Inhorn-AnthropologyInfectiousDisease-1990
Inhorn-AnthropologyInfectiousDisease-1990
Inhorn-AnthropologyInfectiousDisease-1990
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Review of Anthropology
THE ANTHROPOLOGY OF
INFECTIOUS DISEASE
Marcia C. Inhorn
Peter J. Brown
INTRODUCTION
89
0084-6570/90/10 15-0089$02.00
fectious disease as the "broad area which emphasizes the interactions between
sociocultural, biological, and ecological variables relating to the etiology and
prevalence of infectious disease" (26:7). This review uses the same definition,
examining anthropological works on infectious disease (including those by
scholars in related disciplines whose methods or theoretical frameworks are
anthropological in nature) and classifying them for heuristic purposes accord-
ing to their primarily biological, ecological, or sociocultural orientation.
BIOLOGICAL APPROACHES
Microevolutionary Studies
From an evolutionary perspective, infectious diseases have probably been the
primary agent of natural selection over the past 5000 years, eliminating
human hosts who were more susceptible to disease and sparing those who
were more resistant. Individual biological factors that conferred protection
from a specific disease could eventually be selected for in the human pop-
ulations living where the disease was endemic. Thus, as first suggested by
Haldane (102), humans adapted to infectious disease at a most basic level-
the level of the gene (5, 6).
Over the past 40 years, anthropologists and human geneticists have been
testing the hypothesis that specific genotypes may confer immunity or resis-
tance to infection. Such hypotheses have also been suggested to help explain
relatively common genetic conditions that may be adaptive in one context and
maladaptive in another. Allison (4) was the first to suggest that the
heterozygous condition known as sickle-cell trait (i.e. inheritance of the gene
for the common form of hemoglobin from one parent and the sickling
hemoglobin S from the other) appeared with greater frequency in regions of
Africa where life-threatening Plasmodium falciparum malaria was present.
This association led Allison to hypothesize that hemoglobin S, when present
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 between malaria 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 among children who are heterozygous sicklers than among homozygous
normals, differences in parasite densities among individuals of the two geno-
type groups have not been determined (159).
In a classic anthropological work that followed Allison's, Livingstone
(158) related the widespread distribution of the sickle-cell trait in West Africa
to specific factors of cultural evolution: namely, the introduction of iron tools
and subsequent swidden agriculture. He argued that the diffusion of the new
technology led to increased sedentism, horticultural production, and de-
Macroevolutionary Studies
Macroevolutionary studies of infectious disease attempt to reconstruct
epidemiological patterns of disease transmission among prehistoric and
historic human populations. The broad aims of this research are two-fold: (a)
to establish the antiquity and evolution of various infectious diseases in
human populations through examination of prehistoric osteological and, in
some cases, soft-tissue evidence; and (b) to contextualize these findings to the
physical and cultural circumstances of the human populations involved.
Paleopathology has contributed significantly to the understanding of the
prevalence and spread of infectious diseases in human populations. Simply
defined, paleopathology is the study of disease in prehistoric populations
through examination of skeletal and tissue remains, coprolites, and when
available, works of art (1, 130). Because some infectious diseases leave their
marks on the human skeleton and flesh, examination of these remains has
allowed researchers to describe the disease patterns of prehistoric populations
and to establish relative chronologies.
Paleopathological reconstructions utilizing skeletal and tissue remains have
been attempted for infectious diseases including tuberculosis (34, 181), lep-
rosy (179), and American (203) and African trypanosomiasis (151). Studies
of the kidneys of Egyptian mummies have yielded evidence of schistoso-
miasis (191); and coprolite studies, utilizing dried fecal remains found in or
near prehistoric camps and shelters, have provided valuable insights on the
epidemiology of intestinal helminthiases in prehistoric populations (40, 69,
191, 201, 205, 206).
Paleopathology has had a particularly decisive role in the debate over the
antiquity and origin of syphilis in the Old and New Worlds. Using osteologi-
cal evidence, paleopathologists have argued that human venereal syphilis
originated in the Americas and was transported to Europe and then to other
human habitats by European colonists and explorers, including, as Crosby
(45, 46) has argued, Christopher Columbus's crew. This conclusion is based
on abundant evidence of syphlitic skeletal material from pre-Columbian
remains discovered in the New World (43, 93, 94, 179, 181, 200, 222) and
the distinct absence of pre-Columbian, Old World skeletal material with any
of the treponemal stigmata (223). Nevertheless, other reconstructions of the
history of syphilis based on contemporary and historical knowledge of the
treponemal diseases have been put forward (39, 99, 119-122); these have
been well summarized by McNeill (172) and Wood (223).
In addition, paleoepidemiological reconstruction of infectious disease pat-
terns in prehistoric and early historic human populations has been undertaken
through ethnographic analogy-that is, examination of disease patterns in
contemporary isolated hunter-gatherer populations followed by extrapolation
of these findings into the past. First suggested by Dunn (58) and Polunin
(196), this approach has been advocated subsequently by a number of scholars
(16, 17, 40, 95, 185). Basing their theses largely on serological evidence
collected from contemporary hunter-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 more advanced agrarian societ-
ies. Many acute infectious diseases require large numbers of susceptible
individuals to support their chains of transmission, which are characterized by
brief and rapid stages of infection. In early food-foraging groups, populations
of no more than 200-300 persons would not have been large enough to sustain
such a chain of transmission; if introduced, these acute infections would have
run their courses and then died out. From the standpoint of natural selection,
pathogens that live in a long-term commensal relationship with the host (e.g.
the agents of typhoid, amoebic dysentery, trachoma) and those that persist for
periods of time outside the final host or vector (e.g. the agent of schistoso-
miasis) would have been favored, and infections like measles, which spreads
rapidly and immunizes a majority of the population in one epidemic, would
have been rare or absent.
A number of scholars (5, 40, 55, 56, 82, 171, 195) have gone beyond this
original proposition to describe the coevolution of human culture and in-
fectious disease, basing their arguments largely on knowledge of population
size and density and their impact on infection. Humans made a rapid cultural
transition from small, isolated groups of hunter-gatherers to small, scattered
villages of farmers, to large, preindustrial and then industrial cities, marked
by aggregates of people living in close proximity. This cultural transition
profoundly affected the nature of infectious disease patterns by (a) changing
the degree of contact between humans and animals, either directly or via
arthropod vectors, and (b) altering the size of human aggregations and the
communications and movement within and between them. Thus, the con-
tagious epidemic diseases, which would not have had a large enough popula-
tion base to affect hunter-gatherers or even small farming villages, would
eventually decimate populations in urban centers.
Likewise, the clearing of land for cultivation, the domestication of animals,
the increase in sedentism, and the concomitant problems of human and animal
waste removal, all of which occurred during the agricultural revolution of the
Neolithic and Mesolithic periods, provided ideal conditions for many of the
helminthic and protozoal parasites (5). The health consequences of this
transition from food foraging to food production have been topics of consider-
able attention, as seen in the important collection Paleopathology at the
Origins of Agriculture (42). Twelve of the eighteen case studies in this
collection report substantial increases in infection rates from the time of early
hunter-gatherers to early farmers (41). Research from both the Old and New
Worlds shows a repeated pattern of decreased stature, higher infant mortality,
ECOLOGICAL APPROACHES
Theoretical Models
Most anthropological research on infectious disease has been ecological,
focusing on the interaction between agent and host within a given ecosystem.
Disease ecology, as the discipline is often called (33), owes much to the
pioneering work of the medical geographer May, who in his classic volume
The Ecology of Human Disease (167) formalized the role of the environ-
ment both physical and sociocultural in the study of infectious disease
problems. May constructed a model that treated physical environment, dis-
ease pathogens, human hosts, and the cultural practices employed by these
hosts as separate factors in an interactive process. In this view, disease
expresses a temporary maladjustment between human hosts and their environ-
ment. Using examples from his own research in Asia, May demonstrated how
transmission of malaria in North Vietnam and hookworm in China were
affected by specific environmental and cultural patterns. In the North Viet-
namese case, he showed how lowland housing types, which were transplanted
without modification to the highlands, were responsible for the higher rates of
malaria among lowland-to-highland migrant populations, whose ground-level
dwellings exposed them to low-flying mosquito vectors. Native hill peoples,
on the other hand, had adjusted to the malaria threat by constructing stilted
houses with living quarters above the mosquito's 10-foot flight ceiling.
Likewise, in China, May showed how rates of hookworm infection depended
upon the environments within which individuals worked: While rice growers
who worked in fields of mud mixed with nightsoil (raw human feces) were
usually and often seriously infected, silkworm farmers who spent their days
on ladders tending to mulberry leaves were not.
Following May's lead, a number of scholars delineated models of the
interactions among infectious disease agents, human hosts, and the environ-
ment. Audy (10, 11) whose major work focused on the roles of human
behavioral and environmental factors in the transmission of scrub typhus (9),
broadened his approach to disease etiology by incorporating the notion of
"insults" into his model. Insults were defined as physical, chemical, in-
fectious, psychological, or social stimuli that adversely affected an in-
dividual's or population's adjustment to the environment. Audy viewed both
health and disease as states in an individual's dynamic relations with the
environment: Measuring either one depended upon identifying the multiple
positive and negative insults and their cumulative effects. Moreover, expo-
sure to a pathogen was a necessary but not sufficient cause of disease; the
progression from exposure to disease depended in part on the health of the
exposed person, which, given an individual's vulnerability to a complex of
insults, was never a constant.
Audy introduced the concept of insults in an attempt to overcome the
limitations of a pathogen-specific approach to disease. Dunn (68) developed
the even broader concept of "causal assemblages"-complexes of environ-
mental, host-biological, and host-behavioral factors that must be considered
when studying disease etiology or attempting to control disease spread. In his
early work with Malaysian aboriginal groups, Dunn (59, 61) showed how
both environmental factors (e.g. altitude, temperature, soil type, presence of
scavenging animals) and human behavioral factors (e.g. subsistence strat-
egies, housing types, community mobility) significantly affected rates of
parasitic infection. He later demonstrated the important implications of this
model in the design of effective disease control programs (60, 62-64, 66).
In a radical departure that she has labeled the "political ecology of disease,"
Turshen (217) has argued that "bourgeois empiricist" models of disease
causality, such as those described above, are little more than accretions to the
basic epidemiological triad of agent, host, and environment-a model that is
inadequate because it fails to consider the ultimate causes of disease, which
she holds are economic, social, and political. In her own study of infectious
disease and related health problems in Tanzania, Turshen argues that the
continued focus on the former triad is the ultimate cause of scholarly failures
to elucidate why epidemics occur at certain historical moments or why
eradication of a specific infection does not ensure prevention of illness. She
favors a Marxist construction of the causes of poor health, which focuses on
modes and factors of production and changing social relations seen from the
perspective of colonialist and neocolonialist history. This approach has also
been influential in medical geography (131), as well as in the development of
"critical medical anthropology" (211).
Much of the recent empirical work in disease ecology has been, in fact,
political-economic, if not explicitly Marxist in 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 environmental disruptions caused by large-scale, internationally
sponsored projects (123). Dubos (54, 55) was among the first to note that all
technological innovation, whether industrial, agricultural, or medical, upset
the balance of nature; the sensible goal was thus not to maintain the balance of
nature but to change it to the benefit of as many plant and animal species
(including humans) as possible.
Unfortunately, many of the development schemes of the past and present
have been neither balanced nor beneficial. As Hughes & Hunter (123) point
out in their comprehensive review of development projects 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 programs of agricultural, industrial, and in-
frastructural change, as well as resulting population relocations, all un-
dertaken in the name of progress. As they note, development projects 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,
111) notes, schistosomiasis is probably the fastest spreading and most danger-
ous parasitic infection now known. The rapid spread of this disease is almost
entirely due to programs of water resource development involving 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, which are acquired when larval parasites, released in the
water from snail vectors, penetrate immersed human skin. Today, 200-300
million people worldwide are estimated to be infected (134), and new
"epidemics" of the disease occur following the expansion of waterways in
areas of the world where the parasite and vector live. For example, Kloos and
coworkers (140, 141, 144, 145, 147) have described the expanding distribu-
tion of schistosome-transmitting snail populations and escalating rates of
human infection following government-sponsored creation of large, irrigated
farming estates in the Awash Valley 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 dam providing perennial access to a large body
of infective water an increase that was likely to continue, researchers pre-
dicted, given government plans to build more dams in the area (198).
Subtler ecological changes may also be associated with increases in in-
fectious disease. For example, Chapin & Wasserstrom (37) have shown how
increased pesticide use in the intensive production of cotton in both Central
America and India resulted in a serious resurgence of malaria because of the
rapid evolution of insecticide-resistant strains of Anopheles mosquitoes. Sim-
ilarly, the severe epidemic of typhoid fever in Mexico in 1972-73 was the
result of overuse of the powerful antibiotic chloramphenicol for ailments such
as the common cold; this change in disease ecology brought about rapid
selection for chloramphenicol-resistant strains of the typhoid fever bacterium
(218).
SOCIOCULTURAL APPROACHES
infection thought to have killed more people than any other named disease
(159). Genetic adaptations to this disease have merited particular interest, and
malariologists have recognized the important role of human behavior in
malaria control (see the bibliography in 213). Wood (223) summarizes many
of the studies of cultural practices, most of them nondeliberate, that may limit
transmission in areas where malaria is endemic. These include the use of
alkaline laundry soaps that destroy mosquito breeding 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 mosquito vectors. Empirical evidence for the efficacy of such practices
is generally lacking, however. Brown (27) has also argued that the combina-
tion of nucleated settlement pattern and inverse transhumance (flock move-
ment to high elevations in summer) served to reduce exposure to malaria in
Sardinia and to explain its social epidemiological distribution. These and
other traditional behaviors based on the folk theory of miasma probably had
preventive effects. Behavioral adaptations to malaria in other cultural contexts
include fava bean consumption in the Mediterranean (135, 136), traditional
medicines in Nigeria (75, 76), and the use of thick blankets and netting in
Africa (163).
Sexually transmitted diseases (STDs) and labor migration The crucial role
of human behavioral factors in the dissemination of sexually transmitted
diseases (STDs) has been known for 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 consequences of those behaviors has
only been recognized recently. This need has been made more urgent by the
appearance of AIDS during the past decade (13, 81, 97, 127, 176). Prior to
the recognition of AIDS as a widespread problem in sub-Saharan Africa, a
number of behaviorally oriented researchers working in 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: Young men from rural tribal
areas areas plagued by political upheaval, unemployment, rapid moderniza-
tion, and the uneven distribution of economic opportunities migrate to
cities, where they make up the clientele of prostitutes operating from bars,
brothels, dance-halls, and the street. These prostitutes, who face the same
economic pressures 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 STD transmission is
even further increased when men migrate to isolated labor camps and mines
where, characteristically, a small number of prostitutes have sexual relations
RESEARCH NEEDS Although behavioral studies of the kind cited above can
provide useful information on infectious disease transmission, they are never-
theless limited in their utility if they do not proceed beyond the observational
level. As Dunn (62:503) has cautioned in his discussion of schistosomiasis
and water contact, "A further series of studies . . . will be needed in each
situation to specify why people behave as they do, where and when . . . Any
effort to change human behavior must rest on such studies." Dunn's call for
RESEARCH EXAMPLES The need for such information becomes clear in the
literature on ethnomedicine and infectious disease, a number of examples of
which are included here.
ACKNOWLEDGMENTS
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