages of linear enamel hypoplasia (LEH) formation.     

Prevalence and etiology of linear enamel hypoplasia in monkeys and apes from Asia and Africa

Ninety-seven specimens of sympatric monkeys and apes from East Malaysia and 115 monkeys and apes from West Africa are examined in order to evaluate the magnitude and nature of the great ape-monkey linear enamel hypoplasia (LEH) 'dichotomy'. This study demonstrates that great apes from both regions have a higher incidence of LEH and repetitive LEH than do gibbons and monkeys. However, the authors find that the dichotomy is not as clear-cut as previous research suggests, since some monkey samples exhibit high LEH frequencies. The authors evaluate the potential influence of great ape-monkey differences in crown height on this dichotomy. They show that canine crown height variation is weakly associated with LEH variation. Differences between monkeys and great apes in their crown formation spans and in their experience of environmental stress may be more likely causes of the dichotomy.     

禄丰古猿牙齿釉质发育不全的观察研究

对出自禄丰石灰坝的26个禄丰古猿下颌齿列的246枚恒齿进行了观察研究,发现禄丰古猿具有普遍的带状釉质发育不全（LEH）现象,个体LEH比例为100%,恒齿LEH比例为85%。乳齿几乎没有LEH现象,第一恒臼齿的LEH比例也很低仅57%。根据牙齿萌出顺序及现代大猿的牙齿发育年龄特征,作者推断2—3岁之前的幼儿古猿很少出现釉质发育不全现象,这可能与母体的营养关照有关。禄丰古猿的LEH的发生频率具有明显的季节性,结合中新世晚期气候变化特征、古猿的生态环境、生活习性及食性特征分析,作者推测：季节性营养不良可能是造成禄丰古猿釉质发育不全的主要原因。     

Frequency and chronological distribution of linear enamel hypoplasia in a North American colonial skeletal sample

A skeletal sample of 44 individuals born and raised in early 18th century frontier settlements of Northeastern United States is examined for the frequency and chronological distribution of linear enamel hypoplasia (LEH) on the maxillary and mandibular incisors and canines. The prevalence of LEH ranged from 31% on the I² to 66% on the mandibular C and the mean number of defects ranged from .59 on the I² to 1.08 on the mandibular C. These frequencies were generally lower than those reported for two later samples: the Monroe County Poorhouse sample and the Hammon-Todd sample. Individuals in these latter two samples were derived from the lowest socioeconomic stratum of their respective populations. Frequency differences are explained within the context of the changing availability of resources that resulted from the rise of industrialization, urbanization, and wage labor which took place during the 18th and 19th centuries. The frequency of LEH was low prior to 1.5 years of age and may result from attrition and/or decreased susceptibility in the relevant area of the crown or from low morbidity or high mortality. Peak frequencies are observed in all age categories ranging from 2.5 to 3.0 years up to 4.0 to 4.5 years and are too late to result from weaning. Instead, they may reflect the susceptibility of nonimmune children to diseases that were common in colonial North America. As the majority of these diseases were not fatal, most victims who survived may have had one or more LEHs as visible proof of their earlier encounter(s). © 1996 Wiley-Liss, Inc.     

Analysis and significance of linear enamel hypoplasia in Plio-Pleistocene hominins

This study of linear enamel hypoplasia (LEH) in Plio-Pleistocene hominins builds on a previous study (Guatelli-Steinberg [2003] Am. J. Phys. Anthropol. 120:309-322) that focused on LEH in early South African hominins. The present study is more comprehensive, encompassing dental specimens of hominins from East Africa as well, including early Homo. As a developmental defect of enamel, LEH is used in anthropological contexts to reveal information about physiological stress. However, intrinsic aspects of enamel development and morphology can affect the expression of LEH, complicating efforts to understand the significance of these defects. In this study, the analysis of LEH is conducted with respect to enamel development and morphology. It is predicted that Paranthropus should have fewer defects on its canine teeth than Australopithecus and Homo, owing to its abbreviated period of enamel formation. This prediction is supported: Paranthropus has statistically significantly fewer defects per canine than Australopithecus and Homo. The previous study demonstrated that despite the wider spacing of perikymata on the teeth of South African Paranthropus, defects on the canine teeth of this genus were not wider than those of Australopithecus. A multiple linear regression analysis in that study, as well as a separate analysis in the present study, indicate that the number of perikymata within defects is a better predictor of defect width than perikymata spacing. In this study, it was additionally found that the average number of perikymata within Australopithecus defects is statistically significantly greater than it is in Paranthropus, thus explaining why Paranthropus defects are not wider than those of Australopithecus. The biological significance of this difference in the number of perikymata within the defects of Australopithecus and Paranthropus is considered in light of several factors, including: 1) the possibility that other intrinsic attributes of enamel morphology may be involved (specifically the faster extension rates of Paranthropus that result in shallower defects), 2) generic differences in the canalization of enamel development, and 3) generic differences in the duration of disruptions to enamel growth.     

Subadult stress,morbidity, and longevity in Latte Period populations on Guam,Mariana Islands

The frequency and age distribution of linear enamel hypoplasia (LEH) in the dentition of 293 individuals from Latte Period sites (AD 800–1521) on Guam, Mariana Islands, are examined in this study. Individuals dying as subadults (before age 16) and as young adults (ages 16–21) have more frequent LEHs than those who survived to middle or late adulthood, documenting a relationship between LEH-causing stress events and reduced life expectancy. The age distributions of cribra orbitalia and skeletal infection in children who died by age 10 exhibit striking similarities to the etiological age patterns of LEH in children, and those with skeletal infection have more frequent hypoplasias than children without infection. The comorbidity of systemic stress and infection in children, and their impact on life expectancy, are interpreted in the biocultural context of high population density in the large coastal villages of the late prehistoric period in the Marianas. Am J Phys Anthropol 104:363–380, 1997. © 1997 Wiley-Liss, Inc.     

Linear enamel hypoplasia in the great apes: analysis by genus and locality

Most studies report a high prevalence of linear enamel hypoplasia (LEH) in the great apes relative to other nonhuman primates and some human populations. It is unclear if this difference is a direct result of poor health status for the great apes, or if it represents differential incidence due to a lower threshold (sensu Goodman and Rose, 1990 Am. J. Phys. Anthropol. [suppl.] 33:59-110) for the occurrence of enamel hypoplasia among great apes. This study uses the Smithsonian National Museum of Natural History's great ape collection to examine the prevalence of LEH, the most common type of hypoplasia observed. Frequencies of LEH are reported, as well as analyses by taxa and provenience. The study sample consists of 136 specimens and includes 41 gorillas, 25 chimpanzees, and 70 orangutans. Analyses of frequencies are presented for both individuals and teeth by taxonomic category and locality. Among the individuals in this study, 63.97% are affected by LEH. Overall, gorillas (29.27%) exhibit lower frequencies of LEH than chimpanzees (68.00%) and orangutans (82.86%). There is a marked difference in LEH frequencies between mountain and lowland gorillas. There is no difference in LEH frequencies between Sumatran and Bornean orangutans. A range of variation for the great apes in enamel hypoplasia frequencies is found when taxon and locality are considered. It is likely that both biological and environmental factors influence the high frequencies of enamel hypoplasia exhibited in the great apes.     

Response of bone and enamel formation to nutritional supplementation and morbidity among malnourished Guatemalan children

The effects of changes in nutritional and health status upon bone and enamel development are examined in a sample of 63 rural Guatemalan children (24 females, 39 males). The number of ossified hand-wrist centers at 3 years and the number of linear enamel hypoplasias (LEH) in ～0–3 year zones of developing teeth were used to monitor the response of bone mineralization and enamel matrix formation to illness and nutritional supplementation. Numbers of ossified centers and LEH were compared across sex, supplementation, and morbidity groups. Enamel matrix secretion responded positively to increased supplementation. Children who received less than 34.25 kcal/day in supplement had more LEH than those who received more supplement. No differences in ossification status were found between supplementation groups. These data suggest that enamel formation may be more sensitive to changes in nutritional status than is bone mineralization. Disruptions of bone and enamel formation were both associated with frequent illness. Children who were ill more than 3.6% of the time had more LEH and fewer ossified hand-wrist centers than children who were less frequently ill. Conclusions regarding relative environmental sensitivity must take into account the specific aspects of dental and skeletal development examined. © 1993 Wiley-Liss, Inc.     

Brief communication: dental development and enamel thickness in the Lakonis Neanderthal molar

Developmental and structural affinities between modern human and Neanderthal dental remains continue to be a subject of debate as well as their utility for informing assessments of life history and taxonomy. Excavation of the Middle Paleolithic cave site Lakonis in southern Greece has yielded a lower third molar (LKH 1). Here, we detail the crown development and enamel thickness of the distal cusps of the LKH 1 specimen, which has been classified as a Neanderthal based on the presence of an anterior fovea and mid-trigonid crest. Crown formation was determined using standard histological techniques, and enamel thickness was measured from a virtual plane of section. Developmental differences include thinner cuspal enamel and a lower periodicity than modern humans. Crown formation in the LKH 1 hypoconid is estimated to be 2.6-2.7 years, which is shorter than modern human times. The LKH 1 hypoconid also shows a more rapid overall crown extension rate than modern humans. Relative enamel thickness was approximately half that of a modern human sample mean; enamel on the distal cusps of modern human third molars is extremely thick in absolute and relative terms. These findings are consistent with recent studies that demonstrate differences in crown development, tissue proportions, and enamel thickness between Neanderthals and modern humans. Although overlap in some developmental variables may be found, the results of this and other studies suggest that Neanderthal molars formed in shorter periods of time than modern humans, due in part to thinner enamel and faster crown extension rates.     

Under restrictive conditions,can the widths of linear enamel hypoplasias be used as relative indicators of stress episode duration?

Linear enamel hypoplasia (LEH), a type of enamel defect reflecting nonspecific physiological stress, has traditionally been used by bioarchaeologists to assess human health. Initially, measurements of defect width were used to estimate the duration of stress episodes. More recently, methods of counting within-defect perikymata (enamel growth increments) were developed to more accurately assess duration. Because perikymata are often not continuously visible within defects, while widths can usually be measured, the primary purpose of this article was to determine if, under restrictive conditions, the widths of LEH defects might be used as relative indicators of stress episode duration. Using a set of dental replicas from the prehistoric Irene Mound (1150-1400 A.D.), this study also investigated potential sources of variation in defect widths and how often defect widths could be measured and within-defect perikymata counted. Of 120 defects, only 47 contained both measurable defect widths and total within-defect perikymata, while 79 had measurable defect widths. Regression analysis revealed that, for these 47 defects, defect widths were more strongly related to the total number of within-defect perikymata than they were to crown region or tooth type. Although wide prediction intervals indicated that a defect's width could not be used to predict the number of within-defect perikymata for an individual, narrower confidence intervals associated with hypothetical mean population widths suggested that mean defect widths might be used to rank populations in terms of relative average stress episode duration.