Relationship of enamel hypoplasia to the pattern of tooth crown growth: A discussion

The defects of enamel hypoplasia can be related to the layered structure of enamel which represents the sequence of development in tooth crowns. From such studies, it is possible to see that furrow-type enamel defects (the most common form of hypoplasia seen with the naked eye) are just the most prominent expression of a continuum which extends ever smaller, down to a microscopic disturbance to a single layer in the crown formation sequence. Furthermore, the progressive decrease in spacing between development layers which occurs down the crown sides, from occlusal to cervical, affects both the prominence and apparent width of the defects. This makes it difficult to use measurements as a means of estimating the duration of the disturbance causing a particular defect. The difficulty is even greater for the less common pitted or exposed-plane-type defects, for which the apparent width bears very little relationship with the duration of the growth disturbance. The defects of enamel hypoplasia can therefore be understood clearly only when examined under the microscope in relation to the structures which mark the development sequence of the tooth crown. Am J Phys Anthropol 104:89–103, 1997. © 1997 Wiley-Liss, Inc.     

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.     

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 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.     

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.     

Hydranencephaly in two rhesus monkeys (Macaca mulatta)

Spontaneously occurring hydranencephaly was diagnosed at necropsy and confirmed histologically in two stillborn fetuses that were delivered from young female rhesus macaques (Macaca mulatta).     

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.     

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.     

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.     

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.     

Objective measures of health and well-being in laboratory rhesus monkeys (Macaca mulatta)

BACKGROUND: Non-human primates are an invaluable part of biomedical research. Strict regulations insure animals have a maximum likelihood of well-being and optimum health during the course of experimental procedures. Objective assessment of well-being is a critical component of these assurances. METHODS: Here we describe an objective and quantitative system we used to identify two well-being concerns in laboratory rhesus monkeys (Macaca mulatta). We provide a series of indicators for use by laboratory personnel to promote laboratory primate well-being. The indicators measure (1) potentially life threatening clinical concerns, (2) developing clinical issues, (3) atypical behaviors, and (4) laboratory performance. We include specific criteria to facilitate veterinary intervention. RESULTS: The assessment, applied to two case studies reported here, enabled swift veterinary intervention returning the animals to a healthy state. CONCLUSIONS: The measures described here provide a battery of observable and objective measures across multiple dimensions that can further ensure both excellent science and veterinary care.     

Behaviors in rhesus monkeys (Macaca mulatta) associated with activity counts measured by accelerometer

There are large individual differences in the daily pattern and level of physical activity in humans and other species. As it is becoming apparent that activity plays an integral role in a number of physiological processes including arousal, attention, cardiovascular health and body weight regulation, there is an increased interest in quantifying activity. Nonhuman primates are particularly useful experimental models for such studies in that they exhibit a repertoire of activity more similar to humans than the activity of animals such as rodents and domestic animals. Recent studies measuring activity in nonhuman primates have used omnidirectional accelerometers, often worn on collars; however, the exact behaviors and movements detected by monkeys wearing these devices have not yet been characterized. To test the hypothesis that collar-worn accelerometers primarily detect movements that involve movement of the whole body, 16 adult female rhesus monkeys, housed individually in stainless steel cages, wore loose-fitting collars with an attached small metal box housing an activity monitor (Actical omnidirectional accelerometer; MiniMitter Inc., Bend, OR) and behavior was videotaped. Videotaped behaviors were analyzed by frame-by-frame analysis. There was a significant correlation between total (all) movement revealed by videotape analysis and activity counts detected by the accelerometers (r(s)=0.612, P=0.012), primarily reflecting a strong correlation between whole body movement and activity counts (r(s)=0.647, P=0.007). In contrast, arm movement (r(s)=-0.221, P=0.412) and head/neck movement (r(s)=0.193, P=0.474) were not correlated with activity counts. These findings support the hypothesis that activity monitor placement on a collar allows for effective quantification of whole body movement in monkeys, and indicate that behaviors such as chewing and arm movement do not significantly influence activity recorded by collar-mounted accelerometers.     

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.     

Hypothesis for the causes and periodicity of repetitive linear enamel hypoplasia in large, wild African (Pan troglodytes and Gorilla gorilla) and Asian (Pongo pygmaeus) apes

Repetitive linear enamel hypoplasia (rLEH) is often observed in recent large-bodied apes from Africa and Asia as well as Mid- to Late Miocene sites from Spain to China. The ubiquity and periodicity of rLEH are not understood. Its potential as an ontogenetic marker of developmental stress in threatened species (as well as their ancient relatives) makes rLEH an important if enigmatic problem. We report research designed to show the periodicity of rLEH among West African Pan troglodytes (12 male, 32 female), Gorilla gorilla (10 male, 10 female), and Bornean and Sumatran Pongo pygmaeus (11 male, 9 female, 9 unknown) from collections in Europe. Two methods were employed. In the common chimpanzees and gorillas, the space between adjacent, macroscopically visible LEH grooves on teeth with two or more episodes was expressed as an absolute measure and as a ratio of complete unworn crown height. In the orangutans, the number of perikymata between episode onsets, as well as duration of rLEH, was determined from scanning electron micrographs of casts of incisors and canines. We conclude that stress in the form of LEH commences as early as 2.5 years of age in all taxa and lasts for several years, and even longer in orangutans; the stress is not chronic but episodic; the stressor has a strong tendency to occur in pulses of two occurrences each; and large apes from both land masses exhibit rLEH with an average periodicity of 6 months (or multiples thereof; Sumatran orangutans seem to show only annual stress), but this needs further research. This is supported by evidence of spacing between rLEH as well as perikymata counts. Duration of stress in orangutans averages about 6 weeks. Finally, the semiannual stressor transcends geographic and temporal boundaries, and is attributed to regular moisture cycles associated with the intertropical convergence zone modified by the monsoon. While seasonal cycles can influence both disease and nutritional stress, it is likely the combination of seasonal variation in fruiting cycles with specific stressors (malaria and/or intestinal parasites, especially hookworm) that results in this widespread phenomenon. This seasonal stress is sufficiently common and of long duration (6 weeks on average in orangutans) that we think rLEH may reflect significant stress in recent and, inferentially, fossil apes. Increasing seasonality may have impinged negatively on later Miocene apes, especially if they lacked a clear birth peak or seasonality in their reproductive cycles.