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.     

Experimental assessment of nutrition and bone growth's velocity effects on Harris lines formation

Harris lines (HL) are radio-opaque transverse lines traditionally associated with stressors that halt or decelerate growth in humans. Harris lines' status as a stress marker is, however, questionable because their association to illness and deficient growth is low and they commonly form in the absence of stress during periods of accelerated growth. To assess Harris line's reliability as a stress marker, this study examined their association with nutritional status and bone growth velocity through an experimental study in rabbits. Forty-five New Zealand White rabbits were divided into: Control (normal laboratory conditions), Experimental-1 (moderately undernourished), and Experimental-2 (periodically fasted) groups during their growth. Variables analyzed included weight, forelimb length, humeral diaphyseal length, diaphyseal growth velocity, and number of Harris lines. Fewer lines were observed by the end of the study among Experimental-1 animals. More Harris lines formed during periods of rapid growth in the absence of nutritional stress. Accordingly, Harris lines are a poor marker of stress. Intrinsic limitations to paleopathological studies can be overcome, but even the most careful attentiveness to multiple stress markers and cultural context will go amiss if the markers used are unreliable.     

Skeletal manifestations of stress in child victims of the Great Irish Famine (1845–1852): Prevalence of enamel hypoplasia,Harris lines,and growth retardation

The Great Irish Famine of 1845–1852 is among the worst food crises in human history. While numerous aspects of this period have been studied by generations of scholars, relatively little attention has so far been given to the physiological impact it is likely to have had on the people who suffered and succumbed to it. This study examines the prevalence of enamel hypoplasia, Harris lines, and growth retardation in the nonadult proportion of a skeletal population comprising victims of the Famine who died in the workhouse in the city of Kilkenny between 1847 and 1851. The frequency of enamel hypoplasia in these children does not appear to have increased as a consequence of famine, although this fact is likely to be a reflection of the osteological paradox. Harris lines and growth retardation; however, were very prevalent, and the manifestation and age‐specific distribution of these may be indicators of the Famine experience. While there was no clear correlation in the occurrence of the assessed markers, the presence of cribra orbitalia displayed a significant relationship to enamel hypoplasia in 1‐ to 5‐year‐old children. While starvation, metabolic disorders and infectious diseases are likely to have greatly contributed to the manifestation of the markers, the psychosocial stress relating to institutionalization in the workhouse should not be underestimated as a substantial causative factor for skeletal stress in this population. Am J Phys Anthropol 155:149–161, 2014. © 2014 Wiley Periodicals, Inc.     

Harris lines and ethanol consumption during growth period

Harris lines represent episodes of growth arrest followed by recovery, thus reflecting episodes of mismatched imbalance between energy intake and energy expenditure. Consumption of ethanol during the growth period — formerly extended in our wine-producing rural areas- may lead to such a situation, due at least in part to the energy-wasteful MEOS-linked ethanol metabolism. Based on these facts, in the present study we have analysed the relationship between ethanol intake during growth period and the presence of Harris lines in the right tibia in 100 consecutive adult patients admitted to our hospitalization unit. Early ethanol consumption was strongly related with the presence of two or more, and three or more Harris lines, so that ethanol consumption should be considered in the differential diagnosis of Harris lines, and conversely, the presence of Harris lines point to ethanol consumption during growth period. This association was independent from coexisting starvation and/or illness.     

Environmental stress in the Early Mediaeval Slavic population at Borovce (Slovakia)

Several palaeopathological indicators examined in skeletal samples are caused by stress during childhood and remain visible in adults. In this study, dental enamel hypoplasia was observed in 451 individuals from the Early Mediaeval (8th to beginning of 12th c. AD) Slavic skeletal series at Borovce (Slovakia). The presence of enamel hypoplasia was scored in all types of deciduous and permanent teeth. More than one-fourth (27.2%) of the individuals with preserved permanent teeth showed enamel hypoplasia. No significant differences in the occurrence of the enamel lesions were found between males and females. The age at development of hypoplasias was estimated for 74 individuals by measuring the distance of the defect from the cemento-enamel junction. The hypoplastic defects appeared most frequently between 2.5 and 3.0 years. Following the trends observed in the distribution of age at development of the enamel lesions between subadults and adults, individuals stressed earlier in life had a reduced ability to cope with later insults. High prevalence of enamel hypoplasia, especially among 10–14-year-old growing juveniles, has led to the assumption that the Borovce population lived a considerably long period under conditions of high environmental pathogen load, and probably also suffered from some nutritional deficiencies.     

Accessing Developmental Information of Fossil Hominin Teeth Using New Synchrotron Microtomography-Based Visualization Techniques of Dental Surfaces and Interfaces

Quantification of dental long-period growth lines (Retzius lines in enamel and Andresen lines in dentine) and matching of stress patterns (internal accentuated lines and hypoplasias) are used in determining crown formation time and age at death in juvenile fossil hominins. They yield the chronology employed for inferences of life history. Synchrotron virtual histology has been demonstrated as a non-destructive alternative to conventional invasive approaches. Nevertheless, fossil teeth are sometimes poorly preserved or physically inaccessible, preventing observation of the external expression of incremental lines (perikymata and periradicular bands). Here we present a new approach combining synchrotron virtual histology and high quality three-dimensional rendering of dental surfaces and internal interfaces. We illustrate this approach with seventeen permanent fossil hominin teeth. The outer enamel surface and enamel-dentine junction (EDJ) were segmented by capturing the phase contrast fringes at the structural interfaces. Three-dimensional models were rendered with Phong’s algorithm, and a combination of directional colored lights to enhance surface topography and the pattern of subtle variations in tissue density. The process reveals perikymata and linear enamel hypoplasias on the entire crown surface, including unerupted teeth. Using this method, highly detailed stress patterns at the EDJ allow precise matching of teeth within an individual’s dentition when virtual histology is not sufficient. We highlight that taphonomical altered enamel can in particular cases yield artificial subdivisions of perikymata when imaged using X-ray microtomography with insufficient resolution. This may complicate assessments of developmental time, although this can be circumvented by a careful analysis of external and internal structures in parallel. We further present new crown formation times for two unerupted canines from South African Australopiths, which were found to form over a rather surprisingly long time (> 4.5 years). This approach provides tools for maximizing the recovery of developmental information in teeth, especially in the most difficult cases.     

Hardships of contact: Enamel hypoplasias in Tupí-Mondé Amerindians from the Brazilian Amazonia

This paper presents an assessment of enamel defects (hypoplasias) in the permanent anterior teeth of three Tupí-Mondé-speaking groups from the Brazilian Amazonia: the Gavião, Suruí, and Zoró. These are native societies that experienced the onset of permanent contact with Brazilian national society in different periods of the 20th century. Tupí-Mondé dentition is highly hypoplastic, which is possibly related to exposure to adverse health and nutritional conditions. Data for the Gavião, Suruí, and Zoró are in agreement with results from other populations that show that certain teeth, the maxillary central incisors and the mandibular canines in particular, tend to be more hypoplastic. Although all types of teeth show hypoplasia concentrations at some enamel zones, there is substantial intertooth variation in the age at which peaks occur. It is argued that hypoplasia concentrations at certain ages are unlikely to be related to postweaning stresses for the Tupí-Mondé. Statistically significant associations between presence of enamel defects and deficits in physical growth (height-for-age) were detected in children 7–11 years of age. Diachronic assessment of enamel defects, which rested upon the potential of enamel as “memory” of past periods of systemic physiological perturbation, allowed us to unravel aspects related to the dynamics of Tupí-Mondé life during the 20th century. Frequencies of enamel zones with defects peaked during the contact years of each of the Tupí-Mondé groups, attesting to the extreme social and biological hardships that characterized the contact experiences of these native societies with Brazilian national society. Am J Phys Anthropol 109:111–127, 1999. © 1999 Wiley-Liss, Inc.     

The association between Harris lines and enamel hypoplasia in prehistoric California Indians

Hypoplastic defects of tooth enamel and Harris lines in the long bones have been heralded as potentially useful indicators of health conditions in prehistoric populations. Both result from temporary cessation of growth processes due to similar types of disease, malnutrition, or other metabolic insult. An association test for the first six years of life was conducted on a large series of prehistoric California Indians, using femora and canines from young adults. No significant association was found. This is ascribable to differences in etiology and stability.     

The chronological distribution of enamel hypoplasias from prehistoric Dickson Mounds populations

The chronological distributions of enamel hypoplasias (indicators of nonspecific stress) are assessed for 111 individuals from two prehistoric populations from Dickson Mounds, Lewiston, Illinois. The earlier population (circa A.D. 950-1150) involves a transition from an indigenous gathering-hunting tradition to increasing adoption of Mississippian lifeways. The later population (circa A.D. 1150-1300) is fully Mississippian (MM). Based on the occurrence of hypoplasias on all permanent teeth except third molars, 14 half-year periods from birth to 7.0 years are graded for evidence of hypoplasia-stress. Both populations have a low frequency of hypoplasia which occur before 2 years of age and after 4 years of age. A common peak frequency of hypoplasias between 2.0 and 4.0 years is suggestive of an elevated degree of stress at weaning. The peak frequency of hypoplasias is earlier in the MM (2.5-3.0 years versus 3.0-3.5 years in the pre-Mississippian population). In addition, the rise to and decline from peak frequency occurs approximately 0.5 years earlier in the MM. The earlier and sharper rise to peak frequency suggests earlier and more severe weanling-related stress. Hypoplasias chronologies are undoubtedly influenced by age-related host resistance factors (Sarnat and Schour, 1941). Nevertheless, these data demonstrate that populations may vary in their chronological distribution of hypoplasias and that these variations may provide useful information on age-related patterns of exposure to environmental stressors.     

The Occurrence and Age Distribution of Harris Lines in Turkey

Harris lines are widely accepted as indicators of physiological stress and provide valuable data for determining the extent and nature of the physiological stress factors acting on a human community. Traditionally, Harris lines are studied in skeletal populations. In the study reported here, data were collected on living children to eventually clarify if stress is basically chronic or acute in nature, if it has a greater impact on children or adults, and if it is correlated with increased rates of mortality. The existence of Harris lines was determined in a sample of 400 children, 210 males and 190 females, randomly selected from those under examination in the radiology services of hospitals. Radiological analysis was used to analyze Harris lines. The age of Harris line formation and variations in the number of lines with age were established to determine at which age the densest line population was present. For this sample, the formation of Harris lines is around 2–3 years of age, in agreement with published literature. It should be taken into consideration that Harris lines are the end result of multiple factors, rather than a single stress factor, and are influenced by an individual’s immune system and resistance to stress.     

Insights from stable light isotopes on enamel defects and weaning in Pliocene herbivores

A high prevalence of enamel hypoplasia in several herbivores from the early Pliocene Langebaanweg locality, South Africa, indicates general systemic stress during the growing years of life. The presence of several linear enamel hypoplasias per tooth crown in many teeth further suggest that these stress events may be episodic. The δ¹⁸O values along tooth crowns of mandibular second molars ofSivatherium hendeyi (Artiodactyla, Giraffidae) were used to investigate the cause of the stress events in this tooth type. Results show that weaning in this fossil giraffid occurred at a similar ontogenetic age to that in extant giraffes, and that the observed enamel hypoplasia towards the base of this tooth type manifested post-weaning. Further, high-resolution oxygen isotope analyses acrossS. hendeyi third molars suggest that the entire development of defective tooth crowns occurred under conditions of increased aridity in which the cool, rainy part of the seasonal cycle was missing. The high prevalence of this defect in many herbivores suggests that climatic conditions were not favourable. This study reiterates the value of stable isotope analyses in determining both the behaviour of fossil animals and the environmental conditions that prevailed during tooth development.     

Congenital syphilis in the past: slaves at Newton Plantation, Barbados, West Indies.

Hutchinson's incisors and Moon's molars are specific lesions of congenital syphilis. The extensive but fragmentary clinical literature on these conditions describes reduced dimensions and thin enamel in the permanent incisors and first molars, crowding and infolding of the first molar cusps, notching of the upper incisors, and apical hypoplasias of the permanent canines. A Barbados slave cemetery (ca. 1660-1820 AD) includes three individuals with these features, suggesting a frequency at birth of congenital syphilis in the population approaching 10%. These three cases show triple the frequency of all hypoplasias and more than seven times the frequency of pitting hypoplasia present in the remainder of the series. The recognizable congenital syphilis cases account for much of the remarkably high frequency of hypoplasias in the series as a whole. We infer that syphilis contributed substantially to morbidity, infant mortality, and infertility in this population. Presence or absence of congenital syphilis may account for much of the variability in health and mortality seen among nineteenth century African-American populations.     

Enamel hypoplasia in ancestral Puebloan populations from southwestern Colorado: I. Permanent dentition

Dental enamel hypoplasias are used to examine metabolic disruption experienced during early childhood by ancestral Puebloan (Anasazi) inhabitants of southwestern Colorado. The hypoplasia sample consists of the permanent anterior dentition from 147 individuals from Montezuma County and Mesa Verde National Park. Using the individual as the basis of analysis, the study compares different time periods of occupation of the region with respect to prevalence and timing of hypoplasia occurrence. The frequency of enamel hypoplasia in the combined regional sample is high, affecting 90% of the individuals and 66% of the anterior teeth. The earliest onset of hypoplasia in individuals occurs most commonly at 2.5–3.0 years, and the peak age for enamel disruption is 3.0–3.5 years. There are no significant differences in hypoplasia frequency or timing between males and females or between adults and subadults. The level of childhood stress appears to have increased significantly with time from the Basketmaker III to the Pueblo I and Pueblo II periods, then decreased slightly during the Pueblo III. The differences between the Pueblo I, II, and III periods are not significant. The Pueblo II sample from Yellow Jacket Canyon sites 5MT1 and 5MT3 and the Dolores Pueblo I sample show the highest levels of childhood stress in comparison to other Puebloan populations inhabiting this region prior to A.D. 1300. Am. J. Phy. Anthropol. 102:351–367, 1997. © 1997 Wiley-Liss, Inc.     

Intra- and interobserver concordance in scoring Harris lines: A test on bone sections and radiographs

Little attention has been devoted to assessing the reproducibility of (paleo)pathological observations. Harris lines (HL) are among the markers most used to determine chronology of stresses suffered during growth. Nevertheless, their scoring entails remarkable methodological difficulty. Bone sections (S) and radiographs (R) of 29 adult tibiae of archeological provenance (medieval) were scored for HL by five observers. At regular intervals of time, each observer gave two independent counts on both series. Results show a) a substantial interobserver disagreement of HL estimates for both sectional and radiographic records, and b) a high level of intraobserver error. © 1994 Wiley-Liss, Inc.     

Study of Harris lines at the Prat de la Riba necropolis--third to fifth century AD

Harris lines (HL) are considered a nutritional or pathological stress factor in the study of past populations. This study attempts to contribute to the knowledge of the causal agents for HL in terms of assessing the health state of the population of Tarragona in the Roman period. The presence of HL has been analyzed in 614 long bones (214 humeri, 150 femurs and 250 tibias) from 243 skeletons. No HL have been observed in humeri. The frequencies of HL in femurs are higher than 27% and in tibias more than 48%. Although no significant differences in the presence of HL is found among age categories, it seems that the causal agents of these marks acted on individuals from the age of 5, an age from which the long bones of the lower extremities are more prone to producing HL. The hardened living conditions in the Dark Age of the Roman period in Spain between the third to fifth centuries A.D. may be the cause of the high prevalence of HL in this population.     

Factors affecting the distribution of enamel hypoplasias within the human permanent dentition

Frequencies and morphological and chronological distributions of enamel hypoplasias are presented by tooth type (permanent I1 to M2s), based on a sample of 30 prehistoric Amerindians with complete and unworn dentitions. There is nearly a tenfold variation in frequency of defects by tooth, ranging from 0.13 per mandibular second molar to 1.27 per maxillary central incisor. The six anterior teeth average between 0.70 and 1.27 defects/tooth, whereas the eight posterior teeth average between 0.43 and 0.13 defects/tooth. Earlier developing teeth, such as incisors, have earlier peak frequencies of defects (2.0-2.5 years), while later developing teeth, such as second molars, have subsequent peak frequencies (5.0-6.0 years). These variations are relevant when comparing hypoplasia data based on different teeth. Differences in hypoplasia frequencies among teeth are not solely due to variation in time of crown development, as is usually reported. Rather, there is evidence for biological gradients in susceptibility to ameloblastic disruption. Anterior teeth are more hypoplastic than posterior teeth. More developmentally stable "polar" teeth are more hypoplastic than surrounding teeth. Polar teeth may be more susceptible to hypoplasias because their developmental timing is less easily disrupted. In all teeth, hypoplasias are most common in the middle and cervical thirds. Crown development and morphological factors, such as enamel prism length and direction, may influence the development and expression of enamel surface defects.     

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.     

Prevalence and age at development of enamel hypoplasias in Mexican children

Enamel hypoplasias, deficiencies in enamel thickness resulting from disturbances during the secretory phase of enamel development, are generally believed to result from nonspecific metabolic and nutritional disruptions. However, data are scare on the prevalence and chronological distributions. of hypoplasias in populations experiencing mild to moderate malnutrition. The purpose of this article is to present baseline data on the prevalences and chronological distributions of enamel hypoplasias, by sex and for all deciduous and permanent anterior teeth, in 300 5 to 15-year-old rural Mexican children. Identification of hypoplasias was aided by comparison to a published standard (Federation Dentaire Internationale: Int. Dent. J. 32(2):159-167, 1982). The location of defects, by transverse sixths of tooth crowns, was used to construct distributions of defects by age at development. One or more hypoplasias were detected in 46.7% (95% CI = 40.9-52.5%) of children. Among the unworn and completely erupted teeth, the highest prevalence of defects was found on the permanent maxillary central incisors (44.4% with one or more hypoplasias), followed by the permanent maxillary canine (28.0%) and the remaining permanent teeth (26.2 to 22.2%) Only 6.1% of the completely erupted and unworn deciduous teeth were hypoplastic. The prevalence of enamel defects on the permanent teeth was up to tenfold greater than that found in studies of less marginal populations that used the FDI method. The prevalence of defects in transverse zones suggests a peak frequency of hypoplasias during the second and third years for the permanent teeth, corresponding to the age at weaning in this group. In the deciduous teeth, a smaller peak occurs between 30 and 40 weeks post gestation. The frequency of defects after three years of age is slightly higher in females than males, suggesting a sex difference in access to critical resources.     

Dental enamel hypoplasias and health changes in the Middle Bronze Age - Early Iron Age transition at Pella in Jordan.

Dental enamel hypoplasias are increasingly being used in epidemiological studies as indicators of health within both modern and prehistoric populations. This symptom of growth disruption is used here to examine possible changes in health occurring at the transition between the Bronze Age and Iron Age in Jordan, through examination of enamel hypoplasias in skeletal remains from two tombs at the archaeological site of Pella. A small but not statistically significant difference in the prevalence and frequency of hypoplastic defects was found between the two time periods. These results suggest that the political and economic changes occurring at this time were not sufficiently stressful to cause a dramatic deterioration in health at the onset of the Early Iron Age.     

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.