Frontiers in the bioarchaeology of stress and disease: Cross-disciplinary perspectives from pathophysiology,human biology,and epidemiology

Over the last four decades, bioarchaeology has experienced significant technical growth and theoretical maturation. Early 21st century bioarchaeology may also be enhanced from a renewed engagement with the concept of biological stress. New insights on biological stress and disease can be gained from cross-disciplinary perspectives regarding human skeletal variation and disease. First, pathophysiologic and molecular signaling mechanisms can provide more precise understandings regarding formation of pathological phenotypes in bone. Using periosteal new bone formation as an example, various mechanisms and pathways are explored in which new bone can be formed under conditions of biological stress, particularly in bone microenvironments that involve inflammatory changes. Second, insights from human biology are examined regarding some epigenetic factors and disease etiology. While epigenetic effects on stress and disease outcomes appear profoundly influential, they are mostly invisible in skeletal tissue. However, some indirect and downstream effects, such as the developmental origins of adult health outcomes, may be partially observable in bioarchaeological data. Emerging perspectives from the human microbiome are also considered. Microbiomics involves a remarkable potential to understand ancient biology, disease, and stress. Third, tools from epidemiology are examined that may aid bioarchaeologists to better cope with some of the inherent limitations of skeletal samples to better measure and quantify the expressions of skeletal stress markers. Such cross-disciplinary synergisms hopefully will promote more complete understandings of health and stress in bioarchaeological science. Am J Phys Anthropol 155:294–308, 2014. © 2014 Wiley Periodicals, Inc.     

Microbial programming of health and disease starts during fetal life

The pioneer microbiota of the neonatal gut are essential for gut maturation, and metabolic and immunologic programming. Recent research has shown that early bacterial colonization may impact the occurrence of disease later in life (microbial programming). Despite early conflicting evidence, it has long been considered that the womb is a sterile environment and human microbial colonization begins at birth. In the last few years, several findings have reiterated the presence of microbes in infant first stool (meconium) and pointed to the existence of in utero microbial colonization of the infant gut. The dominant bacterial taxa detected in meconium specimens belong to the Enterobacteriaceae family (Escherichia genus) and lactic acid bacteria (notably members of the genera Leuconostoc, Enterococcus, and Lactococcus). Maternal atopy promotes dominance of Enterobacteriaceae in newborn meconium, which in turn may lead to respiratory problems in the infant. This microbial interaction with the host immune system may in fact, originate during fetal life. Our review evaluates the evidence for an intrauterine origin of meconium microbiota, their composition and influences, and potential clinical implications on infant health. Birth Defects Research (Part C) 105:265–277, 2015. © 2015 Wiley Periodicals, Inc.     

Modelling the developmental origins of health and disease in the early embryo

The concept that certain adult diseases, such as hypertension, type 2 diabetes and dyslipidaemia can originate from events occurring in utero arose from epidemiological studies in humans but has since been supported by numerous animal-based studies. Referred to as the "developmental origins of health and disease" or "DOHaD" hypothesis, nutritional studies to date have largely focused on two experimental paradigms involving either calorie or protein restriction for varying intervals during pregnancy, where the favoured animal models have been the sheep and rat. In recent times, attention has been directed towards the earliest stages of gestation, where there is emerging evidence to indicate that the pre-implantation embryo may be particularly sensitive to environmentally induced perturbations leading to impaired health in adulthood. In this article, we make the case for hESCs as a model of the human pre-implantation embryo. Working with comparatively large populations of embryonic cells from the species of clinical interest, the scope exists to investigate the effects of specific genetic manipulations or combinations of metabolites against contrasting genetic backgrounds, where the consequences can be evaluated in downstream tissue specific progenitor and/or terminally differentiated cells. In order to fully realize these potentials, however, both derivation and culture conditions need to be harmonized and refined so as to preclude the requirement for feeder cells and serum.     

Comparison of invertebrate herbivores on native and non‐native Senecio species: Implications for the enemy release hypothesis

The enemy release hypothesis posits that non‐native plant species may gain a competitive advantage over their native counterparts because they are liberated from co‐evolved natural enemies from their native area. The phylogenetic relationship between a non‐native plant and the native community may be important for understanding the success of some non‐native plants, because host switching by insect herbivores is more likely to occur between closely related species. We tested the enemy release hypothesis by comparing leaf damage and herbivorous insect assemblages on the invasive species Senecio madagascariensis Poir. to that on nine congeneric species, of which five are native to the study area, and four are non‐native but considered non‐invasive. Non‐native species had less leaf damage than natives overall, but we found no significant differences in the abundance, richness and Shannon diversity of herbivores between native and non‐native Senecio L. species. The herbivore assemblage and percentage abundance of herbivore guilds differed among all Senecio species, but patterns were not related to whether the species was native or not. Species‐level differences indicate that S. madagascariensis may have a greater proportion of generalist insect damage (represented by phytophagous leaf chewers) than the other Senecio species. Within a plant genus, escape from natural enemies may not be a sufficient explanation for why some non‐native species become more invasive than others.     

Brief communication: Twentieth-century replication of an Egyptian mummy: Implications for paleopathology

Replication in a modern human cadaver of ancient Egyptian mummification focused on tools used by ancient Egyptian embalmers, the use of natron (a mixture of sodium carbonate, bicarbonate, and chloride) in the preparation of the mummy, surgical procedures in the removal of the viscera and brain, and histologic examination of the viscera. The first three areas have been reported separately (Brier and Wade [1997] ZAS 124:89–100). In this paper, we demonstrate a degree of histologic preservation comparable to that seen in Egyptian mummies, indicating the effectiveness of ancient mummification and that the histologic appearance of such mummies is little altered by the passage of millennia. Am J Phys Anthropol 107:417–420, 1998. © 1998 Wiley-Liss, Inc.     

Toothcomb origins: Support for the grooming hypothesis

Debate over the original adaptive significance of the lemuriform toothcomb, whether it was principally a grooming organ or a scraper-feeding tool, currently hinges upon the functional morphology of the lower incisors and canines of lemurs and lorises, and the fossil adapids thought to be their ancestors or structural prototypes. We suggest that the morphology of the upper incisors and the oronasal complex of the latter, given the context of a more general theory of incisor evolution within the primates, exhibits preadaptive conditions foreshadowing the emergence of the toothcomb and also evidence of strepsirhine monophyly. We find in all underived lemuriforms and in most fossil adapids where the elements are known, a striking continuity in upper incisor form, including such derived features as an interincisal diastema, strong central incisor prong, low-crowned morphology and reduced premaxillary size. The pattern suggests a basic strepsirhine reduction in the functional significance of the anterior dentition in feeding and harvesting roles. These features may be related to a novel connection of the rhinarium with the vomeronasal organ via a sulcate pair of labial folds, which serves as a component of a specialized behavioral-physiological complex dealing with olfactory communication. Rather than being the anatomical nucleus of this system, the toothcomb may have been added secondarily in the lemuriform descendants of the preadapted adapids, possibly as a device to stimulate glandular secretion of pheromones by direct pressure, and to simultaneously distribute odorants through the fur.     

Relationship between early puberty and the risk of hypertension/overweight at age 50: Evidence for a modified Barker hypothesis among Polish youth

The objective of this paper is to evaluate: (a) the association between BMI in childhood and adolescence and BMI at age 50, and (b) the association between timing of maturation at puberty and BMI at age 50 and the occurrence of high blood pressure. We explore whether differences in somatic and physiological factors observed among children with early or late onset of puberty indicates that this period of life could be critical for appearance of some CVD risk factors later in the life cycle. Our data include 135 males and 148 females, born in 1953, participants in the Wroc?aw Longitudinal Study. Data pertaining to their growth and several indices of sexual and skeletal maturation were collected yearly between age 8 and 18. Subsequently, their anthropometric traits were measured and cardiovascular health status was assessed at age 50. We find that BMI at distinct stages in the life cycle were positively correlated. Also BMI at 50 were positively associated with blood pressure at 50. Moreover, earlier maturation at puberty is associated with higher values of BMI at age 50. We also find that earlier pubertal maturation is an independent factor that influences the appearance of high blood pressure in adulthood.     

An assessment of health and disease in the prehistoric inhabitants of the Mariana Islands

Using a variety of skeletal and dental stress indicators, an assessment of the health and disease of the indigenous inhabitants of the Mariana Islands, the Chamorro, is made. The major hypothesis to be tested is that the Chamorro were relatively healthy and that deviations from the expected, as well as inter-island variation, may reflect environmental, ecological, and cultural differences. The major skeletal series surveyed include sites on Guam (N = 247 individuals), Rota (N = 14), Tinian (N = 20), and Saipan (N = 102). The majority of the specimens are from the transitional pre-Latte (AD 1–1000) and Latte (AD 1000–1521) periods. These data derive primarily from unpublished osteological reports. The indicators of health and disease surveyed include mortality and paleodemographic data, stature, dental paleopathology, cribra orbitalia, limb bone fractures, degenerative osteoarthritis, and infectious disease (including treponemal infection). Where appropriate, tests of significance are calculated to determine the presence of any patterning in the differences observed within and between the skeletal series. Information recorded in prehistoric Hawaiians provides a standard for external comparisons. Several of the larger skeletal series surveyed have paleodemographic features that are consistent with long-term cemetery populations. Females and subadults are typically underrepresented. Most subadult deaths occur in the 2–5 year age interval. Life expectancy at birth ranges from 26.4 to 33.7 years. A healthy fertility rate is indicated for these series. The prehistoric inhabitants of the Mariana Islands were relatively tall, exceeding living Chamorros measured in the early part of the present century. The greater prevalence of developmental defects in the enamel suggests that the Chamorro were exposed to more stress than prehistoric Hawaiians. The low frequency of cribra orbitalia further indicates iron deficiency anemia was not a problem. There are generally low frequencies of dental pathology in the remains from the Mariana Islands. Betel-nut staining is relatively common in all series which may help to explain the relatively low prevalence of dental pathology. Healed limb bone fractures are rare in these skeletal series; the frequency and patterns of fractures suggest accidental injury as the main cause. Greater physical demands involving the lower back region are indicated by a high frequency of spondylolysis, or stress fracture in the lumbar vertebrae in the Chamorro. Likewise, advanced degenerative bone changes, while of low occurrence, are significantly greater in the Chamorro than Hawaiians. The prevalence of skeletal and dental indicators of stress was generally higher in the smaller islands of the Marianas chain (e.g., Rota), islands with fewer resources to buffer environmental catastrophe. Bony changes suggestive of treponemal (probably yaws) disease are common in most of these Marianas Islands skeletal series. Am J Phys Anthropol 104:315–342, 1997. © 1997 Wiley-Liss, Inc.     

Juvenile infection and male display: testing the bright male hypothesis across individual life histories

Current tests of the bright male hypothesis focus on assaysof adult disease resistance and their relation to male traitdevelopment and female choice. We suggest that if parasiteshave significant harmful effects on juvenile stages of a host,then females selecting males that effectively signal juvenileparasite resistance may gain a significant "good genes" benefit.Currently, there is no information on juvenile and adult infectionor resistance in the same male and whether adult male displayssignal juvenile parasite resistance. In the present study, wemeasure infection of the ectoparasitic louse, Myrsidea ptilonorhynchi,in individual male satin bowerbirds (Ptilonorhynchus violaceus)both as juveniles and nine or more years later as adults. Wetest hypotheses that examine the role of juvenile parasite infectionin mediating sexual selection. We found that (1) juvenile infectionis higher than adult infection in the same individuals, (2)adult males able to hold display sites have lower juvenile infection,and (3) juvenile and adult infection in the same individualsare not significantly correlated. In addition, comparisons amonga larger set of individuals from a single year show that bloodand ectoparasite infections are highly correlated, and bothdecrease with male age and are inversely related to male courtshipsuccess. These results, combined with the evidence that femalesmate exclusively with bower-holding males support the hypothesisthat females use adult male display traits to identify maleswith a high level of juvenile disease resistance. We suggestthat effective tests of the bright male hypothesis should include(1) assessment of infection resistance in both subadult andadult life history stages, (2) tests of whether differencesin age-specific resistance are indicated in adult male displays,and (3) tests to determine if females attend to these traitsin mate choice. Although these requirements increase the difficultyof testing the bright male hypothesis, they are necessary fora more accurate assessment of the effects of parasites on maledisplay and female choice.     

Obesity,race and the indigenous origins of health risks among Mexican mestizos

We explore the discourses of Mexican scientists and doctors on genetics and obesity and how these relate to ideas about race, class and national identity. Drawing on interviews with geneticists and doctors treating obese children, the paper makes two contributions to the literature on race and medical science. First, although our data reveal familiar racializing tendencies among geneticists, a more nuanced view is needed, as medical doctors who are sceptical about genetic explanations nevertheless tend to racialize, using more environmental and cultural explanations, which adduce epigenetic mechanisms. Second, rather than focusing on minority groups, as in much literature on racialization and genetics, in Mexico ideas about racialized genetic (and cultural) ancestry also impinge on the majority “mestizo” (mixed-race) population, opening broader panoramas of racialized pathologization. These two factors represent an overall strengthening of discourses of race in Mexico and probably in much of Latin America.     

External auditory exostosis in prehistoric Chilean populations: A test of the cold water hypothesis

Over one thousand prehistoric crania (n = 1,149) from northern Chile were analyzed to determine if the presence of external auditory exostosis (EAE) was a type of subsistence-induced pathology, a consequence of habitual fishing i the cold water of the Pacific Ocean, rather than genetically determined. To test this occupational hypothesis, the sample was divided according to chronology, type of economy, site elevation, and sex. The crania came from 43 sites, including the coast, lowland valleys (100–2,000 m), and highlands (2,000 to 4,000 m) with a time frame of 7,000 B.C. to the Inca era (1500 A.D.). There was a significant association between EAE, environment, and sex. The coastal inhabitants had the highest prevalence of EAE with 30.7% (103/336), followed by 2.3% (6/264) for the valley people and 0% (0/549) for highlanders. Coastal and valley men were significantly more affected than their female counterparts. Contrary to expectations, there was nonsignificant association between EAE and economy and/or chronology. In the Arica area, the early Chinchorro fishers, without agriculture, had 27.7% (26/94) EAE, the subsequent agro-pastoralists, 42.7% (32/75), and the late Arican agro-pastoral fishers had 35.6% (36/101) EAE. Apparently, with the advent of agriculture, the coastal Arican populations increased their ocean harvests, rather than decreased them, to gain a surplus in order to trade with nonmaritime groups. Am J Phys Anthropol 103:119–129, 1997. © 1997 Wiley-Liss, Inc.     

Toward reducing the prevalence of chronic disease: a life course perspective on health preservation

Chronic disease is now hyper-endemic in the United States and is the central problem to be addressed in efforts to enhance the health of the American population. Efforts to reduce the prevalence of chronic disease through diminished exposure to risk factors have achieved significant success in recent decades, but most have been expressions of secondary or tertiary prevention. Current knowledge suggests it would be more effective to extend efforts directed at reduction of risk to earlier phases in the biology of chronic diseases, and to maintain them over the life course. This approach lends itself to a health preservation perspective-in other words, to an orientation around protection of the future health of the individual across the lifespan, from preconception to old age. This will require linked efforts of the clinical, public health, and policy communities, together with private-sector collaborators in information management, marketing, and other areas of expertise.     

Studies of albumin binding to rat liver plasma membranes: Implications for the albumin receptor hypothesis

To characterize a previously proposed hepatocyte albumin receptor, we examined the binding of native and defatted ¹²⁵I-labeled rat albumin to rat liver plasma membranes. After incubation for 30 min, binding was determined from the distribution of radioactivity between membrane pellet and supernatant following initial centrifugation (15 000 × g for 15 min), after repeated cycles of washing with buffer and re-centrifugation. ¹²⁵I-labeled albumin recovered in the initial membrane pellet averaged only 4% of that incubated. Moreover, this albumin was only loosely associated with the membrane, as indicated by recovery in the pellet of under 0.5% of the counts after three washes. Binding of ¹²⁵I-labeled albumin to the plasma membranes was no greater than to erythrocyte ghosts, was not inhibited by excess unlabeled albumin, and was not decreased by heat denaturation of the membranes, all suggestive of a lack of specific binding. Failure to observe albumin binding to the membranes was not due to a rapid dissociation rate or ‘off-time’, as incubations in the presence of sufficient ultraviolet light to promote covalent binding of ligands to receptors did not increase ¹²⁵I counts bound to the membrane. Finally, affinity chromatography over albumin/agarose gel of solubilized membrane proteins provided no evidence of a membrane protein with a high affinity for albumin. These studies, therefore, do not support the hypothesis that liver cell plasma membranes contain a specific albumin receptor.