Life history, enamel formation, and linear enamel hypoplasia in the Ceboidea

Linear enamel hypoplasia (LEH), a developmental defect of enamel, increases in frequency from prosimian to monkey to lesser ape to great ape grades (Guatelli-Steinberg 2000 Am. J. Phys. Anthropol. 112:395-410, [2001] Evol. Anthropol. 10:138-151; Newell 1998 Ph.D. dissertation, Temple University). This taxonomic pattern in the distribution of LEH is closely related to maturation length across the primate order (Newell 1998 Ph.D. dissertation, Temple University, 2000 Am. J. Phys. Anthropol. [Suppl.] 30:236). Longer maturation periods are associated with higher LEH frequencies; they appear to provide greater opportunity for defects to form. The present study explores the relationship between maturation length and LEH frequency within the Ceboidea. Because of its prolonged period of growth, Cebus is predicted to manifest LEH at a higher frequency than the more rapidly maturing ceboid genera. To test this hypothesis, two separate researchers (E.A.N. and D.G.-S.) examined LEH in nonoverlapping museum series of ceboids. The results support the hypothesis: in 13 genera (n = 1,276), E.A.N. found that LEH frequencies ranged from 0% in Callicebus, Cebuella, and Saimiri to 20% in Cebus. D.G.-S. found similar frequencies among five genera (n = 107), from 0% in Saimiri to 32% in Cebus. Thus, the broad pattern of LEH distribution evident across major taxonomic groups of primates is repeated within the Ceboidea. We also examined a related hypothesis linking the spacing of perikymata, which is influenced by enamel extension rates (Shellis 1998 J. Hum. Evol. 35:387-400), to LEH. The most likely areas of tooth crowns to exhibit LEH in human teeth are those in which perikymata are most closely spaced (Hillson and Bond 1997 Am. J. Phys. Anthropol. 104:89-103). We hypothesized that the longer-maturing Cebus, with its elevated LEH frequency, will also exhibit more closely spaced perikymata than other ceboids. Analysis of a small microscopic subsample (n = 8) lends limited support to this second hypothesis.     

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.     

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.     

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.     

Gross enamel hypoplasia in molars from subadults in a 16th-18th century London graveyard

Dental Enamel Hypoplasia has long been used as a common nonspecific stress indicator in teeth from archaeological samples. Most researchers report relatively minor linear and pitted hypoplastic defects on tooth crown surfaces. In this work we report a high prevalence and early age of onset of extensive enamel defects in deciduous and permanent molars in the subadults from the post-medieval cemetery of Broadgate, east central London. Analysis of the dentition of all 45 subadults from the cemetery, using both macroscopic and microscopic methods, reveals disturbed cusp patterns and pitted, abnormal and arrested enamel formation. Forty-one individuals from this group (93.2%) showed some evidence of enamel hypoplasia, 28 of them showing moderate or extensive lesions of molars, deciduous or permanent (63.6% of the sample). Scanning Electron Microscope images reveal many molars with grossly deformed cuspal architecture, multiple extra cusps and large areas of exposed Tomes' process pits, where the ameloblasts have abruptly ceased matrix production, well before normal completion. This indented, rough and poorly mineralized surface facilitates both bacterial adhesion and tooth wear, and when such teeth erupt fully into the mouth they are likely to wear and decay rapidly. We suggest that this complex combination of pitted and plane-form lesions, combined with disruption of cusp pattern and the formation of multiple small cusps, should henceforth be identified as "Cuspal Enamel Hypoplasia."     

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.     

Meaningful measures of enamel hypoplasia: Prevalence and comparative intensity of developmental stress

Objectives

Developmental stress causing enamel thinning is an important topic in primate biology. Because taxa differ in growth rates and enamel thickness, the goal is to provide a new method allowing direct comparison of prevalence and salience of enamel defects among samples.

Materials and Methods

Casts of ape teeth spanning the Late Pleistocene to Late Miocene from three site areas of increasing seasonality, equator (Sumatra) to 20° (Vietnam) and 25°N latitude (China), were examined for enamel defects among paleo-orangutans (n = 571, 222, respectively) and Lufengpithecus lufengensis (n = 198). Frequency of affected teeth and number of linear enamel hypoplasia were recorded. Defect dimensions were measured with a confocal microscope. Simple prevalence is compared to weighted prevalence (%), calculated by dividing “number of LEH from specific tooth groups” by “specific tooth sample size”; this quantity divided by “tooth-specific years of imbricational enamel formation.” Defect dimensions are reduced to a dimensionless index termed “enamel deficit ratio” through dividing “daily enamel deficit” by “daily secretion rate.”

Results

Weighted prevalence increases to the North, highlighting latitudinal similarities. In contrast, “enamel deficit ratio,” designed to express comparative severity of developmental stress among samples, was least in the high latitude sample and differed little between paleo-orangutan samples.

Discussion

The actual numbers generated are not as important as efficacy of the proposed methods for other taxa. Developmental stress appears least severe in the high latitude (Lufengpithecus) sample but affects a greater proportion, compared to paleo-orangutans. Regardless of findings, the proposed solutions to improve comparability of disparate samples, yield reasonable results.     

Invisible impacts but long-term consequences: hypoplasia and contact in central Australia

The dental casts taken of Aboriginal people resident at Yuendumu, Central Australia, between 1950-1970 preserve a unique historical record of defects of the dental enamel (DDEs) among people born from 1890-1960 (n = 377). These data are used, in comparison with precontact data, to trace the chronological changes in childhood development that occurred among Aboriginal people from the point of initial engagement with white settlers to a period of overwhelming government control. The results demonstrate very little change in the frequency of DDE from the precontact period to 1929 but increases after that time, particularly after the forcible settlement of people on a government establishment at Yuendumu in 1946. Apart from the absolute increase in frequency, it is also clear that population variation decreased markedly, with growing numbers of children experiencing multiple defects in early childhood (ca. 0.8-1.5 years of age). The results also indicate that an early onset of DDE constituted a risk for further episodes. These changes in DDE correspond to periods of increasingly intense contact between Aboriginal people and Europeans and with changes to government policy aimed at assimilating the indigenous population. Such policies had marked costs for childhood development. The lack, however, of a visible marker of initial contact demonstrates the importance of the intensity of and motives behind interactions between indigenous and colonial populations in determining the health consequences of colonial encounters.     

Amelogenesis imperfecta in the dentition of a wild chimpanzee

This report describes a case of amelogenesis imperfecta in the dentition of a female chimpanzee. Amelogenesis imperfecta is a group of rare genetic conditions that create severe enamel defects, which, although well researched in humans, has not yet been investigated in wild non‐human primates.     

Some orangutans acquire enamel defects at regular intervals,but not according to seasonal cycles

Objectives

Developmental defects of tooth enamel are associated with systemic physiological stress and have been linked to seasonal environmental factors such as rainfall, temperature, and fruit availability. Here, we evaluate whether linear enamel hypoplasia and accentuated perikymata occur with any cyclicity on lower canines and then whether cycles differ between Bornean and Sumatran orangutans.

Materials and Methods

Epoxy casts of lower canines from Pongo abelii (n = 14) and P. pygmaeus (n = 33) were evaluated for perikymata and dental enamel defects. Individual developmental sequences (IDSs) were generated for each canine, tracking the position of each defect in the context of continuous perikymata (time). Autocorrelation, a form of time-series statistical analysis was run for each canine to identify whether any cyclicity of defect expression was discernable.

Results

Autocorrelation revealed cycles of defect expression within canines, but no common cycle periodicities were identified between individuals of the same species or across species. P. pygmaeus averaged more linear enamel hypoplasia per year than P. abelli, but no other comparisons (number of defects, number of perikymata between defects, and autocorrelation analysis) revealed differences between the species.

Discussion

Although no common patterns of defect expression were identified within or between P. abelli and P. pygmaeus, the potential for autocorrelation analysis is promising for primatological and paleoanthropological studies of seasonal phenomena.

     

Patterns of enamel hypoplasia in two medieval populations from Nubia's Batn el Hajar

Analysis of enamel hypoplasia frequencies for two medieval populations representing the earliest and latest Christian periods of ancient Nubia reveals important diachronic shifts in childhood stress. The mean frequency for hypoplastic bands among the early Christians is 4.2, while the late Christian sample has a mean frequency of 3.7. In addition, the earlier Christians show a prolongation of hypoplastic occurrences through childhood corresponding to a prolonged period of intensified childhood mortality. The modal time interval between hypoplastic occurrences is also shorter for the early Christian children. A comparison of hypoplasia frequencies by sex also reveals a pattern of considerable interest. Females show both lower frequencies of hypoplasias as well as a delay in onset. The diachronic differences are consistent with other indications from paleopathology and paleodemography that childhood stress decreased in later Christian times. The sex differences suggest that during the infancy and early childhood females were more resilient than their male counterparts.     

Brief communication: linear enamel hypoplasia and the shift from irregular to regular provisioning in Cayo Santiago rhesus monkeys (Macaca mulatta)

This study investigates changes in the prevalence of linear enamel hypoplasia (LEH) before and after the shift from irregular to regular provisioning in the Cayo Santiago rhesus monkey population. Prior to 1956, monkeys on this island colony did not receive consistent provisions, and were reported to be in poor health (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). A regular provisioning program, instituted in August 1956, resulted in the improved health of individuals and the growth of the population (Rawlins and Kessler [1986] The Cayo Santiago Macaques; Albany: State University of New York Press). LEH, a developmental defect of enamel, is a sensitive indicator of systemic physiological stress (Goodman and Rose [1990] Yrbk. Phys. Anthropol. 33:59-110). It was therefore hypothesized that the prevalence of LEH would be higher in monkeys who were irregularly provisioned than in monkeys who experienced regular provisioning. To test this hypothesis, teeth were examined for LEH in a sample of 181 female rhesus monkeys. The results support the hypothesis: the mean number of defects was statistically significantly higher in the preprovisioned group than it was in the postprovisioned one. When LEH prevalence was assessed using only defects occurring on antimeric pairs, the preprovisioned group again had a higher prevalence than the postprovisioned one, although the difference was not statistically significant, most likely because of the reduced sample size. The results of this study indicate that changes in LEH prevalence, at least in this population of rhesus monkeys, are associated with changes in nutritional status.     

Linear enamel hypoplasias as indicators of systemic physiological stress: evidence from two known age-at-death and sex populations from postmedieval London

Enamel hypoplasias are useful indicators of systemic growth disturbances during childhood, and are routinely used to investigate patterns of morbidity and mortality in past populations. This study examined the pattern of linear enamel hypoplasias in two different burial populations from 18th and 19th Century church crypts in London. Linear enamel hypoplasias on the permanent dentitions of individuals from the crypt of Christ Church, Spitalfields, were compared to enamel defects on the teeth of individuals from St. Bride's. The method used involves the identification of enamel defects at a microscopic level, and systemic perturbations are detected by matching hypoplasias among different tooth classes within each individual. The pattern of linear enamel hypoplasias was contrasted between individuals from the burial sites of Spitalfields and St. Bride's, between males and females, and between those aged less than 20 years of age and those aged over 20 years at death. Six different parameters were examined: frequency of linear enamel hypoplasias, interval between defects, duration of hypoplasias, age at first occurrence of hypoplasia, age at last occurrence of hypoplasia, and the percentage of enamel formation time taken up by growth disturbances. All individuals in the study displayed linear enamel hypoplasias, with up to 33% of total visible enamel formation time affected by growth disruptions. Multiple regression analysis indicated a number of significant differences in the pattern of enamel hypoplasias. Individuals from Spitalfields had shorter intervals between defects and greater percentages of enamel formation time affected by growth disturbances than did individuals from St. Bride's. Females had greater numbers of linear enamel hypoplasias, shorter intervals between defects, and greater percentages of enamel formation time affected by growth disturbances than males. There were also differences in the pattern of enamel hypoplasias and age at death in this study. Individuals who died younger in life had an earlier age at first occurrence of enamel hypoplasia than those who survived to an older age. The pattern of enamel hypoplasias detected in this study was influenced by tooth crown geometry and tooth wear such that most defects were found in the midcrown and cervical regions of the teeth, and greater numbers of defects were identified on the anterior teeth. Differences in sensitivity of the parameters used for the detection of enamel hypoplasias were found in this study. The percentage of visible enamel formation time affected by growth disturbances was the parameter that identified the greatest number of significant differences among the subgroups examined.     

Microstructural defects and enamel hypoplasia in teeth of Toxodon Owen, 1837 from the Pleistocene of Southern Brazil

Enamel hypoplasia is characterized by reduction in the enamel thickness, resulting from a disruption of ameloblast activity due to systemic physiological stress. The euhypsodont teeth of Toxodon, a notoungulate from the Pleistocene of South America, often exhibit signs of enamel hypoplasia, in the form of continuous grooves or a series of pits where the enamel is thinner than in normal areas. These defects alternate with areas of normal enamel, and sometimes more than one form of enamel hypoplasia is present on the same tooth. This study analysed teeth of Toxodon from the Pleistocene Touro Passo Formation and the coastal plain of State of Rio Grande do Sul, Southern Brazil. Six types of enamel hypoplasia were observed. Upper teeth present mainly superficial grooves on the buccal surface, and the defects are less severe than those observed in the lower teeth. In the lower incisors, deep grooves with mesiodistal rows of pits were observed, showing clearly cyclical changes, which to a lesser degree, exist in all teeth. These changes are likely related to the continuous growth of euhypsodont teeth. Seven specimens were analysed under scanning electron microscopy and optical microscopy, which showed the occurrence of microstructural changes associated with the macroscopic enamel defects. Enamel underlying in the vicinity of hypoplastic defects was aprismatic and associated with prominent pathologic striae. These pathological findings might indicate that toxodonts were exposed to some stressing conditions or that their teeth were more easily abraded due to a change in diet items, related to shifting climatic conditions.