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Annu. Rev. Anthropol. 1998. 27:247–71
Copyright 1998 by Annual Reviews. All rights reserved
Epidemiologic TransitionRonald Barrett, Christopher W. Kuzawa, Thomas McDade, and
Department of Anthropology, Emory University, Atlanta, Georgia 30322; e-mail:
email@example.com; firstname.lastname@example.org; email@example.com;
KEY WORDS: health transition, history of disease, political ecology, paleopathology,
We use an expanded framework of multiple epidemiologic transitions to re-
view the issues of re/emerging infection. The first epidemiologic transition
was associated with a rise in infectious diseases that accompanied the Neo-
lithic Revolution. The second epidemiologic transition involved the shift
from infectious to chronic disease mortality associated with industrializa-
tion. The recent resurgence of infectious disease mortality marks a third epi-
demiologic transition characterized by newly emerging, re-emerging, and
antibiotic resistant pathogens in the context of an accelerated globalization
of human disease ecologies. These transitions illustrate recurring sociohis-
torical and ecological themes in human–disease relationships from the Pa-
INTRODUCTIONThe problem of emerging infectious disease has recently captured the public’s
imagination and the attention of the scientific community. Popular books (e.g.
Preston 1994) and movies (e.g. Outbreak
, released in 1995) tell grisly tales of
hapless victims bleeding from all orifices, prey to mutating microbes that chal-
lenge the supremacy of Western biomedical progress. A number of books
aimed at an educated general audience chronicle the scientific research effort
to understand these deadly pathogens (Garrett 1994; Rhodes 1997; Ryan 1993;
Ryan 1997). Recent academic conferences (Lederberg et al 1992; Morse 1994)
have brought together researchers in microbiology, public health, and bio-
medicine to survey the seriousness of the problem; they report an ominous re-
surgence of morbidity and mortality from new and old infectious diseases.
These reports warn of the eroding efficacy of antimicrobial therapies in the
face of growing multidrug resistance (Lewis 1994; Swartz 1994; Vareldzis et
al 1994). They note the first rise in infectious disease deaths in affluent post-
industrial nations since the Industrial Revolution: In the US, age-adjusted mor-
tality from infectious disease has increased by 40% from 1980 to 1992 (Pinner
et al 1996). For its part, the US Centers for Disease Control and Prevention
(CDC) has compiled a list of 29 pathogens that have emerged since 1973
(Satcher 1995), and has initiated an online journal—Emerging Infectious Dis-
—to address this growing problem.1
The current spate of attention belies the fact that emerging infections are not
a recent phenomenon but have always played a major role throughout human
history (Armelagos & McArdle 1975; Boyden 1970; Cockburn 1971; Fenner
1970; Lambrecht 1985; Polgar 1964). We seek to contextualize these recent
emerging infectious disease trends within an evolutionary and historical per-
spective, using an expanded framework of epidemiologic transition theory. By
tracing the emergence of disease in the Paleolithic Age, the Neolithic Age, the
Industrial Revolution, and contemporary global society, we argue for the exis-
tence of three distinct epidemiologic transitions, each defined by a unique pat-
tern of disease that is intimately related to modes of subsistence and social
structure. We suggest that current trends—the re/emergence of infectious dis-
ease in the industrialized world and an increasingly globalized disease ecology
(Colwell 1996; Elliot 1993; Gubler 1996; Patz et al 1996)—herald the arrival
of a qualitatively distinct third epidemiologic transition in human health.
Recognizing the complexity of the diverse sociocultural processes involved
in the re/emergence of infectious disease, many researchers in biology, medi-
cine, and public health are calling for input from the social and behavioral sci-
ences (Sommerfeld 1995). With its integrative approach to complex biocul-
tural issues, anthropology is well positioned to make significant theoretical
In the sections that follow, we provide a brief overview of epidemiologic
transition theory and propose an expanded framework to consider the recur-
ring social, political, and ecological factors implicated in emerging disease
1 1Full text articles from CDC’s Emerging Infectious Diseases
and Morbidity and Mortality
can be accessed electronically using the CDC’s Web site at http://www.cdc.gov.
patterns from the late Paleolithic era to the Industrial Revolution. We apply
this broader framework to explain the most recent pattern of emerging disease
as part of a third, qualitatively distinct, epidemiologic transition.
AN OVERVIEW OF EPIDEMIOLOGIC TRANSITIONSThe concept of the epidemiologic transition was first formulated by Omran as
a model for integrating epidemiology with demographic changes in human
populations (Omran 1971). Omran stated that this model “focuses on the com-
plex change in patterns of health and disease and on the interactions between
these patterns and the demographic, economic, and sociological determinants
and consequences.” Omran described the epidemiologic transition as occur-
ring in three successive stages, or “ages”: 1. of pestilence and famine; 2. of re-
ceding pandemics; and 3. of degenerative and man-made diseases. The third
age described the shift in age-specific disease mortality from infectious dis-
eases to chronic degenerative diseases in England and Wales following the In-
dustrial Revolution. Classically associated with the concept of the epidemiol-
ogic transition as a whole, this particular sequence of events represented an im-
portant tradeoff between mortality and morbidity as a result of the interaction
between epidemiological and demographic processes. On one hand, decreased
child and maternal mortality resulting from declining infectious diseases re-
sulted in an overall increase in population size. On the other hand, a subse-
quent increase in life expectancy entailed an aging population with increasing
mortality because of chronic degenerative diseases associated with the latter
Important criticisms have been made concerning this initial framing of the
epidemiologic transition. Akin to assumptions of unilinear evolutionary prog-
ress in early models of cultural evolution, this framework implies that each
stage of the transition is more advanced and desirable than previous stages. Be-
cause epidemiologic transition theory focuses solely upon trends in mortality,
debates surrounding the ramifications of increased longevity for quality of life
and well-being are not addressed by the model. It has been argued that the in-
crease in life expectancy associated with the shift from acute infectious to
chronic disease may be gained at the expense of increased total suffering and
ill-health (Johansson 1992; Riley 1992; Riley & Alter 1989). However, others
contend that populations undergoing the epidemiologic transition may eventu-
ally experience a delay in the age of onset of chronic disabilities and disease
(Fries 1980; Olshansky & Ault 1986).
Second, although this framework emphasizes socioeconomic and ecologi-
cal factors as chief determinants in disease mortality transition, the use of
whole nations as units of analysis has been criticized for burying the differen-
tial experience of these events according to race, gender, and class within
population statistics (Gaylin & Kates 1997). A parallel criticism has been
made of “emerging infectious diseases,” a classification which may not signify
the emergence of new pathogens as much as a re-emerging awareness among
affluent societies of old problems that never went away (Farmer 1996). These
critiques underscore the need to expand this model to account for the heteroge-
neity of disease experience within populations undergoing epidemiologic tran-
While Omran accounted for accelerated, delayed, and transitional variants
of his “classical” model of epidemiologic transition in Europe and North
America (Omran 1971, 1983), more recent modifications have improved its
applicability to a broader array of contexts and issues. Bobadilla and col-
leagues adapted the model to fit observations in “middle income” nations such
as Mexico, where trends in chronic disease have increased despite a persis-
tence of infectious disease morbidity and mortality, resulting in what they de-
scribe as an overlap of eras (Bobadilla et al 1993). Popkin suggests that some
chronic conditions have entered a refractory stage in populations such as in the
United States, where individuals have changed their diet and lifestyle in an ef-
fort to prolong a healthy lifespan (Popkin 1994). This is akin to an additional
stage of the epidemiologic transition proposed to explain the delayed onset of
the symptoms and ill-health associated with chronic conditions in some indus-
trial nations (Olshansky & Ault 1986).
Even with these modifications, however, the epidemiologic transition is re-
stricted to a particular set of historical circumstances in the recent shift from
infectious to chronic disease mortality. Yet, by further expanding this frame-
work to include multiple transitions from the Paleolithic Age to the present
day, we are able to illustrate how recurring sociohistorical and ecological
themes have had an important influence on shifting disease patterns through-
out modern human evolution. In this manner, we have reset the baseline for
three distinct epidemiologic transitions to the conditions that existed just prior
to the widespread changes that occurred with the adoption of agriculture in hu-
PALEOLITHIC AGE TO THE INDUSTRIAL REVOLUTIONPaleolithic Age Baseline
During much of our evolutionary history, hominid ancestors of modern hu-
mans roamed the African savanna as small, nomadic bands of foragers. Early
hominid populations likely were too small and dispersed to support many of
the acute communicable pathogens common in densely populated sedentary
communities (Burnet 1962), especially those for which human populations are
the only disease pool (Cockburn 1971; Polgar 1964). Acute upper respiratory
infections decline soon after being introduced to isolated communities, sug-
gesting that they would have been absent from the dispersed populations of the
Paleolithic era (Popkin 1994). Similarly, pathogens such as smallpox, measles,
and mumps were unlikely to afflict early hominid groups (Cockburn 1967a).
Hominid social organization and demographics would have presented less
of a barrier to the transmission and perpetuation of pathogens with long peri-
ods of latency or low virulence. Viruses such as chickenpox and herpes sim-
plex may survive in isolated family units, suggesting that they could have been
sustained in early dispersed and nomadic population. The current distribution
of parasite species common to human and nonhuman primates provides evi-
dence for longstanding hominid-parasite relationships that predate the diver-
gence of the hominid lineage (Cockburn 1967b; Kliks 1983). Sprent (1969b)
coined the apt term “heirloom species” to describe such parasites, which he
distinguished from the “souvenir” parasites contracted through chance en-
counters with infected nonhuman hosts or vectors.
Long-term coevolutionary relationships between hominids and a heirloom
parasite imply a good match between the parasite’s mode of transmission,
virulence, and lifecycle, and the lifestyle and demographics of early foraging
bands (Sprent 1962, 1969a). As one example, the gregarious behavior, nesting
habits, and frequency of hand-to-mouth contact typical of hominoid primates
likely favored the persistence of the pinworm Enterobius vermicularis
hominid evolution, which continues to inflict contemporary human popula-
tions (Kliks 1983). Similarly, ectoparasites such as head and body lice (Pedi-
) and enteric pathogens such as Salmonella
would likely have
infested early hominids (Cockburn 1971; Polgar 1964).
Hominids would have contracted novel, or souvenir, parasites in their daily
rounds of collecting, preparing, and eating raw plants, insects, meat, and fish
(Audy 1958; Bennett & Begon 1997). The distribution and characteristics of
these pathogens would have placed constraints on the ecosystems open to
hominid exploitation. Lambrecht contends that the trypanosomiasis parasite
carried by the tsetse fly opened ecological niches for hominid exploitation by
eliminating trypanosome-susceptible fauna (Lambrecht 1980). Because mod-
ern humans are trypanosome-susceptible and thus have not developed genetic
resistance to the disease, Lambrecht argues that early hominids must have
adapted culturally and behaviorally to tsetse by residing in fly-free areas, and
perhaps through the advent and use of fire. Similarly, Kliks argues that particu-
larly problematic and ubiquitous helminths, such as those associated with
schistosomiasis and onchocerciasis, may have limited access to productive
niches, much as they do throughout large tracts of Africa today (Kliks 1983).
The distinction between the heirloom and souvenir parasites afflicting early
hominid bands underscores the antiquity of disease “emergence” in human
populations, which is as old as the hominid lineage itself (Sprent 1969a,b).
Then as today, the environment provided the pool of potential emerging infec-
tions or parasites, and the social, demographic, and behavioral characteristics
of hominid adaptation provided the opportunity for disease emergence. The
rate of emergence may have increased as tool use allowed exploitation of novel
ecological niches (Kliks 1983), and as ecological zones shifted with climate
change during glacial and interglacial periods (Lambrecht 1980). The eventual
movement of hominid populations out of Africa into Europe, Asia, and beyond
would have exposed migrating bands to novel ecologies and parasites, increas-
ing the rate of emergence at least temporarily in such groups. However, it is
likely that disease ecologies in these new habitats would have remained quali-
tatively similar, owing to the continuation of a nomadic foraging adaptation
and low population densities.The First Epidemiologic Transition
Beginning about 10,000 years ago, a major shift occurred in most human popu-
lations, from a nomadic hunting and gathering lifestyle to sedentism and pri-
mary food production. This shift involved major changes in human social or-
ganization, diet, demographics, and behavior that created conditions favorable
for zoonotic infections to make the transition to human hosts, and for pre-
existing human pathogens to evolve to more virulent forms. We describe the
subsequent increase in infectious disease mortality that arose in the context of
these changes as the first epidemiologic transition.
The shift to permanent settlements created larger aggregates of potential
human hosts while increasing the frequency of interpersonal contact within
and between communities, likely fostering the spread and evolution of more
acute infections (Ewald 1994). In addition, accumulation of human waste
would have created optimal conditions for dispersal of macroparasites and
gastrointestinal infections. Skeletal remains from archaeological sequences
spanning this cultural transition generally show an increase in the prevalence
of infectious lesions as populations shifted from foraging to sedentism and
food production (Cohen & Armelagos 1984), adding empirical support to
The appearance of domesticated animals such as goats, sheep, cattle, pigs,
and fowl provided a novel reservoir for zoonoses (Cockburn 1971). Tubercu-
losis, anthrax, Q fever, and brucellosis could have been readily transmitted
through the products of domesticated animals such as milk, hair, and skin, as
well as increased ambient dust (Polgar 1964). In these contexts, it should not
be surprising that many contemporary human infections have their origins in
the zoonoses of domesticated animals (Bennett & Begon 1997).
Agricultural practices increased contact with nonvector parasites such as
schistosomal cercariae, contracted in irrigation work, and intestinal flukes,
which were acquired through use of feces as fertilizer (Cockburn 1971). With
the advent of food storage, the threat of contamination and wide-scale out-
breaks of food poisoning increased (Brothwell 1972). Breaking the sod during
cultivation may expose workers to insect bites and diseases such as scrub ty-
phus (Audy 1961). Other vectors developed dependent relationships with hu-
man habitats, as in the case of the yellow and dengue fever-carrying mosquito,
, which breeds preferentially in artificial containers (Thompson
& O’Leary 1997; Whiteford 1997).
Reliance upon staple crops and a decline in dietary diversity may have pre-
disposed Neolithic populations to nutritional problems similar to those experi-
enced by subsistence-level agrarian communities in developing nations today
(Harrison & Waterlow 1990). Most staple crops are efficient producers of
calories capable of supporting more dense populations yet often lack critical
micro- or macronutrients. Nutrient deficiencies are thus common in agrarian
societies and are often exacerbated during periods of seasonal hunger or peri-
odic droughts (Chambers et al 1981). Skeletal evidence suggests that such nu-
tritional problems were typical in early agrarian communities and increased
with agricultural intensification in some areas (Cohen & Armelagos 1984),
and may have contributed to a more vulnerable host population.
Skeletal analyses demonstrate that women, children, and—with develop-
ment of stratified societies—the lower classes suffered disproportionately
from the first epidemiologic transition. Female remains among Neolithic
populations indicate higher frequencies of bone loss and nutritional anemia
(Martin & Armelagos 1979). Comparisons between agricultural populations
and their foraging predecessors show greater mortality, dental defects, and im-
paired bone growth among infants and young children for populations in tran-
sition (Cohen & Armelagos 1984). Artifacts indicating social status differ-
ences correlate positively with nutrition and bone-growth among Lower Illi-
nois Valley males during the Middle Woodland Period, emphasizing the role
of early social stratification in the differential experience of disease (Buikstra
1984). Related issues of political organization also had health implications, as
in the case of Nubian populations during the Neolithic period, in which life ex-
pectancies were inversely related to the degree of political centralization (Van-
The severity of disease outbreaks during the first epidemiologic transition
intensified as regional populations increased and aggregated into urban cen-
ters. The crowded, unsanitary living conditions and poor nutrition characteris-
tic of life in these early cities fostered rapid and devastating regional epidemics
(Flinn 1974; McNeill 1976; McNeill 1978). The establishment of large cities
increased problems of supplying clean water and removing human waste,
while facilitating spread of more virulent pathogens in enclosed and densely
crowded habitations (McNeill 1976; Risse 1988). Cholera contaminated water
supplies, epidemics of vector-borne disease such as plague and typhus devas-
tated populations, and outbreaks of measles, mumps, smallpox, and other viral
infections were increasingly common (Knapp 1989). Unlike the infectious dis-
ease mortality common in early Neolithic populations, adults were frequently
the target of epidemic outbreaks, paralyzing societies economically in their
wake. As a dramatic example, tuberculosis routinely killed one third of all
adults in many European communities, and by the end of the nineteenth cen-
tury had claimed an estimated 350 million lives (Knapp 1989). Similarly, the
Black Death of the 1300s is estimated to have eliminated at least a quarter of
the European population in a decade (Laird 1989).
McNeill (1976) also discusses two important historical trends that initiated
the global spread of pathogens across previously intractable geographic
boundaries. First, increasing migration and trade between state-level societies
in Eurasia led to the convergence of regional infectious disease pools begin-
ning in the fifth century CE. Second, expansion of these networks into the New
World through exploration and conquest brought European populations with
acquired immunity to childhood infections into contact with Native Americans
with no history of exposure to these pathogens (Black 1990). This contact re-
sulted in massive pandemics of smallpox and typhoid that killed millions of
people and facilitated the colonial domination of two continents (McNeill
1976, Dobyns 1993). It also probably resulted in the introduction of trepone-
mal infections to Europe (Baker & Armelagos 1988), where sexual promiscu-
ity in crowded urban centers may have favored a venereal mode of transmis-
sion in the form of syphilis (Hudson 1965). These historical events illustrate
how the globalization of state-level societies has provided opportunities for
pathogens to cross considerable social and geographic boundaries.The Second Epidemiologic Transition
The second epidemiologic transition roughly coincided with the Industrial
Revolution in mid-nineteenth century Europe and North America. It is distin-
guished by a marked decline in infectious disease mortality within developed
countries. This decline is the major focus of the second proposition in Omran’s
model of epidemiologic transition: “a long-term shift in mortality and disease
patterns whereby pandemics of infection are gradually displaced by degenera-
tive and manmade disease as the chief form of morbidity and primary cause of
The decline of infectious diseases in the nineteenth and twentieth centuries
has often been cited as an objective landmark in the progress of modern civili-
zation—a product of developments in medical science and technology in the
industrialized world that would eventually diffuse to less-developed societies.
Garrett shows how early successes in the eradication of polio and smallpox in-
fluenced western medical establishments in their confident forecast for the
eminent demise of infectious diseases before the end of this century (Garrett
1994). However, these projections did not consider that the larger secular trend
of declining infectious disease mortality was already well under way before
the advent and application of antimicrobial technologies (McKeown 1976).
Based largely upon data from Scandinavia, Germany, France, Italy, and
England, Schofield & Reher roughly estimated the decline in European infec-
tious disease mortality to have occurred in three major phases beginning in the
late seventeenth century (Schofield & Reher 1991). The first phase, lasting
from the late seventeenth century to the beginning of the nineteenth century, is
characterized by a flattening of crisis mortality peaks owing to sporadic epi-
demics of diseases such as plague, smallpox, and typhus. Beginning in the
mid-nineteenth century, the second phase was characterized by an overall
secular decline in mortality that, although subject to significant regional varia-
tion, contributed to an increased life expectancy by more than three decades,
resulting in a major overall population increase despite concurrent fertility de-
clines. The third phase began with the advent of antimicrobial therapies in the
1940s, representing a more modest decline in infectious disease mortality in
more affluent nations that continued until the early 1980s.
McKeown argued for the primacy of nutritional factors in declining Euro-
pean mortality (McKeown 1976). However, McKeown has been criticized for
weighing nutritional inferences beyond the resolution of available data
(Schofield & Reher 1991; Johansson 1992). While evidence suggests that the
creation of an international grain market may have spurred improved agricul-
tural yields and distribution networks, the relative importance of other factors
such as pasteurization, public hygiene, and home-based primary health care
deserve further evaluation (Kunitz 1991; Woods 1991). Moreover, there is lit-
tle disagreement that certain biomedical innovations such as the worldwide
vaccination campaigns against smallpox played a significant role in mortality
The decrease in infectious disease in industrialized nations and the subse-
quent reduction in infant mortality has had unforeseen consequences for hu-
man health. Namely, the subsequent extension of life expectancy has also
brought increased morbidity from chronic diseases (Riley & Alter 1989).
These so-called “diseases of civilization” include cancer, diabetes, coronary
artery disease, and the chronic obstructive pulmonary diseases (Kaplan & Keil
1993). Other health tradeoffs of the second transition concern the role of indus-
trial technology in the creation of artificial environments that have influenced
the appearance of chronic diseases. Particularly in urban environments, in-
creasing water and air pollution subsequent to industrialization has been
linked to significantly higher rates of cancer (Anwar 1994; Dietz et al 1995),
allergies (Barnes et al 1998), birth defects (Palmer 1994), and impeded mental
development (Perrera 1993). These issues are compounded by the psychoso-
matic effects of urbanization, which is correlated with increased levels and in-
cidences of hypertension (Grossman & Rosenthal 1993), as well as depression
As in the cases of the Paleolithic-era baseline and the first epidemiologic
transition, social inequalities account for many of the differences in the way
the second transition has been experienced within and between populations.
Within more industrialized societies, socioeconomic, ethnic, and gender dif-
ferences are strongly associated with differences in morbidity and mortality
for both chronic and infectious diseases (Arriaga 1989; Blair 1993; Dressler
1993). Buried within national statistics, and temporarily masked by antibiot-
ics, the conditions selected for the first transition persisted among the poorest
people of the richest nations in the second.
Following the Second World War, the second epidemiologic transition
made a more modest appearance in many less-developed nations and was
marked by improvements in child survival and life expectancy at birth (World
Bank 1993). Unlike the epidemiologic transitions experienced in the United
States and Europe, which largely proceeded the advent of modern biomedical
innovation, biomedical fixes such as oral rehydration therapy, immunizations,
and antibiotics played a pivotal role in the initial successes in mortality reduc-
tion in these societies (Gwatkin 1980; Hill & Pebley 1989; Ruzicka & Kane
1990). While variability of these declines between countries and their possible
deceleration since the 1960s has been a source of controversy (Gwatkin 1980;
United Nations 1982), there is little doubt that the second transition has fallen
short of optimistic projections for the developing world (Gobalet 1989). Rapid
urbanization combined with marked social inequalities and a continued lack of
public health infrastructure have led to communicable diseases among the ur-
ban poor, with chronic degenerative diseases among the affluent and slowly
emerging middle classes (Muktatkar 1995). In middle-income countries such
as Mexico and Brazil, socioeconomic status now relates inversely to important
chronic disease risk markers like obesity and hypertension (Popkin 1994), akin
to similar associations in the United States, the United Kingdom, and other af-
fluent nations (Kaplan & Keil 1993).
THE THIRD EPIDEMIOLOGIC TRANSITIONThe current phenomenon of emerging infectious diseases indicates a third epi-
demiologic transition characterized by three major trends. First, an unprece-
dented number of new diseases have been detected over the last 25 years that
are becoming significant contributors to adult mortality. Second, there is an in-
creased incidence and prevalence of preexisting infectious diseases that were
previously thought to have been under better control. Third, many of these re-
emerging pathogens are generating antimicrobial-resistant strains at a faster
rate than safe new drugs can be developed. These three trends are occurring
within the broader context of an increasing globalization, involving not only
international trade, migration, and information networks, but also the conver-
gence of human disease ecologies.Recently Emerging Infections
The Centers for Disease Control and Prevention (CDC) has compiled a list of
29 newly emerging pathogens since 1973 (Satcher 1995). It is possible that the
overall size of this list is more a function of increased detection than the actual
emergence of new pathogens in human populations. Such is the case of the Le-
bacterium responsible for the high-mortality pneumonia known as
Legionnaire’s Disease. Following its initial detection during a 1976 outbreak
in a convention of American World War II veterans (Fraser et al 1977), envi-
ronmental and retrospective patient cultures subsequently indicated that Le-
had long been responsible for 2000 to 6000 deaths previously diag-
nosed as pneumonias of unknown etiology (McDade et al 1977), many of
which were attributed to the exposure of susceptible elderly hosts to contami-
nated large-scale air conditioning units (Miller 1979; Morris et al 1979; Sara-
Despite possible increases in detection rates, it cannot be denied that at least
some of these new diseases are making unprecedented contributions to adult
mortality. The most dramatic example of this is the Human Immunodeficiency
Virus (HIV). Although retrospective studies have detected cases in Europe and
Africa going back as far as 1959 (Huminer et al 1987; Nahmias et al 1986),
HIV has more recently become the second leading cause of death among adult
males aged 25–40 years of age in the United States, and the chief contributor to
a 40% increase in infectious disease mortality over the past 15 years (Pinner et
al 1996). With the exception of the flu pandemic of 1918, this trend marks the
first of such increases in affluent societies since the Industrial Revolution.
Phylogenetic analyses of HIV and related retroviruses indicate a recent
evolution from a simian virus of Central African origin (Essex & Kanki 1988).
Yet biological evolution alone does not account for the rampant spread of this
disease, nor its unequal distribution within and between populations (Ewald
1994; Feldman 1990; MacQueen 1994). Throughout Asia, Africa, and the
Americas, high HIV and sexually transmitted disease (STD) prevalence rates
have been indices of deeper sociohistorical issues such as neocolonialism
(Alubo 1990), the disintegration of poor families because of seasonal labor mi-
grations (Hunt 1995), sexual decision-making strategies (Bolton 1992; Wad-
dell 1996), and the gendered experience of poverty (Connors 1996; Daily et al
1996; Farmer et al 1993; MacQueen et al 1996; McCoy et al 1996). Yet, nei-
ther is this simply a case of the poor transmitting their problems to the affluent.
For example, contrary to the myth of Haitian origin following the initial dis-
covery of AIDS, evidence suggests an earlier transmission to urban Haiti by
more affluent Westerners engaging in sex tourism (Farmer 1992).
The social history of AIDS provides a prototype for similar issues sur-
rounding the transmission of other infectious diseases. Outbreaks of Ebola
hemorrhagic fever have received much attention in the popular press, which
has mainly focused on the gory aspects of its clinical manifestations, high mor-
tality rates, and fears of airborne transmission accentuated with images of “vi-
rus hunters” running around in spacesuits (Preston 1994). Contrary to these
dramatized accounts, however, the instances of possible airborne transmission
was restricted to very close contact between unprotected healthcare workers
and patients in the late stages of this disease (Garrett 1994). The Ebola out-
breaks along Kinshasa Highway of Central and Eastern Africa in the 1970s
mainly involved transmission via the commercial sex trade and the reuse of
dirty syringes by untrained Western missionaries and underequipped health-
care workers (Garrett 1994). Regarding fears of transmission across national
borders, the appearance of the closely related filoviruses detected in Reston,
Virginia, and Marburg, Germany, were caused by the importation of primates
for drug research, which ironically included the development of vaccines for
other viruses (Bonin 1971; Morse 1993, 1995).
Ebola and Marburg are but two examples of a much larger set of recently
discovered hemorrhagic diseases. Recent outbreaks of these diseases in the
New World have been linked to climatic fluctuations and ecological disrup-
tion. In 1993, a sudden outbreak of a virulent hemorrhagic fever in the Four
Corners region of the American Southwest was quickly identified as a novel
strain of hantavirus spread through the excreta of the deer mouse, Peromyscus
, but not before infecting 98 individuals in 21 states and claiming
51 lives (Weigler 1995). The 1993 outbreak was associated with abnormal
weather patterns (Epstein 1995), and oral histories of local American Indian
healers describe three clusters of similar outbreaks that coincide with identifi-
able ecological markers (Chapman & Khabbaz 1994), supporting the idea that
this disease has long coexisted with and periodically afflicted human popula-
tions across the United States without detection by the medical community
(Weigler 1995). The initial outbreaks of Argentinian hemorrhagic fever, or Ju-
nin, were traced to ecological disruption associated with the spread of maize
agriculture and increasing rodent vector habitats (Benenson 1995).
First identified in the mid 1970s, tick-borne Lyme disease has since sur-
faced in all 50 states as well as overseas (Jaenson 1991), and has rapidly be-
come the most often reported anthropod-born disease in the United States (Ol-
iver 1996). Regrowth of Eastern forests felled in the eighteenth and nineteenth
centuries to make way for agricultural fields has greatly expanded the habitat
of deer, mice, and their Ixodes
tick parasites, which carry the disease-causing
spirochete (Walker et al 1996). Residential housing has expanded
into forested areas, bringing populations into contact with the ticks and their
wild-animal reservoirs. As exemplified by diseases as distinct as HIV, Ebola
virus, and Lyme disease, pathogens are often provided the opportunity to jump
the “species barrier” (Lappe 1994) by a combination of ecological disruption
or change, and increased contact between humans and wild reservoir species.
The size and mobility of human populations increases the potential for the
pathogen to escape its geographic barrier (Armelagos 1998).
RE-EMERGING INFECTIONS Ecological disruption has also been cited as a ma-
jor factor in re-emerging infectious diseases as well. Warmer climates have led
to increased coastal blooms of algae, creating favorable environments for the
proliferation of Vibrio cholerae
, and inland changes in temperature and hu-
midity are increasing the reproduction of malaria vectors (Martens et al 1995;
Patz et al 1996). In addition, climactic fluctuations such as El Niño are thought
to have significant effects on pathogen and disease vector environments
(Bouma & Dye 1997; Colwell 1996).
While acts of nature may account for changing disease patterns, most of
these ecological changes have anthropogenic origins (Brown 1996; Coluzzi
1994; de Zulueta 1994). In the last 15 years, dengue fever has shown a dra-
matic resurgence in Asia and Latin America, where poorly developed urban
environments have led to the proliferation of the Aedes egypti
tors in open water pools (Chinery 1995; Whiteford 1997), contributing as well
to sporadic outbreaks in the Southwestern United States (Gubler & Clark
1995). The practice of combined swine-duck agriculture in Southern China as
well as commercial swine and turkey farming in the United States is thought to
contribute to the genetic adaptability of flu viruses (Shortridge 1992; Shu et al
1994; Wright et al 1992). Bradley critically reviewed the practice of “third-
world dumping” by multinational corporations, in which industrial production
facilities are “outsourced” into developing countries with cheap labor pools
and greatly relaxed environmental regulations, resulting in localized climate
changes (Bradley 1993a,b). Increases in mosquito populations have com-
pounded the problem of malaria and dengue in places where poor living condi-
tions and the unequal distribution of health resources have already contributed
to higher levels of preventable mortality (Brown et al 1996; Gubler & Clark
Among the re-emerging infectious diseases, tuberculosis (TB) is the great-
est contributor to human mortality, and it is estimated that nearly a third of the
world’s population has been latently infected with the mycobacterium (Malin
et al 1995). After more than a century of steady decline, the incidence of re-
ported TB cases in the United States increased by more than 20% from 1985 to
1992. This trend is particularly unsettling given that the previous decline of TB
was the single largest contributor to North American and European declines in
infectious disease mortality during the middle stages of the second epidemiol-
ogic transition (Caselli 1991; Puranen 1991).
The resurgence of tuberculosis in affluent nations was preceded by de-
creased public health expenditures, becoming a forgotten disease in the con-
text of overly optimistic predictions for its continued decline (Ryan 1993). Yet
TB has remained the leading cause of infectious disease mortality in develop-
ing countries, where 95% of all cases occur (Raviglione et al 1995). Notori-
ously endemic to populations living under conditions of malnutrition, poor
sanitation, and inadequate housing, tuberculosis has long been considered to
be the classic disease of poverty (Darbyshire 1996). While HIV comorbidity is
implicated in the most recent first world resurgence of TB, especially among
young adults, higher rates of both diseases among the urban homeless indicate
that socioeconomic issues play much the same etiological role in the re/emer-
gence of infectious diseases today as they have in centuries past (Barclay et al
1995; Barnes et al 1996; Farmer 1997; Zolopa 1994).
ANTIMICROBIAL RESISTANCE The history of antimicrobial resistance is al-
most as long—or rather, as short—as the widespread use of the drugs them-
selves. The first recorded instance of drug resistance occurred in 1917 during
the initial trials of Optochine in the treatment of pneumococcal pneumonia
(Moellering 1995; Moore 1917). Three years after the 1941 introduction of
penicillin for clinical use against gram-positive “staph” infections,2 new
strains of Staphylococcus aureus
began to emerge with penicillin-destroying
beta lactamase enzymes (Neu 1992). The lessons of emerging resistance were
well known even before the DDT fumigation campaigns to eradicate malaria-
mosquitoes, in which warnings of impending insecticide
susceptibility accompanied strong recommendations for a single major inter-
national campaign (Brown 1996; Olliaro et al 1996; Roberts & Andre 1994).
These unheeded warnings would prove correct, not only for the vectors, but for
the quinine and chloroquine-resistant plasmodium parasite itself (de Zulueta
1994; Longworth 1995; Roberts & Andre 1994).
At present, more than 95% of S. aureus
strains are resistant to most forms of
penicillin, and strains resistant to methycilline (MRSA) have become endemic
to US nursing homes and acute-care settings around the world (Jacoby 1996).
Last year, the first strains of S. aureus
possessing intermediate resistance to
vancomycin were identified in Japan and the United States (Centers for Dis-
ease Control 1997), joining the ranks of already emerging Enteroccoci
full resistance to this antibiotic (Nicoletti & Stefani 1995; Rice & Shlaes 1995;
2 2Although Alexander Fleming first identified a staphylocidal substance in Penicillium notatum
molds in 1928, the actual development and distribution of penicillin for clinical use took another 13
Swartz 1994). In many cases, vancomycin represents the last in the line of
“magic bullet” defenses against these kinds of pathogens (Gruneberg & Wil-
son 1994; Nicoletti & Stefani 1995; Rice & Shlaes 1995). As such, the emer-
gence of vancomycin-resistant pathogens hails the beginning of what has been
called “The Post-Antimicrobial Era” (Cohen 1992).
In many ways, biological evolution provides the ultimate critique of bio-
medicine by demonstrating the inevitability of genetic adaptations of microor-
ganisms to the selective conditions posed by human technology and behaviors
(Lederberg 1997). Beyond this, however, predictions of specific resistance
patterns have been problematic. Streptococcus pneumoniae
provides a good
example of this problem. Long since ranked among the pneumonias known as
“the old man’s friend” in affluent nations (Garrett 1994), S. pneumoniae
also been the microbial source of more than 1,000,000 annual deaths of chil-
dren under five years of age (Obaro et al 1996). In the last five years, drug-re-
sistant strains of this bacteria have emerged worldwide (Gerber 1995; Gold-
stein & Garau 1994; Jernigan et al 1996), with reported frequencies as high as
50% among clinical isolates (Obaro et al 1996). Yet there is no theoretical ex-
planation for why it took more than 40 years for this organism to develop anti-
biotic resistance, while other drug-resistant species emerged in less than a dec-
Bartlett & Froggatt outline three general themes in the emergence of anti-
microbial resistance: 1. that high-grade resistant organisms are typically fore-
shadowed by low-grade resistant intermediates; 2. that resistant strains are
typically resistant to more than one antibiotic; and not surprisingly, 3. that re-
sistance develops under conditions of extensive antibiotic use (Bartlett &
Froggatt 1995). The overuse of antibiotics by both trained and untrained health
providers throughout the world is a major factor in the evolution of
antimicrobial-resistant pathogens (Kollef 1994; Kunin 1993; Kunin et al
Besides the practices of health providers, the patients themselves have cre-
ated selective conditions for antimicrobial resistance by early termination of
prescribed courses of antibiotics, providing additional generation time for
partly reduced organism populations within the host (Appelbaum 1994). This
is especially problematic for diseases such as tuberculosis, which requires up
to a year of medication adherence in the absence of detectable symptoms to
completely eliminate the mycobacterium (Barnes & Barrows 1993). Acquired
resistance owing to incomplete adherence to TB regimens is partly responsible
for the emergence of multi-drug–resistant tuberculosis (MDRTB) (Jacobs
1994; Nunn & Felten 1994)—a situation compounded by issues of access and
conflicting explanatory models between patients and healthcare providers
(Dedeoglu 1990; Menegoni 1996; Rubel & Garro 1992; Sumartojo 1993; Vec-
Host susceptibility is another major factor in the evolution of antimicrobial-
resistant pathogens (Morris & Potter 1997). The large majority of MDRTB
outbreaks in the United States occurred in the context of comorbidity among
HIV-infected patients (Crawford 1994; Zolopa 1994). Multi-drug resistant no-
socomial infections are predominantly found among elderly and immunocom-
promised patients in long-term and acute-care hospital settings (Hayden &
Hay 1992; Koll & Brown 1993; Kollef 1994; Rho & Yoshikawa 1995; Schen-
tag 1995; Toltzis & Blumer 1995). The emergence of the eighth cholera pan-
demic, involving the drug-resistant 0139 Bengal strain, has been found among
populations of refugees and the poorest inhabitants of the fourth world already
susceptible to the effects of unsanitary water sources (Martin et al 1994; Sid-
dique et al 1995; Islam et al 1995; Toole 1995; Weber et al 1994).
The overuse of antiobiotics in industrial animal husbandry also contributes
to the rise of multi-drug resistant strains of food-borne pathogens (Tauxe
1997). Nontyphoid strains of Salmonella
have been on the rise in the United
States since the Second World War, where it is currently the most common
food-borne infection. Overuse of antibiotics in chickens has contributed to the
emergence of Salmonella
strains resistant to all known drug therapies. These
were recently identified in British travelers returning from the Indian subconti-
nent (Rowe et al 1997). In Europe, the emergence of strains of Campylobacter
resistant to enrofloxacin increased in parallel to the use of this antibiotic
among poultry (Endtz et al 1991). Similarly, the use of avoparicin as a growth-
promoter in European livestock is believed to have created selective condi-
tions for the emergence of vancomycin-resistant enterococci (VRE), which are
transmitted to human hosts through fecal-contaminated animal products
While antibiotics have played a relatively minor role in the latter stage of
the second epidemiologic transition, the erosion of these human cultural adap-
tations in the face of more rapid genetic adaptations of microorganisms forces
us to confront major issues without the aid of technological crutches. We will
discover to what degree these magic bullets may have subsequently obscured
the relative efficacy of primary prevention in both affluent and underdevel-
INFLUENZA AND THE GLOBALIZATION OF HUMAN DISEASE ECOLOGIES Had
the historical precedents of influenza been given closer consideration, pre-
vious projections for the continued decline in infectious diseases might not
have been so optimistic. With an estimated worldwide mortality of over
20,000,000, the Spanish influenza pandemic of 1918–1919 killed more human
beings than any previous war or epidemic in recorded history (Crosby 1989).
This was followed by the less-virulent pandemics of 1957, 1968, and 1977
(Wiselka 1994), each bringing the millenialist promise of another major out-
break at some unknown year to come (Glezen 1996; Webster et al 1993).
Noting the rapidity with which the Spanish Flu spread throughout the world
in the days of steamships and isolationism, Garrett grimly suggested how such
an outbreak could spread in the present age of international economics and jet
travel (Garrett 1994), a timely subject given the recent appearance of a poten-
tially lethal influenza strain in Hong Kong poultry markets with H5 antigens,
to which humans have no known history of previous exposure (Cohen 1997;
Shortridge 1995). With revolutionary changes in transportation technology
(Reid & Cossar 1993; Wilson 1996), worldwide urbanization (Muktatkar
1995; Phillips 1993), and the increasing permeability of geopolitical bounda-
ries (Farmer 1996), human populations are rapidly converging into a single
global disease ecology (McNeill 1976).
McNeill (1976) cites the early effects of transnationalism on the transmis-
sion of infectious diseases with the establishment of extensive Eurasian trade
networks in the fifth century CE. Intercontinental shipping routes provided for
the transport of pathogens as well as trade goods and organized violence. The
European conquests of the new World presented a dramatic example of this
trend, in which adult carriers of childhood diseases endemic to post-first tran-
sition populations suddenly infected unexposed Native American populations,
resulting in massive pandemics of smallpox and typhus. Neither was this a
one-way trade, as returning sailors brought syphilis and tobacco back to the
The current trend of accelerated globalization challenges us to consider the
health implications not just of converging microbial ecologies, but also of the
international flow of ideologies, behavior patterns, and commodities that un-
derlie human disease patterns. This broader picture of globalization, involving
the international exchange of memes
(units of cultural information) as well as
microbes, entails a convergence of both chronic and infectious disease pat-
terns. This is evidenced in the many developing societies that are suffering
what has been called the “worst of both worlds”—the postwar rise in chronic
degenerative diseases among the poor without significant declines in infec-
tious disease mortality (Bradley 1993a), while these infections re-emerge in
post-second transition societies (Armelagos et al 1996).
Buoyed by early successes in the control of scourges such as polio and small-
pox in the 1950s and 1960s, the Western medical establishment claimed that it
was time to close the book on infectious diseases and focus research attention
on the growing problem of chronic degenerative disease (Garrett 1993). Un-
fortunately, the book on infectious disease remains very much open, and new
chapters continue to be added at an alarming pace. We address this issue from
an evolutionary perspective, using the concept of epidemiologic transition the-
ory as an organizing framework. Our discussion of epidemiologic transitions
during the course of human evolution reveals that disease “emergence” is not
new but has been a dynamic feature of the interrelationships between humans
and their sociocultural and ecological environments since the Paleolithic peri-
od.The initial formulations of the epidemiologic transition provided a useful
interdisciplinary framework for macrolevel analyses of demographic changes
associated with major declines in infectious disease mortality in Europe and
North America in the wake of the Industrial Revolution (Omran 1971). De-
spite later modifications, however, interpretations of this framework still re-
mained largely restricted to a single set of events at a particular period of hu-
man history (Omran 1983). The subsequent particularism of this transition
fueled notions of unilinear progress, resulting in falsely optimistic projections
for the continued decline and eventual elimination of infectious disease in hu-
man populations (Garrett 1994). Our expanded framework of multiple epide-
miological transitions avoids these pitfalls by providing a broader historical
and evolutionary perspective that highlights common themes that pervade
changing human-disease relationships throughout modern human evolution.
In our review of epidemiologic transitions, we have highlighted the socioe-
cological, technological, and political factors involved in human disease dy-
namics. The US Institute of Medicine has identified six principal factors con-
tributing to the current problem of re/emerging infectious diseases: 1. ecologi-
cal changes; 2. human demographics and behavior; 3. international travel and
commerce; 4. technology and industry; 5. microbial adaptation and change;
and 6. breakdown in public health measures (Lederberg et al 1992; Morse
1995). The degree to which these factors are fundamentally anthropogenic
cannot be overstated, nor can the influence of socioeconomic inequalities
Recognizing the complexity of these sociobehavioral dynamics, many re-
searchers in biology, medicine, and public health are calling for greater in-
volvement of social and behavioral scientists in addressing infectious disease
issues (Morse 1995; Satcher 1995; Sommerfeld 1995). By taking a holistic ap-
proach to these important human issues, anthropologists are well positioned to
make significant theoretical and practical contributions within interdiscipli-
nary research settings. For example, 40 years ago, Livingstone described the
emergence of malaria following the introduction of agriculture in sub-Saharan
Africa in what has become a classic example of the ability of humans to shape
their physical environments—with unforeseen health consequences (Living-
Anthropologists have explored the health implications of (a
) sexual behav-
iors (Lindenbaum 1991; MacQueen et al 1996; Waddell 1996); (b
practices (Lindenbaum 1990); (c
) ethnic conflict and genocide (Tambiah
1989); and (d
) population displacement (Bisharat 1995; Malkki 1995; Toole
1995). Recent work in transnationalism identifies the political, economic, and
social trends that are increasingly integrating the world’s diverse populations
(Kearney 1995). The emerging paradigm of evolutionary medicine demon-
strates the applicability of evolutionary principles to contemporary health is-
sues (Armelagos 1997), and emphasizes the ability of humans to shape their
environment through pathogen selection (Lederberg 1997). Finally, anthro-
pologists have critiqued the political-economic constraints that limit access to
health care and basic public-health needs (Farmer 1996; Inhorn & Brown
1990; Risse 1988). Given this range of issues impacting human-disease rela-
tionships, even anthropologists not directly concerned with infection can make
significant contributions to an improved understanding of disease emergence.
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Critérios para doação de sangue e plaquetas por aférese O doador de sangue ou componentes deve ter idade de, no mínimo, 18 anos completos e, Peso : O peso mínimo para um candidato ser aceito para a doação é de 50 kg. Freqüência e intervalo entre as doações Para doação de sangue: 4 (quatro) doações anuais para os homens, e de 3 (três) doações anuais para O inte
NEWS from AEFJN – No. 55, January 2012 _________________________________________________________________________________ CORPORATE SOCIAL RESPONSIBILITY How big business has seized control of global climate negotiations The Polaris Institute has prepared a report outlining how multinational corporations and their lobbyists haveinfiltrated the United Nations and are influencing the ou