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THE ANTHROPOLOGYOF
INFECTIOUS DISEASE
Annu. Rev. Anthropol. 1990.19:89-117. Downloaded from arjournals.annualreviews.org
Marcia C. lnhorn
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Department
of Anthropology,University of California, Berkeley, California 94720
Peter J. Brown
Departmentof Anthropology,EmoryUniversity, Atlanta, Georgia30322
KEYWORDS:
evolution, disease ecology, behavioral research, ethnomedicine, infectious
disease control
INTRODUCTION
BIOLOGICAL APPROACHES
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Microevolutionary Studies
Froman evolutionary perspective, infectious diseases have probably been the
primary agent of natural selection over the past 5000 years, eliminating
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humanhosts who were more susceptible to disease and sparing those who
were moreresistant. Individual biological factors that conferred protection
from a specific disease could eventually be selected for in the humanpop-
ulations living where the disease was endemic. Thus, as first suggested by
Haldane(102), humansadapted to infectious disease at a most basic level--
the level of the gene (5, 6).
Over the past 40 years, anthropologists and humangeneticists have been
testing the hypothesis that specific genotypes mayconfer immunityor resis-
tance to infection. Such hypotheses have also been suggested to help explain
relatively common genetic conditions that maybe adaptive in one context and
maladaptive in another. Allison (4) was the first to suggest that the
heterozygouscondition knownas sickle-cell trait (i.e. inheritance of the gene
for the commonform of hemoglobin from one parent and the sickling
hemoglobinS from the other) appeared with greater frequency in regions of
Africa where life-threatening Plasmodiurnfalciparum malaria was present.
This association led Allison to hypothesize that hemoglobinS, whenpresent
in the heterozygous state, conferred resistance to death from malaria.
Although this hypothesis has been a prominent textbook example for two
decades, the statistical correlation betweenmalaria prevalences and sickle-
cell gene frequencies in West Africa has only recently been systematically
confirmed(70). Moreover,while there is significantly higher malaria mortal-
ity amongchildren who are heterozygous sicklers than amonghomozygous
normals, differences in parasite densities amongindividuals of the two geno-
type groups have not been determined (159).
In a classic anthropological work that followed Allisons, Livingstone
(158) related the widespreaddistribution of the sickle-cell trait in WestAfrica
to specific factors of cultural evolution: namely,the introduction of iron tools
and subsequent swiddenagriculture. He argued that the diffusion of the new
technology led to increased sedentism, horticultural production, and de-
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92 INHORN & BROWN
and HbF. Similarly, it has been argued that the Duffy blood group negative
genotype, characteristic of most African and USblacks, provides a high level
of protection from Plasmodiumvivax, a more benign strain of malaria (164).
In an examinationof fava bean consumptionand its relation to malaria in the
G6PD-deficiency-endemic, circum-Mediterranean area, Katz &Schall (136)
have suggested that the combination of nonexpressed gene and consumption
of lava beans (the "gene-beaninteraction") mayprotect heterozygousfemales
from malaria death. This may be viewed as an excellent example of the
"coevolution" of genes and cultural traits, which, in combination, offer
substantial protection from disease (135), although in this case, G6PD-
deficient males maysuffer potentially fatal hemolyticcrises of favism (32).
Other studies tentatively linking infectious diseases to genetic traits and
cultural factors have recently emerged. For example, Blangero (18) studied
the relationship amonghelminthic zoonoses, the P2 allele of the P blood
group system (which is hypothesized to confer resistance to these zoonoses),
and subsistence practices involving animal husbandry. He has shownthat
high frequencies of the P2 allele occur in populations manifesting heavy
dependenceon and contact with domesticated livestock. In a different con-
text, Meindl (174) has hypothesized that, for European populations with
long history of pulmonarytuberculosis and high frequencies of cystic fibrosis,
carriers of the recessive genefor cystic fibrosis mayhave increased resistance
to tuberculosis.
Conversely, anthropologists helped to demonstrate that the hepatitis B
surface antigen (HBsAg)was not part of the genetic endowmenttransmitted
from parents to offspring. Rather, the clustering of the antigen observed in
families was due to both horizontal (i.e. person to person) and vertical (i.e.
mother to infant) infectious transmission (20-22)---a finding made,in part,
through participant observation of family life in NewHebrides (51, 52).
Thesediscoveries played a role in the successful developmentof a hepatitis B
vaccine.
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INFECTIOUSDISEASE 93
Macroevolutionary Studies
Macroevolutionary studies of infectious disease attempt to reconstruct
epidemiological patterns of disease transmission amongprehistoric and
historic humanpopulations. The broad aims of this research are two-fold: (a)
to establish the antiquity and evolution of various infectious diseases in
humanpopulations through examination of prehistoric osteological and, in
somecases, soft-tissue evidence; and (b) to contextualize these findings to the
physical and cultural circumstances of the humanpopulations involved.
Paleopathologyhas contributed significantly to the understanding of the
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(16, 17, 40, 95, 185). Basing their theses largely on serological evidence
collected from contemporaryhunter-gatherer groups, they hypothesize that,
because of their small numbers,mobility, and relative isolation from other
groups, ancient hunter-gatherers were relatively free from the acute, epidemic
infectious diseases that later took their toll on moreadvancedagrarian societ-
ies. Manyacute infectious diseases require large numbersof susceptible
individuals to support their chains of transmission, whichare characterized by
brief and rapid stages of infection. In early food-foraging groups, populations
of no more than 200-300persons wouldnot have been large enoughto sustain
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other primary and secondarysources, they have chronicled the impact of such
infectious diseases as the plague (53), typhus (226), cholera (202), malaria
(105), and smallpox(115), for better and for worse, uponstate-level societies
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ECOLOGICAL APPROACHES
Theoretical Models
Most anthropological research on infectious disease has been ecological,
focusing on the interaction betweenagent and host within a given ecosystem.
Disease ecology, as the discipline is often called (33), owes muchto the
pioneering work of the medical geographer May,who in his classic volume
The Ecology of HumanDisease (167) formalized the role of the environ-
ment--both physical and sociocultural--in the study of infectious disease
problems. Mayconstructed a modelthat treated physical environment, dis-
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96 INHORN & BROWN
Muchof the recent empirical work in disease ecology has been, in fact,
political-economic, if not explicitly Marxistin orientation, in that it focuses
on the untoward consequences of ecologically ill-advised development
schemes. It concerns the so-called "developo-genic" diseases, the conse-
quence of environmentaldisruptions caused by large-scale, internationally
sponsoredprojects (123). Dubos(54, 55) was amongthe first to note that
technological innovation, whether industrial, agricultural, or medical, upset
the balance of nature; the sensible goal was thus not to maintainthe balance of
nature but to change it to the benefit of as manyplant and animal species
(including humans)as possible.
Unfortunately, manyof the developmentschemes of the past and present
have been neither balanced nor beneficial. As Hughes&Hunter (123) point
out in their comprehensive review of developmentprojects and disease in
Africa, few of the projects initiated on that continent over the past two
centuries have been undertaken within a preconceived ecological framework.
They include in their survey programsof agricultural, industrial, and in-
frastructural change, as well as resulting population relocations, all un-
dertaken in the nameof progress. As they note, developmentprojects of dam
construction, land reclamation, road construction, and resettlement in Third
World countries have probably done more to spread infectious diseases
such as trypanosomiasis, schistosomiasis, and malaria than any other single
factor.
The life-threatening blood fluke infection schistosomiasis (bilharziasis)
provides a trenchant example of the unforeseen health consequences of
ecological disruption caused by development schemes. As Heyneman(110,
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98 INHORN & BROWN
111) notes, schistosomiasis is probably the fastest spreading and most danger-
ous parasitic infection nowknown.The rapid spread of this disease is almost
entirely due to programsof water resource developmentinvolving the con-
struction of high dams, man-made lakes and reservoirs, and irrigation canals
(50, 110, 111, 208). These waterways have provided an ecological "free
zone" for the snails that are the intermediate host of the schistosomal para-
sites. As the snail population has spread throughout Africa and parts of the
Middle East, Asia, South America, and the Caribbean, so have schistoso-
miasis infections, whichare acquired whenlarval parasites, released in the
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areas of the world wherethe parasite and vector live. For example, Kloosand
coworkers (140, 141, 144, 145, 147) have described the expanding distribu-
tion of schistosome-transmitting snail populations and escalating rates of
humaninfection following government-sponsoredcreation of large, irrigated
farming estates in the AwashValley of Ethiopia. In neighboring Sudan, the
disease cycle was established within a few years of the start of the Gezira
scheme, a large-scale, irrigated cotton project south of Khartoum(83, 98,
147), which was also responsible for an increased prevalence of malaria in
this region (98). In Nigeria, the prevalence of schistosomiasis soared follow-
ing construction of a low-earth damproviding perennial access to a large body
of infective water--an increase that was likely to continue, researchers pre-
dicted, given governmentplans to build more damsin the area (198).
Subtler ecological changes mayalso be associated with increases in in-
fectious disease. For example, Chapin & Wasserstrom (37) have shownhow
increased pesticide use in the intensive production of cotton in both Central
Americaand India resulted in a serious resurgence of malaria because of the
rapid evolution of insecticide-resistant strains of Anophelesmosquitoes.Sim-
ilarly, the severe epidemic of typhoid fever in Mexicoin 1972-73 was the
result of overuse of the powerfulantibiotic chloramphenicolfor ailments such
as the commoncold; this change in disease ecology brought about rapid
selection for chloramphenicol-resistantstrains of the typhoid fever bacterium
(218).
SOCIOCULTURAL APPROACHES
infection thought to have killed more people than any other nameddisease
(159). Geneticadaptations to this disease havemerited particular interest, and
malariologists have recognized the important role of humanbehavior in
malaria control (see the bibliography in 213). Wood(223) summarizes
of the studies of cultural practices, most of themnondeliberate, that maylimit
transmission in areas where malaria is endemic. These include the use of
alkaline laundry soaps that destroy mosquitobreeding sites, clothing styles
that serve as mechanical barriers to biting insects, the use of malodorous
traditional pesticides and insect repellents, and seasonal migrations away
from mosquitovectors. Empirical evidence for the efficacy of such practices
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Sexually transmitted diseases (STDs) and labor migration The crucial role
of humanbehavioral factors in the dissemination of sexually transmitted
diseases (STDs) has been knownfor hundreds of years and is a reason why
these conditions were dubbed"social diseases." However,the need for social
scientific studies of the behaviors placing individuals at risk from STDs--and
of the sociocultural determinants and consequencesof those behaviors has
only been recognized recently. This need has been mademore urgent by the
appearance of AIDSduring the past decade (13, 81, 97, 127, 176). Prior
the recognition of AIDSas a widespread problem in sub-Saharan Africa, a
numberof behaviorally oriented researchers workingin that region (7, 15, 49,
173, 197,219) noted the roles of rural-to-urban migration and prostitution in
the transmission of STDs, primarily gonorrhea. The typical pattern of
transmission included the following components:Youngmenfrom rural tribal
areas--areas plagued by political upheaval, unemployment,rapid moderniza-
tion, and the uneven distribution of economicopportunities--migrate to
cities, wherethey makeup the clientele of prostitutes operating from bars,
brothels, dance-halls, and the street. These prostitutes, whoface the same
economicpressures as the males and are mostly young (aged 15-30), rural-
born, uneducated, unmarried (often as the result of abandonment by
nonreturning migrant husbands), and highly mobile, constitute the major
reservoir of sexually transmitted infection. The risk of STDtransmission is
even further increased when menmigrate to isolated labor camps and mines
where, characteristically, a small numberof prostitutes have sexual relations
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INFECTIOUSDISEASE 103
fact that villagers had their own ideas, both "scientific" and "magico-
religious," about the cause of the outbreak; for mostvillagers, prevention did
not involve acceptance of an injection. Similarly, in BangChan, Thailand,
only a handful of villagers availed themselves of diphtheria immunization,
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ACKNOWLEDGMENTS
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