Reconciling “Stress” and “Health” in PhysicalAnthropology: What Can Bioarchaeologists LearnFrom the Other Subdisciplines?

Laurie J. Reitsema1* and Britney Kyle McIlvaine2

1Department of Anthropology, University of Georgia, Jackson St., Athens, GA, 306022Department of Anthropology, University of Northern Colorado, Greeley, CO 80639

KEY WORDS bioarchaeology; human biology; interdisciplinary; skeletal stress;paleopathology

ABSTRACT The concepts of “stress” and “health” arefoundational in physical anthropology as guidelines forinterpreting human behavior and biocultural adaptationin the past and present. Though related, stress andhealth are not coterminous, and while the term “health”encompasses some aspects of “stress,” health refers to amore holistic condition beyond just physiological disrup-tion, and is of considerable significance in contributingto anthropologists’ understanding of humanity’s livedexperiences. Bioarchaeological interpretations of humanhealth generally are made from datasets consisting ofskeletal markers of stress, markers that result from(chronic) physiological disruption (e.g., porotic hyperosto-sis; linear enamel hypoplasia). Non-specific indicators ofstress may measure episodes of stress and indicate thatinfection, disease, or nutritional deficiencies were pres-

ent in a population, but in assessing these markers, bio-archaeologists are not measuring “health” in the sameway as are human biologists, medical anthropologists, orprimatologists. Rather than continue to diverge on sepa-rate (albeit parallel) trajectories, bioarchaeologists areadvised to pursue interlinkages with other subfieldswithin physical anthropology toward bridging “stress”and “health.” The papers in this special symposium setinclude bioarchaeologists, human biologists, molecularanthropologists, and primatologists whose researchdevelops this link between the concepts of “stress”and “health,” encouraging new avenues for bioarchaeolo-gists to consider and reconsider health in past humanpopulations. Am J Phys Anthropol 155:181–185,2014. VC 2014 Wiley Periodicals, Inc.

In physical anthropology, understanding stressorsimplicit in human interactions with the environmentand with each other is a key component of interpreting,and even anticipating, human health. Human skeletalremains offer a deep well of information about humanvariation, activity patterns, use of landscapes, diet andfood distribution, demography, disease, and stress.Extrapolating from skeletal data sets, bioarchaeologistsmake inferences about health and lifestyle of past popu-lations. Yet, the relationship between skeletal stress andhealth is difficult to pinpoint. “Stress” can be defined asa physiological change caused by strain on an organismfrom environmental, nutritional, and other pressures(Huss-Ashmore et al., 1982; Goodman et al., 1988), andis a useful proxy for estimating some aspects of pasthealth. “Health” is a holistic concept used colloquially toencompass elements of quality of life, daily functioning,and community interaction, and is at the crux of evolu-tionary and biocultural approaches in anthropology.Although “health” has broad colloquial recognition, ithas been difficult to quantify. In practice, health is per-haps most commonly understood to be something that iscompromised when any number of factors, including dis-ease, infection, nutritional quality, or psychological fac-tors, affect an individual’s quality of life. However, theWorld Health Organization includes the stipulation thathealth is “a state of complete physical, mental, andsocial well-being and not merely the absence of disease,or infirmity” (WHO, 1999). Even a new infant with tenfingers, ten toes, and all of their organs in place is recov-ering from the trauma of birth and cannot be said

ideally to represent health (Goodman and Armelagos,1989). Expressions of “health” exist on a continuum,meaning that even if consensus is reached over themeaning of health as a concept, the meaning of “healthy”remains vague. As difficult as health, lifestyle, and well-being are to define and measure in living populations,these aspects of human existence become even more elu-sive when dealing with past populations, whose symp-toms and etiologies are less apparent and more difficultto interpret (Wood et al., 1992).

Although we may never be able to agree on what rep-resents “healthy,” we may be able to agree that physio-logical changes in the body as a result of stress are“unhealthy”; although they are examples of humanadaptation and adaptability (Seckler, 1980; Stuart-MacAdam, 1992), physiological changes often exert a taxon the human body. Viewed in this manner, stress is auseful proxy for health in past populations (Goodmanet al., 1988; Goodman and Armelagos, 1989). Generallyspeaking, bioarchaeologists are aware that stress and

*Correspondence to: Laurie J. Reitsema. Department of Anthro-pology, University of Georgia, 250 Baldwin Hall, Jackson St., Ath-ens, Georgia 30602, USA. E-mail: reitsema@uga.edu

Received 18 July 2014; revised 7 August 2014; accepted 8 August2014

DOI: 10.1002/ajpa.22596Published online 19 August 2014 in Wiley Online Library

(wileyonlinelibrary.com).

� 2014 WILEY PERIODICALS, INC.

AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 155:181–185 (2014)

health are not coterminous (McIlvaine and Reitsema[2013] report a metanalysis of authors’ use of theseterms in leading journals during past decades). Bioarch-aeological stress models account for synergistic interac-tions of environmental constraints, biology, culturalbuffering systems, and psychological disruption in con-tributing to a physiological stress response (Goodmanet al., 1988; Temple and Goodman, this issue). Otherproxies for interpreting health may include a popula-tion’s access to proper sanitation and nutrition, changesin living conditions within a person’s lifetime, the partic-ular timing of onset of disease or malnutrition, commu-nity structure and family or community support, andtraits of resistance or susceptibility to stress and diseasefrom the genome and epigenome. Contextual elementssuch as these may or may not be available to the bio-archaeologist, but should be included in all assessmentsof skeletal remains, where possible, to better understandthe etiology and pathophysiology of skeletal stressmarkers (Goodman, 1993; Goodman and Leatherman,1998).

To infer past human health from skeletal stressrequires a middle ground. Conveniently for physicalanthropologists, this middle ground can be built by com-municating across anthropology’s subfields. The articlesin this issue stem from a symposium organized for the2013 meeting of the American Association of PhysicalAnthropologists, conceived initially by the authors as ameans to draw together interdisciplinary perspectives onstress. The effort to understand ancient stress andhealth scientifically crystallized notably with the 1984publication of the edited volume, “Paleopathology at theOrigins of Agriculture” (Cohen and Armelagos, 1984).Enthusiasm for this topic is evidenced by the continuedscholarly work undertaken and published in the decadesthat followed. The goal of the symposium was to re-castlight on the relationship between stress and health, andrefocus researchers on the symposium’s theme—fleshingout the skeletal record with insights from the otheranthropological subdisciplines—such that this themecould be revisited as a concrete conceptual target toguide and inspire future, focused, holistic research inbioarchaeology. The original 2013 symposium comprisedhuman biologists and bioarchaeologists whose researchspecifically addresses the imperfect relationship betweenstress and health. Additional papers contributed hereinclude considerations of stress and health in primatol-ogy, molecular anthropology, and biomechanics.

This symposium set and additional contributed papersbridge the concepts of stress and health in two ways: (1)incorporating perspectives from modern humans andnon-human primates to link the past with the present,and (2) highlighting recent bioarchaeological work thatspecifically addresses an imperfect relationship betweenstress and health. The papers drawn together here pro-vide new insight into our current understanding ofstress and health in bioarchaeological populations.

REVISITING THE RELATIONSHIP BETWEENSTRESS AND HEALTH: INTRODUCTION

TO PAPERS IN THE SPECIAL ISSUE

The purpose of this issue is to promote cross-subdisciplinary awareness, in order to account for thesynergistic interactions of environmental constraints,biology, cultural buffering systems, and psychologicaldisruption in contributing to a physiological stress

response. Links with human biologists, primatologists,and geneticists help to identify those social and culturalconditions that contribute to physiological stress, butthat cannot be directly observed in bioarchaeologicalsamples. Two papers in this issue use a molecularapproach to address the effects of very early life condi-tions—particularly, social stressors—on growth, develop-ment, health, and well-being using epigenetic proxies(Kinnally [this issue]; Rodney and Milligan [this issue]).Erin Kinnally examines the relationship between earlymaternal care quality, DNA methylation, and later-lifehealth outcomes among rhesus macaques. Kinnally’sdata show that better maternal care, in the form of posi-tive contact, relates to lower methylation of a possiblestress pathway gene (serotonin transporter, 5-HTT).Furthermore, among rhesus infants whose 5-HTT regionwas methylated, poor health outcomes were observedlater in their lives. These outcomes include low bodyweight, overall poor body condition, and lifetime inci-dence of inflammatory disease (diarrhea). Studies ofDNA methylation in osteoclasts, which are related towhite blood cells, may play a role in bioarchaeology.

Very early life and intergenerational effects play aconsiderable role in health and stress. Sobering evidenceof this phenomenon is presented by Rodney and Mulli-gan (this issue), who explored the biological consequen-ces of war stress on mothers and their infants in theDemocratic Republic of Congo. Exposure to war stress,and especially experience of rape, is associated with lowinfant birth weight and methylation levels. The authorsfind that effects of war stress on the epigenome are notgenome wide, but targeted at specific genes—in thiscase, glucocorticoid receptor gene NR3C1. The relation-ship between glucocorticoids and skeletal growth impliesthat psycho-social stress has effects on the growth anddevelopment of subsequent generations. In addition toproviding new perspectives on the relationship betweenearly life stressors and health outcomes, the papers byKinnally and Rodney and Mulligan in this issue are tes-taments to the importance of social stress in long-termadverse physiological consequences, and a reminder thatage, sex, status, ancestry, etc. do not present a completecontextual framework for interpreting skeletal stress.Kinnally and Rodney and Mulligan demonstrate thatvery early life and generational effects play an impor-tant role in manifestations of health and stress.

A complication when using physiological stressmarkers to measure health in past populations is thatself-perceptions of health and quality of life may nottrack well with a person’s physiological state. For thisreason, it is important to use living populations to exam-ine critically the relationships between perceptions ofhealth and (skeletal) indicators of stress. The work ofPiperata and colleagues (this issue) and Tanner (thisissue) provide a cautionary tale for bioarchaeologistswho assume a one-to-one association between a singleskeletal stress marker (e.g., porotic hyperostosis; infec-tion) and economic status, quality of life, and/or lifeexperiences. However, these papers also demonstrate thepossibilities for addressing health in skeletal populationsthrough the assessment of multiple stress indicators(Steckel and Rose, 2002), and the need for addressingindividual frailty within skeletal assemblages (see alsoWilson, this issue). Piperata and colleagues’ (this issue)paper demonstrates disconnects between self-perceptionof health and anemia status at the individual and house-hold levels. The authors report that despite a statistical

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association of anemia status with economic status, self-perceptions of health, and work capacity, there was sig-nificant variation within the anemic and non-anemicgroups as the result of individual frailty stemming fromboth biological and cultural risk factors. This observa-tion indicates that porotic hyperostosis should not betaken as a direct indicator of health or economic status.Piperata et al. (this issue) also show that biological andcultural factors place children under the age of five atthe highest risk for anemia. As porotic hyperostosis typi-cally is representative of a childhood condition (Stuart-MacAdam, 1985), it may not accurately estimate physio-logical status of an individual at the time of death, sug-gesting that greater care should be taken bybioarchaeologists to document active versus healedlesions (Walker et al., 2009) and to control for age-at-death (DeWitte, this issue; Wilson, this issue).

Anthropologists are uniquely capable of appreciatinghow socioeconomic and environmental changes relatedto human health. However, these relationships are medi-ated by individual, household, and community factorsthat bioarchaeologists may not be able to reconstructfully, but which should be appreciated as variablesaffecting, and frequently muddying, the relationshipbetween stress and health in the past. The work ofSusan Tanner (this issue) on helminth infections amongthe Tsimane’ of lowland Bolivia examines individual,household, and community factors that explain why peo-ple’s infection by widespread soil-transmitted helminthworms is not clearly associated with general nutritionalstatus. Her work shows how proximity to a regionalmarket center mediates the severity of helminth infec-tion and malnutrition, albeit not in straightforwardways. Despite the potential that childhood infectionshave to adversely affect growth and health adversely,Tanner’s work shows how this near-ubiquitous source ofnutritional and energetic stress is only loosely related toreduced functionality and skeletal markers of stress.Tanner’s results also demonstrate the importance of con-sidering health in the context of communities andregional settlement structures: among the participantsin her study, individuals living farthest from the mod-ernizing effects of a market center exhibit the highestprevalence of helminth infection, followed by people liv-ing closest to the market center. The communities mid-way from the market center exhibit the lowest rates ofinfection, possibly reflecting a mix of traditional subsist-ence and modern sanitation that fostered betterhealth—at least, in terms of infection burden.

Bioarchaeology in this special issue builds on work ofothers who have shown that taking a populationapproach, standardizing for skeletal age, appreciatingsociodemographic context, and analyzing multiple indi-cators of stress may mitigate errors in our interpreta-tions of health, using stress indicators as proxies.Several papers in this issue emphasize the importanceof critically evaluating commonly accepted indicators ofstress and health, such as stature (Robbins-Schug, thisissue, Vercellotti et al., this issue) and skeletal lesions(DeWitte, this issue; Wilson, this issue), in light ofpopulation approaches, updated techniques, andcomplementary lines of evidence.

Stature is a commonly used proxy for stress andadverse health, yet has multiple etiologies. GiuseppeVercellotti and colleagues (this issue) highlight the com-plex relationship between stature and early life condi-tions in both living and archaeological populations.

Their work provides a cautionary tale for researchersmaking simple correlations between stature and lifeexperiences, and demonstrates that ultimate adult stat-ure results from a combination of genetic, cultural, andenvironmental factors, including genetic height poten-tial, environmental quality and nutrition early in life,catch-up growth, social and economic inequality, and cul-tural buffering. To circumvent the issues inherent inassociating terminal adult stature directly with life con-ditions, Vercellotti and colleagues bridge the gapbetween bioarchaeological and human biological analy-ses of stature to examine the many dimensions ofstature.

As Vercellotti et al. (this issue) discuss, stature is com-monly used as a proxy for stress and adverse health, yetbody size is influenced by other factors, including genes.Gwen Robbins-Schug (this issue) tests the hypothesisthat reduced body size observed in a population post-dating abandonment of traditional agricultural methodsand depopulation of agglomerated centers was, in fact,the result of homeostatic disruption from health chal-lenges by evaluating bone geometry and histology amongsubadults. Speculatively, reductions in body size withsociodemographic change are the result of growth falter-ing and health challenges (for which stature is a proxy).However, a low prevalence of gross bone pathologyreported for the population complicated an associationbetween health challenges and growth faltering. Histo-logical evidence indicates children under the age of tendid not acquire or maintain bone mass expected for theirage and their demonstrated mobility patterns, support-ing the hypothesis that body size is the result of poorhealth during growth in this case. This work under-scores a theme in the special issue; namely, that com-monly used indicators of stress should not uncriticallybe accepted as evidence of poor health.

Equal in importance to evaluating the underlying eti-ologies of skeletal manifestations of stress critically isthe appreciation of context in the skeletal record. Wheninferring stress and health from subadults in archaeo-logical contexts, a cross-sectional approach is commonlytaken, wherein many individuals in a population whodied at different ages are interpreted to represent thelife history trajectory of the population at large. Withtheir publication on the osteological paradox, Wood et al.(1992) noted that selective mortality (the fact that allpeople who are dead are inherently unhealthy, therebyoverestimating the prevalence of skeletal lesions in eachage category) and hidden heterogeneity (essentially, theproblem of interpreting individuals who survived longenough to develop skeletal stress markers as unhealthywhen their survival may be a testament to their surviv-ability and good health) complicate the assessment ofphysiological markers of stress in human skeletalremains. The problems of selective mortality and differ-ential frailty are salient considerations in cross-sectionalapproaches, because subadults who died at young agesmay have experienced different circumstances than thesubadults who lived past a young age (i.e., the adults ina population).

DeWitte (this issue) and Wilson’s (this issue) researchhighlights the importance of modeling physiologicallesions against age-at-death to assess frailty better (afterBoldsen et al., 2002). Sharon DeWitte’s paper empha-sizes the need for new methods (transition analysis toestimate age) and detailed contextual information whenassessing health outcomes from skeletal remains. On the

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surface, DeWitte’s data seems to suggest that healthdeclined following the Black Death in England. However,standardization for age shows that while the prevalenceof periostitis is higher in her post-Black Death sample,this sample includes a larger proportion of older adultswho were able to live long enough to accumulate perios-teal lesions throughout their relatively longer lives. Herwork shows that a major selective pressure (the BlackDeath) targeted the frailest individuals, leaving a gener-ally healthier population with greater survivorship fol-lowing the Black Death.

Like DeWitte (this issue), Jeremy Wilson’s paper inthis special issue demonstrates the importance of exam-ining age- and sex-specific mortality patterns in associa-tion with physiological markers of skeletal stress. Hiswork uses hazard models to explore variation in risk ofdeath with age in order to address the issues of selectivemortality and differential frailty in skeletal assemblages.The results of Wilson’s (this issue) research show thatwomen of reproductive age had an increased risk ofdeath, yet surviving these reproductive years is associ-ated with increased survivorship into old age, when com-pared with their male counterparts. Risk of death in thereproductive years among females increased throughtime and likely contributed to depopulation of the lowerMidwest around A.D. 1500. Concurrently, individualswho experienced childhood stress, as evidenced by linearenamel hypoplasia, had an increased risk of death at allages for both males and females. Wilson’s (this issue)research demonstrates how childhood experiencesimpact health outcomes later in life (also see Kinnally,this issue).

Other papers in this issue emphasize the importanceof interpreting stress and health from a life-history per-spective. Paul Sandberg and colleagues (this issue)examine weaning age of subadults from the Kulubnarticollection of Sudanese Nubia using a longitudinalapproach, achieved via incremental sampling of toothdentine from individuals. In creating a refined life his-tory of diet and weaning behavior, the authors are ableto report that the timing of stress (estimated from linearenamel hypoplasias) accords with the period of weaning,rather than the period before or after weaning. Theauthors also compare dentine stable isotope ratios ofsubadults with rib stable isotope ratios of adults fromthe same population. The comparison of weaning behav-ior of subadults who lived (i.e., adults), and subadultswho died, reveal weaning may have occurred earlier forindividuals who lived past childhood, suggesting“healthy” benefits of a life history strategy involving ear-lier weaning, helping to clarify the role of weaning ininfant mortality bias. Sandberg and colleagues’ workshows how a life history approach to bioarchaeology tapsa deeper well of data from skeletal samples towardinforming our assessment of “health” in the past,addressing issues implicit in the osteological paradox.

A goal of the symposium from which this issue devel-oped was promoting cross-disciplinary awareness inphysical anthropology. Haagen Klaus’ (this issue) paperembraces this theme by combining multiple lines of evi-dence, not only within physical anthropology, but draw-ing from a wide array of cross-disciplinary perspectiveson stress. Klaus provides a thoughtful and comprehen-sive discussion of the molecular signaling factorsinvolved in the development of periostitis; implicationsof epigenetic phenomena on disease and other healthoutcomes; the role of the microbiome in altering

hormone levels, levels of inflammation, and the develop-ment of the immune system as underpinnings of futurehealth outcomes; and the importance of examining theinfluences of age-at-death on disease prevalence (seealso Wilson, this issue). Klaus’ work should serve as amodel for all bioarchaeologists in considering the epide-miology and pathophysiology of skeletal stress markersthey study.

CONCLUSION

The impetus for this symposium is straightforward:the most meaningful understanding of health possiblecomes from work with living humans and non-humanprimates. This special issue set facilitates a betterappreciation of the meanings and definitions of “stress”and “health,” the biocultural context of “health,” innova-tive approaches in bioarchaeology, and the meaningfulimpact of stress on actual day-to-day functioning. Ratherthan serving as a check to bioarchaeology, the papers inthis issue show that greater collaboration among humanbiologists and bioarchaeologists will permit greater, notless, liberty in accurately estimating past health. Byimproving our understanding of physical manifestationsof poor health, disease, malnutrition, and stress, and bystudying the functional consequences of these conditionsin their varying degrees of severity, we can assess moreconfidently not only stress in the past, but also legaciesand prospects in human health.

ACKNOWLEDGMENTS

The authors wish to thank all the authors who contrib-uted to this special issue and who participated in the 2013symposium. They are also grateful to Peter Ellison for hissupport in putting together this special issue, the helpfulfeedback of an anonymous reviewer, and the AmericanAssociation of Physical Anthropologists.

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