PALEOEPIDEMIOLOGY OF DIPHYLLOBOTHRIOSIS: CULTURAL AND ENVIRONMENTAL FACTORS AFFECTING ADENOCEPHALUS INTENSITY AND PREVALENCE.

Peruvian and Chilean mummies and coprolites provide a source of population-based parasitological information. This is especially true of the fish tapeworm, Adenocephalus pacificus. Our analysis of Chinchorro and Chiribaya mummies and diversified coprolite samples from Chile and Peru show variation in infection. There is a statistically significant difference in prevalence between Chinchorro hunter-gatherer and Chiribaya mixed-subsistence contexts. Furthermore, the most pronounced differences occur between populations within these groups. Chinchorro differences in cemeteries at the same location can be related to El Niño-Southern Oscillation variations. Pronounced prevalence variations between 3 Chiribaya villages within 7 km of each other relate to fish distribution and preparation variation. As with other recent archaeoparasitology studies, eggs-per-gram data exhibit overdispersion.

HEAD LOUSE PALEOEPIDEMIOLOGY IN THE OSMORE RIVER VALLEY, SOUTHERN PERU.

Recent studies of louse ectoparasites from mummies have developed robust data sets that allow a true epidemiological approach to the prehistory of louse parasitism. One epidemiological principle is that the binomial of overdispersion is normally negative, meaning that in a host population, parasites are aggregated in a few individuals. We demonstrate the overdispersion of lice in 3 different prehistoric communities that differ along 3 axes or variables: environmental setting, socioeconomic status, and cultural affiliation. Distinct cultural practices could have been involved in different patterns of louse infestation. Prevalence, intensity, and abundance of infestations exhibit statistically significant differences between the communities. We also find differences in prevalence between subadults and adults that contrasted by cultural affiliation and suggest conditions different from those seen today. We show that overall prevalence was affected primarily by ecological setting, not socioeconomic status nor cultural affiliation. These findings demonstrate that statistical analysis of archaeological data can reveal the states of infestation in past populations with lifestyles not seen in modern people. Our approach paves the way for future comparisons of subpopulations within archaeological communities.

Geographically dispersed zoonotic tuberculosis in pre-contact South American human populations.

Previous ancient DNA research has shown that Mycobacterium pinnipedii, which today causes tuberculosis (TB) primarily in pinnipeds, infected human populations living in the coastal areas of Peru prior to European colonization. Skeletal evidence indicates the presence of TB in several pre-colonial South and North American populations with minimal access to marine resources- a scenario incompatible with TB transmission directly from infected pinnipeds or their tissues. In this study, we investigate the causative agent of TB in ten pre-colonial, non-coastal individuals from South America. We reconstruct M. pinnipedii genomes (10- to 15-fold mean coverage) from three contemporaneous individuals from inland Peru and Colombia, demonstrating the widespread dissemination of M. pinnipedii beyond the coast, either through human-to-human and/or animal-mediated routes. Overall, our study suggests that TB transmission in the pre-colonial era Americas involved a more complex transmission pathway than simple pinniped-to-human transfer.

Examining variation in skeletal tuberculosis in a late pre-contact population from the eastern mountains of Peru.

OBJECTIVE AND MATERIALS: This research evaluates the presence and chronology of tuberculosis (TB) in the northeastern highlands of Peru (CE 800-1535) through the analysis of osseous lesions from Pre-Contact Kuelap, Chachapoyas. METHODS: We examined macroscopic lesion morphology and distribution from the skeletal series (MNI = 207). RESULTS: We determined that skeletal evidence was highly consistent with advanced multifocal and spinal tuberculosis in 13 individuals. Destructive lesions of the lower thoracic and/or lumbar vertebra bodies and sacroiliac joints are evident in most cases, but we also observed lesions within the manubriosternal, hip, and knee joints. Both adult males (n = 7) and females (n = 6) present skeletal lesions from young adult to older adults, but there is only one late adolescent. Only three individuals demonstrate similar lesion distributions. CONCLUSIONS: Variation in lesion distribution in this population-based study shows the importance of identifying extra-vertebral tuberculosis and suggests that the disease may have manifested differently than at other coastal sites. These cases confirm the presence of tuberculosis both before and after Inca occupation across this central Andean highlands region. SIGNIFICANCE: This evidence for the likely endemic presence of TB in the New World prior to European Contact furthers our understanding of the distribution of this infectious disease across the region as well as elucidating lesion distribution. LIMITATIONS: The diagnosis of tuberculosis is based on skeletal lesions and it should be confirmed by molecular analysis. FUTURE RESEARCH: Additional examination of vertebral bodies (including juvenile remains) for evidence of earlier manifestations of infection.

Advances in the molecular detection of tuberculosis in pre-contact Andean South America.

Andean paleopathological research has significantly enhanced knowledge about the geographical distribution and evolution of tuberculosis (TB) in pre-Columbian South America. In this paper, we review the history and progress of research on ancient tuberculosis (TB) in the Andean region, focusing on the strengths and limitations of current approaches for the molecular detection of ancient pathogens, with special attention to TB. As a case study, we describe a molecular screening approach for the detection of ancient Mycobacterium tuberculosis in individuals from Late Intermediate Period (1000-1400 CE) contexts at the site of Huari, Peru. We evaluate 34 commingled human vertebrae and combine morphological assessments of pathology with high throughput sequencing and a non-selective approach to ancient pathogen DNA screening. Our method enabled the simultaneous detection of ancient M. tuberculosis DNA and an evaluation of the environmental microbial composition of each sample. Our results show that despite the dominance of environmental DNA, molecular signatures of M. tuberculosis were identified in eight vertebrae, six of which had no observable skeletal pathology classically associated tuberculosis infection. This screening approach will assist in the identification of candidate samples for downstream genomic analyses. The method permits higher resolution disease identification in cases where pathology may be absent, or where the archaeological context may necessitate a broad differential diagnosis based on morphology alone.

New world origin of canine distemper: Interdisciplinary insights.

OBJECTIVE: Canine distemper virus (CDV), human measles virus (HMV), and rinderpest virus (RPV) of cattle are morbilliviruses that have caused devastating outbreaks for centuries. This paper seeks to reconstruct the evolutionary history of CDV. MATERIALS AND METHODS: An interdisciplinary approach is adopted, synthesizing paleopathological analysis of 96 Pre-Columbian dogs (750-1470 CE) from the Weyanoke Old Town, Virginia site, with historical reports, molecular analysis and morbilliviral epidemiology. RESULTS: Both measles (c.900CE) and rinderpest (c. 376 BCE) were first reported in Eurasia, while canine distemper was initially described in South America much later (1735 CE); there are no paleopathological indications of CDV in Weyanoke Old Town dogs. Molecularly, CDV is closely related to HMV, while viral codon usage indicates CDV may have previously infected humans; South American measles epidemics occurred prior to the emergence of canine distemper and would have facilitated HMV transmission and adaptation to dogs. CONCLUSIONS: The measles epidemics that decimated indigenous South American populations in the 1500-1700 s likely facilitated the establishment of CDV as a canine pathogen, which eventually spread to Europe and beyond. SIGNIFICANCE: Understanding the historical and environmental conditions that have driven morbilliviral evolution provides important insights into potential future threats of animal/human cross-species infections. LIMITATIONS: Interpreting historical disease descriptions is difficult and the archaeological specimens are limited. Molecular sequence data and codon usage analyses rely on modern viruses. SUGGESTIONS FOR FURTHER RESEARCH: Interdisciplinary approaches are increasingly needed to understand diseases of the past and present, as critical information and knowledge is scattered in different disciplines.

Recovering parasites from mummies and coprolites: an epidemiological approach.

In the field of archaeological parasitology, researchers have long documented the distribution of parasites in archaeological time and space through the analysis of coprolites and human remains. This area of research defined the origin and migration of parasites through presence/absence studies. By the end of the 20th century, the field of pathoecology had emerged as researchers developed an interest in the ancient ecology of parasite transmission. Supporting studies were conducted to establish the relationships between parasites and humans, including cultural, subsistence, and ecological reconstructions. Parasite prevalence data were collected to infer the impact of parasitism on human health. In the last few decades, a paleoepidemiological approach has emerged with a focus on applying statistical techniques for quantification. The application of egg per gram (EPG) quantification methods provide data about parasites' prevalence in ancient populations and also identify the pathological potential that parasitism presented in different time periods and geographic places. Herein, we compare the methods used in several laboratories for reporting parasite prevalence and EPG quantification. We present newer quantification methods to explore patterns of parasite overdispersion among ancient people. These new methods will be able to produce more realistic measures of parasite infections among people of the past. These measures allow researchers to compare epidemiological patterns in both ancient and modern populations.

Pre-Columbian mycobacterial genomes reveal seals as a source of New World human tuberculosis.

Modern strains of Mycobacterium tuberculosis from the Americas are closely related to those from Europe, supporting the assumption that human tuberculosis was introduced post-contact. This notion, however, is incompatible with archaeological evidence of pre-contact tuberculosis in the New World. Comparative genomics of modern isolates suggests that M. tuberculosis attained its worldwide distribution following human dispersals out of Africa during the Pleistocene epoch, although this has yet to be confirmed with ancient calibration points. Here we present three 1,000-year-old mycobacterial genomes from Peruvian human skeletons, revealing that a member of the M. tuberculosis complex caused human disease before contact. The ancient strains are distinct from known human-adapted forms and are most closely related to those adapted to seals and sea lions. Two independent dating approaches suggest a most recent common ancestor for the M. tuberculosis complex less than 6,000 years ago, which supports a Holocene dispersal of the disease. Our results implicate sea mammals as having played a role in transmitting the disease to humans across the ocean.

Tuberculosis and leprosy in perspective

Two of humankind's most socially and psychologically devastating diseases, tuberculosis and leprosy, have been the subject of intensive paleopathological research due to their antiquity, a presumed association with human settlement and subsistence patterns, and their propensity to leave characteristic lesions on skeletal and mummified remains. Despite a long history of medical research and the development of effective chemotherapy, these diseases remain global health threats even in the 21st century, and as such, their causative agents Mycobacterium tuberculosis and M. leprae, respectively, have recently been the subject of molecular genetics research. The new genome-level data for several mycobacterial species have informed extensive phylogenetic analyses that call into question previously accepted theories concerning the origins and antiquity of these diseases. Of special note is the fact that all new models are in broad agreement that human TB predated that in other animals, including cattle and other domesticates, and that this disease originated at least 35,000 years ago and probably closer to 2.6 million years ago. In this work, we review current phylogenetic and biogeographic models derived from molecular biology and explore their implications for the global development of TB and leprosy, past and present. In so doing, we also briefly review the skeletal evidence for TB and leprosy, explore the current status of these pathogens, critically consider current methods for identifying ancient mycobacterial DNA, and evaluate coevolutionary models.

Patterns of tuberculosis in the Americas: how can modern biomedicine inform the ancient past?

Tuberculosis (TB) is an infectious disease that continues to take its toll on human lives. Paleopathological research indicates that it has been a significant cause of death among humans for at least five thousand years. Because of the devastating consequences to human health, social systems, and endangered primate species, TB has been the subject of many and varied research efforts throughout the world, efforts that are amassing an enormous amount of data concerning the causative agent Mycobacterium tuberculosis. Despite sequencing of the M. tuberculosis genome and numerous molecular epidemiological studies, many questions remain regarding the origin, evolution, and future co-evolutionary trajectory of M. tuberculosis and humans. Indeed, the origin of pre-Columbian New World TB has been and remains hotly debated, and resolution of this controversy will likely only come with integration of data and theory from multiple disciplines. In this paper, we discuss the pre-Columbian TB controversy, and then use research from biological and biomedical sciences to help inform paleopathological and archaeological studies of this ubiquitous disease that plagued our ancient forbears.

Patterns of tuberculosis in the Americas: how can modern biomedicine inform the ancient past?

Tuberculosis (TB) is an infectious disease that continues to take its toll on human lives. Paleopathological research indicates that it has been a significant cause of death among humans for at least five thousand years. Because of the devastating consequences to human health, social systems, and endangered primate species, TB has been the subject of many and varied research efforts throughout the world, efforts that are amassing an enormous amount of data concerning the causative agent Mycobacterium tuberculosis. Despite sequencing of the M. tuberculosis genome and numerous molecular epidemiological studies, many questions remain regarding the origin, evolution, and future co-evolutionary trajectory of M. tuberculosis and humans. Indeed, the origin of pre-Columbian New World TB has been and remains hotly debated, and resolution of this controversy will likely only come with integration of data and theory from multiple disciplines. In this paper, we discuss the pre-Columbian TB controversy, and then use research from biological and biomedical sciences to help inform paleopathological and archaeological studies of this ubiquitous disease that plagued our ancient forbears.

Trauma-induced changes in diaphyseal cross-sectional geometry in two elites from Copan, Honduras.

This research utilized biplanar radiographs to estimate cross-sectional biomechanical properties for the skeletal remains of two elite individuals from the Early Classic period (ca. AD 400-600) of Copan, Honduras: K'inich Yax K'uk' Mo' (Hunal Burial 95-2), founder of the Early Classic Dynasty at Copan, and the primary female interment (Burial 37-8) from the Motmot tomb. Both individuals survived severe blunt-force insults to the right forearm. Gross skeletal examination and evaluation of the radiographs for K'inich Yax K'uk' Mo' suggest that these traumas resulted from, at least in part, disuse atrophy of the affected forearm skeletal elements. Gross and radiologic evaluation of the Motmot remains countered the possibility that she suffered from a metabolic bone disease, and confirmed the presence of a well-healed parry fracture of the right ulna. The degree of asymmetry in cross-sectional biomechanical properties reported here for K'inich Yax K'uk' Mo' is likely the secondary result of the described blunt-force trauma. The results obtained for the principal Motmot interment are not as dramatic, but suggest subtle changes to humeral cross-sectional geometry subsequent to trauma.

Anemia and childhood mortality: latitudinal patterning along the coast of pre-Columbian Peru.

Hrdlicka ([1914] Smithson. Inst. Misc. Collect. 61:1-69) reported that pre-Columbian skeletal material from the coastal lowland Andean region exhibited a high frequency of porotic hyperostosis, a pathological condition of bone that generally is thought to indicate childhood anemia. While subsequent studies tended to reinforce this conclusion, factors implicated in the condition have yet to be fully explored in the region as a whole. This study explores regional and intravalley variation as one step in establishing biocultural variables that increase the apparent risk of childhood anemia. The study sample includes 1,465 individuals: 512 from Peruvian collections housed at the Field Museum of Natural History, and 953 from systematically excavated contexts from Moquegua, Peru. Environmental stressors, such as parasites and disease, rather than specific dietary practices were found to be more likely associated with childhood anemia in these coastal Andean samples. The study supports cribra orbitalia as an earlier expression of porotic hyperostosis and suggests that porotic hyperostosis, as recorded here, cannot be easily dismissed as a result of cranial shape modification. No clear temporal patterns were observed. Finally, the study establishes that comparing data for children and adults can reveal the relative association between childhood anemia and mortality. Childhood mortality associated with anemia was elevated where the presence of tuberculosis or tuberculosis-like conditions was more common and the presence of water-borne pathogens was negligible. In contrast, those buried at lower altitudes, closer to the coast, and consuming mainly marine resources were less likely to die in childhood with anemia than in the other contexts studied.

Field paleoradiography of skeletal material from the early classic period of Copan, Honduras.

OBJECTIVE: To perform a radiographic evaluation of the skeletal remains of 2 elite individuals from the Early Classic Period of Copan, namely, K'inich Yax K'uk' Mo' (Hunal Burial 95-2), founder of the Early Classic Dynasty, and the primary female interment from the Motmot tomb (Burial 37-8). Our aims were to document pathologies and subsequent changes in long-bone density resulting from physiologic or functional adaptations, such as disuse atrophy. METHODS: Standardized anteroposterior and mediolateral radiographs were obtained using a portable veterinary x-ray unit and Polaroid film. Orthogonal radiographs were used to estimate the cross-sectional biomechanical properties of the long bones. RESULTS: In the case of Yax K'uk' Mo', it appears that there was trauma-induced disuse atrophy of the right forearm resulting in an accelerated loss of cortical bone in the right humerus relative to the left humerus. The restructuring of this individual's left shoulder girdle probably resulted in radical structural and functional changes. Although this fracture could have contributed to degenerative changes and paralysis, there was no evidence of disuse atrophy in the left upper limb. The gracile Motmot skeleton showed no signs of osteoporosis, osteopenia or disuse atrophy. CONCLUSIONS: The use of radiography in the assessment of the skeletal material described here vastly increased our ability to document the pathologic processes that affected these centuries-old individuals during their lifetimes. In addition, the use of radiographs allowed us to expand our understanding of how these processes may have affected biomechanics and, subsequently, long-bone geometric properties.

A 9,000-year record of Chagas' disease.

Tissue specimens from 283 principally spontaneously (naturally) desiccated human mummies from coastal and low valley sites in northern Chile and southern Peru were tested with a DNA probe directed at a kinetoplast DNA segment of Trypanosoma cruzi. The time interval spanned by the eleven major cultural groups represented in the sample ranged from approximately 9,000 years B.P. (7050 B.C.) to approximately the time of the Spanish conquest, approximately 450 B.P. ( approximately 1500 A.D.). Forty-one percent of the tissue extracts, amplified by the PCR reacted positively (i.e., hybridized) with the probe. Prevalence patterns demonstrated no statistically significant differences among the individual cultural groups, nor among subgroups compared on the basis of age, sex, or weight of specimen tested. These results suggest that the sylvatic (animal-infected) cycle of Chagas' disease was probably well established at the time that the earliest humans (members of the Chinchorro culture) first peopled this segment of the Andean coast and inadvertently joined the many other mammal species acting as hosts for this parasite.

Louse infestation of the Chiribaya culture, southern Peru: variation in prevalence by age and sex.

In order to improve the interpretive potential of archaeoparasitology, it is important to demonstrate that the epidemiology of ancient parasites is comparable to that of modern parasites. Once this is demonstrated, then we can be secure that the evidence of ancient parasitism truly reflects the pathoecology of parasitic disease. Presented here is an analysis of the paleoepidemiology of Pediculus humanus infestation from 146 mummies from the Chiribaya culture 1000-1250 AD of Southern Peru. The study demonstrates the modern parasitological axiom that 10% of the population harbors 70% of the parasites holds true for ancient louse infestation. This is the first demonstration of the paleoepidemiology of prehistoric lice infestation.

Pathoecology of Chiribaya parasitism.

The excavations of Chiribaya culture sites in the Osmore drainage of southern Peru focused on the recovery of information about prehistoric disease, including parasitism. The archaeologists excavated human, dog, guinea pig, and llama mummies. These mummies were analyzed for internal and external parasites. The results of the analysis and reconstruction of prehistoric life from the excavations allows us to interpret the pathoecology of the Chiribaya culture.

Louse infestation of the Chiribaya Culture, Southern Peru: variation in prevalence by age and sex

In order to improve the interpretive potential of archaeoparasitology, it is important to demonstrate that the epidemiology of ancient parasites is comparable to that of modern parasites. Once this is demonstrated, then we can be secure that the evidence of ancient parasitism truly reflects the pathoecology of parasitic disease. Presented here is an analysis of the paleoepidemiology of Pediculus humanus infestation from 146 mummies from the Chiribaya culture 1000-1250 AD of Southern Peru. The study demonstrates the modern parasitological axiom that 10 percent of the population harbors 70 percent of the parasites holds true for ancient louse infestation. This is the first demonstration of the paleoepidemiology of prehistoric lice infestation

Pathoecology of Chiribaya parasitism

The excavations of Chiribaya culture sites in the Osmore drainage of southern Peru focused on the recovery of information about prehistoric disease, including parasitism. The archaeologists excavated human, dog, guinea pig, and llama mummies. These mummies were analyzed for internal and external parasites. The results of the analysis and reconstruction of prehistoric life from the excavations allows us to interpret the pathoecology of the Chiribaya culture