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Annu. Rev. Anthropol. 2008.37:267-282. Downloaded from www.annualreviews.org
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ANNUAL
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From Resilience to Resistance:
Political Ecological Lessons
from Antibiotic and
Pesticide Resistance
Kathryn M. Orzech and Mark Nichter
Department of Anthropology, University of Arizona, Tucson, Arizona 85721;
email: [email protected], [email protected]
Annu. Rev. Anthropol. 2008. 37:267–82
Key Words
First published online as a Review in Advance on
June 18, 2008
antibiotic misuse, hygiene hypothesis, tragedy of the commons, global
health governance
The Annual Review of Anthropology is online at
anthro.annualreviews.org
This article’s doi:
10.1146/annurev.anthro.37.081407.085205
c 2008 by Annual Reviews.
Copyright All rights reserved
0084-6570/08/1021-0267$20.00
Abstract
This article investigates the interplay of natural and human systems with
reference to the growing global problem of antibiotic resistance. Among
the diverse causes of antibiotic resistance, we focus broadly on three related causes: pharmaceutical practice and the liberal consumption of
antibiotics, the use of antibiotic-containing products in the home, and
the use of antibiotics in commercial animal husbandry and agriculture.
We draw a parallel between pesticide and antibiotic resistance and examine whether lessons learned from one case may be applicable to the
other. Although our main focus is a microecological analysis examining
how humans are changing their environments, our conclusion addresses
larger implications of this problem for global health. Through the theoretical lens of political ecology, we ask how we may address the “tragedy
of the antibiotic commons” through public education and consumer activism as well as global health governance.
267
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INTRODUCTION
Antibiotic resistance:
when a bacterial
genetic mutation
interferes with an
antibiotic’s ability to
effectively control or
kill bacteria
Political ecology:
theoretical perspective
combining ecology
with political
economy, looking at
the natural, social,
political, and economic
worlds as intertwined
268
The complex adaptive nature of ecosystems
means that evolutionary forces are strongest at
lower levels of organization; we have learned
that the hard way in our continual battles with
the evolution of resistance to pesticides and
antibiotics, and the unwillingness of microorganisms to take a reasonable approach to making things easy for us. (Levin 2001, p. 17)
Widespread antibiotic resistance is one of the
hallmarks of the third epidemiological transition, where populations move from a chronic
disease burden back to an increasingly uncontrollable burden of infectious disease (Barrett
et al. 1998). Experts have been sounding the
alarm about antibiotic resistance for some time
(Anderson 2004, Morse 1995), but the many
stakeholders involved in the development and
spread of antibiotic resistance have been reluctant to take action. A major challenge in
addressing antibiotic resistance is that both
human and microbial factors contribute to its
persistence. This article addresses antibiotic resistance in an evolutionary context by viewing
it from both the human and microbe points of
view, as well as by taking a broad view of human antibiotic use behavior. The perspective of
political ecology is useful here because it combines the examination of ecology with political economy. It looks at the natural world as
intertwined with the social, political, and economic world created by humans and explores
the unequal power relations that often mediate human-environmental interaction (Bryant
1998, Greenberg & Park 1994). Although humans can anticipate and prepare for the future, biotic systems rely on “the success of past
evolutionary experimentation” (Peterson 2000,
p. 325), an important distinction to make when
exploring the factors contributing to antibiotic
resistance and also its potential solutions.
This article draws on Darwin’s original definition of evolution as descent with modification
(Darwin 1958 [1859]). The modern synthesis
of evolution illuminates contemporary ideas of
heritability (Mayr 2001), but the focus here is on
modifications favored by natural selection that
Orzech
·
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better fit organisms to their environments. This
emphasis may differ from other utilizations of
evolution because it acknowledges a sometimes
pervasive idea that selection should work for the
benefit of humans. It is clear from the example of antibiotic resistance, however, that natural selection does not favor one species over
another.
Antibiotics have been widespread since the
mid-twentieth century, but as soon as an antibiotic is introduced into a hospital or community
setting, some resistance typically develops. For
example, with penicillin resistance, a few bacteria came into contact with a naturally occurring
fungus, and those bacteria that survived passed
on this genetic immunity to future generations. Since the 1970s, however, antibiotic resistance has been rising more rapidly than before
(Barrett et al. 1998, Harrison & Lederberg
1998, Lewis 1995). According to a Web resource designed to publicize environmental
public health research findings, the rate of penicillin resistance increased by more than 300%
between 1997 and 2002 (EMS 2002). Although
it is beyond the scope of this review, antiviral
resistance is also a growing problem, exemplified by the rapidly-evolving human immunodeficiency virus.
The importance of antibiotic resistance as a
growing public health problem cannot be overstated (WHO 2001). Mortality, likelihood of
hospitalization, and the length of hospital stay
are approximately twice as great for individuals with resistant infections, compared with
individuals with susceptible strains of bacteria
(Holmberg et al. 1987). Disease transmission
also increases because people remain infected
longer. Antibiotic-resistant infections are more
expensive to treat, and sometimes, because of
costs or drug scarcity, they may be untreatable (Alliance Prudent Use Antib. 2005). Noting that the presence of resistant bacteria leads
to poorer outcomes, however, does not tell the
whole story. As resistance rates rise in one area,
a switch may be made to a more expensive
first-line antibiotic, so even those patients with
infections susceptible to the initial antibiotic
pay the additional cost to be treated with the
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more expensive drug (Howard et al. 2003). The
misuse of a common antibiotic resource by a
few individuals results in negative consequences
for many (Baquero & Campos 2003, Foster &
Grundmann 2006), bringing to mind the concept of tragedy of the commons (Hardin 1968).
What Factors Encourage
Antibiotic Resistance?
Antibiotic resistance is difficult to control
because of the involvement of many different stakeholders. Following Blaikie (1995),
Figure 1 presents a “chain of explanation” for
antibiotic resistance. Although many areas of
the world have interconnected problems of
resistance, this example uses the United States
as a specific locus for the problem.
Humans have created an ideal environment
for the development of antibiotic resistance.
Health care providers often use antibiotics as
part of a diagnosis-by-treatment strategy. Antibiotics are also freely available to laypeople
over the counter in developing countries, and
people often use these drugs to self-medicate
(Abellanosa & Nichter 1996, Kamat & Nichter
1998, Nichter & Vuckovic 1994, Saradamma
et al. 2000). Individuals may take antibiotics
prophylactically, including for a cold or flu or
even to reduce the chances of acquiring HIV
or anthrax. Natural selection dictates that the
selective pressure of antibiotic use will increase
the number of resistant bacteria (Lieberman &
Wootan 1998), but each of the stakeholders involved sees only a partial picture of the consequences for his/her actions. The situation is
complicated by the fact that bacteria may also
exist in a benign form in the body. When an
individual is treated with a broad-spectrum antibiotic, the bacteria are exposed and resistant
strains may be selected (Courvalin 2005). These
resistant bacteria can then spread and colonize
other people (Lipsitch & Samore 2002).
In addition to ingesting antibiotics, humans
may be altering their environments by using antibacterial products in the home. These products, originally developed for use in hospitals,
have made their way onto commercial shelves
in increasing numbers. From 1990 to 2003, the
number of antibacterial products jumped from
23 to more than 700 (Levy 2003). A direct relationship between use of antibacterial products
and antibiotic resistance is hard to determine
(Aiello & Larson 2003). A major concern remains, however, that relatively harmless bacteria that develop resistance from exposure to
household products may transfer their resistance genes to other bacteria that will be more
hazardous to human health (Lipsitch & Samore
2002, Tan et al. 2002).
Antibiotic resistance is also promoted
through modern animal and plant husbandry.
Animals are often raised in very close quarters, and farmers use low levels of antibiotics in animal feed to keep the group of animals healthy. Antibiotics are also often used as
growth promoters, and these constant subtherapeutic doses are an ideal environment for the
selection of resistance genes. Experts estimate
that between 36% and 70% of all antibiotics
used in the United States are used on animals
(EMS 2002).
Although the numbers presented in Table 1
are from 1995, they provide a graphic overview
of quantities of antibiotics used annually in the
United States alone. The 1995 date also indicates the difficulty of finding data across several
major sites of antibiotic use in the same time
frame.
Tragedy of the
commons: conflict
over finite resources
readily available within
the public domain
results in tension
between self interest
and the common good
Selective pressure:
the influence of some
factor that affects
natural selection to
promote survival of
one organism over
another
Broad-spectrum
(versus narrowspectrum)
antibiotics: are active
against a wider group
of bacterial types than
are narrow-spectrum
antibiotics
Antibacterial
products: products
containing an
antibacterial, a
substance that
interferes with the
growth and
reproduction of
bacteria
View from the Microbe
One difficulty in coping with antibiotic resistance is that bacteria acquire and express
resistance in diverse ways (Figure 2). Replication mutations are common in bacteria, as is
gene swapping within and between bacterial
species (Lemon 2003). Under stress, such
as antibiotic exposure, bacteria can increase
their mutation rates, which could result in
an accelerated rate of selection and produce
more resistant organisms (Martinez & Baquero
2000). Cross-resistance, when a bacterial
mutation in the presence of one antibiotic
proves effective against other antibiotics,
may be problematic (Levy 2001). Recently
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Table 1
Estimated annual antibiotic use in humans and animals in the United States, and resistant pathogensa
Target
group
Site of use
Humans
Hospital
Therapeutic,
prophylactic
∼190 million annually
defined daily doses
25%–45%
Staphylococci, enterococci,
gram-negative rods
Humans
Community
Therapeutic,
prophylactic
∼145 million courses
(110 million outpatient,
35 million emergency room)
20%–50%
Pneumococci, gonococci, Group
A streptococci, Escherichia coli,
Mycobacterium tuberculosis
Animals
Farm
Therapeutic
∼4 million pounds
40%–80%
Salmonella, campylobacter
Prophylactic
∼16 million pounds
Uses
Amount
Use estimated
as unnecessary
Resistant pathogens
a
This table follows table 3 in Harrison & Lederberg (1998 pp. 40–41), drawn from a September 1995 Congressional Office of Technology Assessment
report, Impacts of Antibiotic-Resistant Bacteria, OTA-H-629.
Fitness cost:
regarding natural
selection, anything
that decreases the
amount of genetic
material an individual
can pass on to the next
generation
TB: tuberculosis
discovered interspecies communication among
bacteria (Federle & Bassler 2003, Waters &
Bassler 2005) may also worsen the effects of
resistance for humans. The human immune
system may be able to mediate some effects of
antibiotic resistance but is limited by its own
set of biological and social constraints (see
sidebar, View from the Immune System).
VIEW FROM THE IMMUNE SYSTEM
In early life, stem cells migrate to the thymus, where they mature into T-lymphocytes (T-cells), which mediate cellular immunity against pathogens. When a pathogen enters the body,
accessory cells process the antigen and present it to the T-cells
that have receptors for that antigen. This action allows the adaptive immune system to identify the pathogen and educate itself
to recognize this interloper in the future (Hoffman-Goetz 1986).
Immunity also depends on factors such as the life stage of the affected individual and his or her social and economic status. Children are particularly at risk for infections because of immature
immune systems, lack of attention to hygiene, and close proximity to other children (Bradley 2003). Breastfeeding increases
the infant’s maternal antibodies and defense factors (McDade &
Worthman 1999). Adequate nutritional resources are required to
ensure adequate immune response, but in individuals of lower status, these may be diminished (Bhaskaram 2002). However, affluence and quick physician access may lead to overuse of antibiotics
(Lieberman & Wootan 1998). This may result in an immune system that has not been properly “educated” on how to cope with
pathogens (for more on this education model of immunity, see
Aaby 1995, Cone & Martin 1998).
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For a microbe, the evolutionary question is
whether the fitness cost is low or high for the
genetic changes that mediate resistance. This is
still an open question (Levy 1998, Luskin 2001),
but research with izonaid-resistant tuberculosis (TB) seems to support the “low cost” side
(Cohen et al. 2004).
HUMAN PRESCRIPTION
AND CONSUMPTION
OF ANTIBIOTICS
General overuse of antibiotics has been documented in both developed and developing
countries. Patients may covertly or overtly
demand antibiotics from physicians or may
purchase antibiotics over the counter or from
nonpharmacy sources in many countries
(Radyowijati & Haak 2003). Although the ability to purchase antibiotics without a physician
prescription may seem to encourage misuse,
several authors have addressed the positive side
of this practice (Bang et al. 1990, van der Geest
1987).
In competitive health-care markets around
the world, doctors look for drugs with a
“demonstration effect” so patients feel that they
have “really received care” and will return to
that practitioner. As a result, doctors may prefer injections and broad-spectrum antibiotics
to pills or a narrow-spectrum drug that may
not produce as noticeable of an effect (Nichter
2008, Nichter & Vuckovic 1994).
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Another factor that contributes to overuse of
antibiotics is that, especially in countries with an
organized insurance scheme, hospital patients
are increasingly seriously ill. “At any given time,
25 to 40% of hospital patients are receiving intravenous antibiotics” (Lieberman & Wootan
1998, p. 5). Hospitals use broad-spectrum antibiotics at a high rate rather than waiting the
24 hours necessary to conduct a culture and
susceptibility test to determine whether a
narrow-spectrum antibiotic might prove more
effective (Lieberman & Wootan 1998).
Although many infections are viral in origin and improve without any treatment, practitioners may prescribe inappropriate antibiotics
to respond to patient demands (Paredes et al.
1996). Practitioners may be pressed for time
and have a desire to help their patients, and
writing a prescription for a powerful antibiotic
convinces the patient that he or she has “received care” from the practitioner (Nizami et al.
1997). Inadequate provision of practice guidelines and supervision may also play a role in inappropriate prescription of antibiotics (Chalker
2001). Where medication is limited, practitioners may prescribe what the dispensary has on
hand rather than the antibiotic most appropriate for the patient’s condition.
Failing to complete full courses of antibiotics is a worldwide practice, but especially
common in non-Western countries, where it
is possible to buy antibiotics over the counter.
Individuals may buy an incomplete course of
antibiotics because of financial constraints, to
test the efficacy of a remedy, or to limit the
amount of powerful medicine ingested by a
patient (Kamat & Nichter 1998, Simon et al.
1996). By taking an incomplete course, an individual may be left with “extra” antibiotics to use
at a later date, causing these drugs to become
staples of the home medicine cabinet (Okumura
et al. 2002, Stratchounski et al. 2003). Counterfeit drugs are also much more prevalent in
developing countries and may contain too little
of the active ingredient or different ingredients
entirely (Kelesidis et al. 2007, WHO 1999).
The prophylactic use of antibiotics in humans is a worldwide problem that contributes
to antibiotic resistance. Patients being prepped
for surgery in the United States may receive
antibiotics to prevent postsurgical infection,
and teenagers with acne may be put on low
doses of tetracycline to decrease levels of acnecausing bacteria (Lieberman & Wootan 1998).
In other countries, for example, the Philippines
and Thailand, individuals may take an antibiotic, often a first-line TB drug, Rifampin, after
eating food of questionable hygienic status or as
protection against contracting a sexually transmitted disease (STD) after visiting a prostitute
(Nichter 2001). With increasing “medicalization” of daily life, prophylactic use of antibiotics and the use of medications to preemptively
combat a potential illness will continue to be
common practices unless a strong case is made
against them.
Susceptibility test:
a measure of how well
an antibiotic affects
bacteria. Susceptible
bacteria are killed or
inhibited by an
antibiotic
Hygiene hypothesis:
suggests that exposure
to antigens via
childhood infections
educates the immune
system and results in a
lower prevalence of
allergies
IMMUNE SYSTEM HARM
REDUCTION: ANTIBACTERIAL
OVERLOAD AND THE
HYGIENE HYPOTHESIS
From 1990 to 2003, the number of available
antibacterial products jumped from 23 to more
than 700 (Levy 2003). This increase does not
reflect just cleaning products infused with an
antibacterial agent. Many products are modified to contain triclosan (a common antibacterial agent), including pillows, sheets, towels,
and slippers (Levy 2001). Despite a lack of scientific data to support the efficacy of antibioticcontaining products in the home, more than
45% of consumer soaps, for example, contain
an antibiotic agent (Tan et al. 2002).
Society’s move away from nature, and the
microbes such proximity entails, changes a previously held balance. The disadvantage of living in close proximity to animals is zoonotic
disease, but the benefit of this nearness may
be exposure to antigens early in life that educate our immune systems about what to react
to and what to ignore. Epidemiologist David
Strachan (1989) codified this idea in the hygiene
hypothesis.
The hygiene hypothesis asserts that children exposed to bacterial and viral antigens via
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infections have a lower prevalence of allergies
(atopy). Protective factors against atopy include
the presence of siblings and day care attendance
early in life (Douwes & Pearce 2002, Strachan
1999). Living on a farm also seems to show a
protective effect (Leynaert et al. 2001). More
recent studies have affirmed some protective
effect of the above-mentioned factors but
have not found childhood infections to be
a prime protective factor against later atopy
(Benn et al. 2004). A 2005 paper introduces
an alternative hypothesis that ties increasing
rates of childhood asthma (a rise that has
paralleled the increase in allergies) to “artificial
habitats.” This hypothesis suggests that atopy
and asthma have not been driven by changes
in infection levels from the “environment of
evolutionary adaptation,” but instead have
increased because of a more complicated set
of interrelated factors concerning housing and
lifestyle (Maziak 2005).
ANTIBIOTIC USE IN ANIMALS
AND PLANTS
Each year more than 8 million kilograms (kg) of
antibiotics are given to animals and 22,000 kg
are applied to fruit trees, representing more
than 40%—and perhaps as much as 70%—
of the antibiotics manufactured in the United
States (Horrigan et al. 2002, Khachatourians
1998). As much as 80%–90% of this total
is administered in subtherapeutic doses for
growth promotion, improved feed conversion,
and disease prevention (EMS 2002, Levy 1998,
Lieberman & Wootan 1998; Mellor 2004).
In addition to direct exposure (consumption of animal products harboring resistant
bacteria), there are a number of other ways
for humans to acquire bacteria from animals.
Antibiotic-resistant bacteria may be acquired
from crops fertilized by or water contaminated by animal waste (EMS 2002), or bacteria may pass from person to person. A recent study found that ∼26% of bacterial isolates
taken from swine farm workers harbored resis-
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tant bacteria. Those farms that used antibioticcontaining food for their pigs had a higher
percentage of resistant isolates, a finding that
echoes previous studies of poultry farms (Akwar
et al. 2007). Although recent data such as these
are alarming, meat producers are often unwilling to change practices for fear that the economic impact will be too great. Evidence suggests, however, that modification of procedures
to decrease the use of antibiotics can be performed without a loss in production (Thomke
& Elwinger 1997).
Direct links may be made between use of
particular antibiotics in animals and a corresponding rise in resistance among bacteria that afflict humans. Fluoroquinolone use
in poultry has been tied to fluoroquinoloneresistant Campylobacter. The use of the antibiotic avoparcin in food animals and a rise in
vancomycin-resistant enterococci (VRE) have
also been linked (Keep Antibiot. Work. 2001,
Lieberman & Wootan 1998; Wegener 2005).
Even more recently, Chinese farmers have been
dosing poultry flocks with the antiviral amantadine, potentially selecting for resistant strains
of the H5N1 bird flu virus and rendering amantadine useless against human flu cases (Sipress
2005).
The use of antibiotics on crops is also a
salient part of antibiotic resistance. Although
only a small percentage of antibiotics produced
for agriculture are used on plants, the quantity
is still large enough for plant pathogens to have
developed streptomycin resistance and for nonpathogenic orchard bacteria to have acquired
tetracycline resistance (McManus 1999). The
main bacterial pathogen for plants is related to
other bacteria such as Escherichia coli, Salmonella,
and Shigella, all common human pathogens
(Lieberman & Wootan 1998). Aspects of this
kind of antibiotic application, where antibiotics
are applied over physically large areas in ways
that may affect both groundwater and fruit supplies, leave the potential danger of this practice open for further investigation (McManus
1999).
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THE PESTICIDE RESISTANCE
PARALLEL
In 2001, the Food and Agriculture Organization reported more than 700 pest species were
resistant to pesticides. A parallel may be drawn
between the way that the presence of an antibiotic and the presence of a pesticide both select
for resistance in their target species. Bacteria
and insects often acquire resistance in the same
way, through a single mutation. In the common
fruit fly Drosophila, one gene change allows the
fly to overproduce an enzyme that breaks down
dichloro-diphenyl-trichloroethane (DDT) and
other poisons. As seems to be the case in at least
some instances of antibiotic resistance, removal
of the selective agent (the global decline in the
use of DDT in this case) does not necessarily
cause the insects to revert back to a susceptible
state (Major et al. 2003).
Given that pesticide resistance emerged as a
problem earlier than did antibiotic resistance,
what can we learn from this experience? Two
methods to slow the development of resistance
in pests are rotating pesticides and using mixtures of chemicals. These methods (and their
parallels in antibiotic cycling and combination
therapies) ensure that individuals are not repeatedly exposed to the same pesticide and/or
antibiotic. Targeting a specific pest or bacterial
species through “spot spraying,” analogous to
using narrow-spectrum antibiotics in humans,
also limits exposure for other organisms, reducing cross-resistance. Evaluating the results of
treatment can also help farmers or doctors to
choose a more effective treatment (Gemplers
2008).
Two places where an antibiotic/pesticide
parallel breaks down are in the areas of behavioral modification and creation of “refugia.”
Whereas insects can modify their behavior
(for example, to dwell on the underside of
leaves where pesticide concentrations may be
lower), bacteria are not capable of this kind
of behavior modification. Creating “refugia”
where antibiotic-susceptible bacteria could live
(parallel to not spraying certain sections of
fields to encourage development of pesticide-
susceptible insects) (Gemplers 2008) would be
unethical because it would mean denying some
patients necessary antibiotics. Instead, limiting
antibiotic misuse helps to maximize the number
of susceptible bacteria.
POTENTIAL SOLUTIONS
To minimize antibiotic resistance, solutions
may be drawn from biological, social, and evolutionary realms, with the most effective plans
combining elements from all three. See Table 2
for several possible biological solutions.
Combination therapies are a particularly
useful biological solution because with this
method each drug attacks bacteria in a different way, minimizing resistance (Kaplan 2003).
Antibiotic cycling, on the other hand, may not
be as promising a solution because the assumed
fitness cost to bacteria for becoming antibiotic
resistant seems slight, and true cycling requires
a return to the original antibiotic agent or class.
When that occurs, resistance to that agent usually resurfaces rapidly (Gerding 2000, Hodges
& White 2001).
A variety of social solutions may also help
minimize antibiotic resistance (see Table 3).
Educating patients on proper antibiotic use
is an important first step. Recent research has
linked specific antibiotic overuse to specific
rises in resistant bacteria within certain countries (Abramson & Givner 1999, Albrich et al.
2004). Each time an antibiotic is ingested, the
likelihood increases that the antibiotic will be
less effective in the future not only for the
person who took the antibiotic, but for others as well (Laxminarayan & Brown 2001).
This reality returns us to the tragedy of the
commons. By conceptualizing antibiotics as an
always-effective global resource, neither patients nor practitioners think about the effects
of their antibiotic misuse on the larger population (Simpson et al. 2007).
Encouraging consumers to demand more
responsible antibiotic use has proven effective in some cases. McDonalds Corporation
now prohibits their direct suppliers from using “medically important antibiotics” as growth
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Table 2
Biological solutionsa
Solution
Methods to achieve solution
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Getting the antibiotic right
More bacterial testing of individuals
Better surveillance of resistant pathogens at the local (Mabey et al. 2004), national (Invasive
Bacterial Infection Surveillance (IBIS) Group 1999, Simonsen et al. 2004, Thomas et al. 2003),
and global levels (data sharing)
Redefining “a dose” of antibiotics
Calculating appropriate dosage based on the individual
Social marketing about the meaning of “a dose”
Blister packs with “a full dose”
Prescribing shorter courses of
antibiotics
Confirm effectiveness of shorter (3-day versus 5-day) courses (el Moussaoui et al. 2006); if equally
effective these could:
1. increase compliance with treatment,
2. reduce financial burden of taking antibiotics, and
3. diminish selective pressure on bacteria
Combination therapies
“Free combinations” (several different pills are taken together)
FDCs (more than one drug combined in a single pill)
Antibiotic cycling
a
Rotating antibiotics to allow bacteria to revert back to a susceptible state (Empey et al. 2002,
Schentag 2001)
Abbreviations: FDC, fixed dose combination.
promoters. However, the practice of treating
whole flocks or herds for disease when a few
animals fall ill is still permitted (UCS 2003).
Legislative regulation of antibiotics has generally been less effective, however. In 2005, bills
to limit the agricultural use of eight “medically
important” antibiotics were introduced in both
houses of Congress and referred to committee.
In 2007, a modified version of the bill was introduced again, but again stalled in committee.
The FDA has recently been spurred to action
by a variety of food contamination cases, however, and has curbed the sale of farm-raised fish
from China, citing indiscriminate use of antibiotics, particularly fluoroquinolones, by Chinese
farmers (Martin 2007).
Finally, two evolutionary solutions may minimize antibiotic resistance (see Table 4).
CONCLUSION: WHAT CAN WE
LEARN FROM THE RISING TIDE
OF RESISTANCE?
The evolution of antibiotic resistance is
strongly influenced by the economic behavior
of individuals and institutions. The more antibiotics are used (or misused), the greater the
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selective pressure placed on bacteria to evolve.
The problem, therefore, arises from the absence of economic incentives to take into
account the negative impact of their use of
antibiotics on social welfare. (Laxminarayan
& Brown 2001 p. 184)
The age of globalization is the age of universal
contagion. (Hardt & Negri 2000, p. 136)
Antibiotic resistance teaches us about the complex interactions among microbes, plants, animals, and humans. One key lesson is that overreliance on quick fixes is often shortsighted,
leaving us blindsided by new problems. Antibiotic resistance is a wake-up call for those who
have adopted a view of health that pays scant
attention to the interaction among species in
an ever-changing micro- as well as macroenvironment. Evolutionarily, it is clear that natural
selection fits organisms to their environments
and does not favor one species over another.
Given the multitude of factors contributing to
antibiotic resistance, complex systems thinking such as that found in political ecology and
ecosocial approaches to epidemiology (Krieger
2001) are needed to account for the impact
Table 3
Social solutionsa
Solution
Methods to achieve solution
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Minimize microbes
Even given the realities of poverty, endeavor to provide clean water and well-ventilated housing
(Okeke et al. 1999, Pang & Guindon 2004)
Encourage better hand-washing practices worldwide (Tierno 2001)
Implement vaccination programs against common illnesses like pneumonia and measles
Educate patients on proper
antibiotic use to avoid misuse
Encourage the use of replacement medications such as vitamins or other needed supplements
Delay prescription of antibiotics for illnesses that are often viral in origin, perhaps with a
safety-net prescription to be filled just in case (Rietveld et al. 2006, Siegel et al. 2003)
Address patients’ “individual” understanding of resistance (Bull 2000) by conducting translational
research to express that by not completing a course of antibiotics, patients increase the presence
of resistant bacteria, which is a danger to all in the long term
Educate practitioners on
appropriate prescribing
Reduce misinformation given to providers about which drugs should be relied upon as first-line
drugs
Focus on practitioner oversight through education and STGs, which have proven effective (2000,
Bavestrello & Cabello 2000)
Make sure practitioners are alert to the possibility of inappropriately curbing antibiotic use (Price
et al. 2004)
Minimize influence of
pharmaceutical companies
Be aware that most drug information provided to practitioners in developing countries may come
from pharmaceutical representatives, who are likely to be biased toward recommending newer
and more costly drugs (Lexchin 2000)
Make efforts to monitor phamaceutical advertising
Consider economic issues
Encourage pharmaceutical companies to invest in new classes of antibiotics (Spellberg et al. 2004)
to treat the growing number of multidrug-resistant infections aptly illustrated by the recent
flare-up of community-acquired MRSA (Klevens et al. 2007)
Reduce antibiotic use in animals
and plants
Encourage consumers to demand an end to the use of antibiotics as growth promoters
a
Implement regulations through Congress or the FDA (Keep Antibiot. Work. 2001)
Abbreviations: FDA, Food and Drug Administration; MRSA, multi-drug resistant Staphylococcus aureus; STG: standard treatment guideline.
of political economic policy on medicine use.
Attention must be turned to the set of human
factors that affect medication use, especially in
the private medical sector encouraged by prevailing neoliberal policies across much of the
world.
Table 4
A second key lesson taught to us by antibiotic resistance is just how rapidly the global
can be affected by the local in the realm of
microecology (Avorn & Solomon 2000, Martin
2006), a lesson we are also learning from emergent diseases such as severe acute respiratory
Evolutionary solutions
Solution
Turn bacteria against themselves
Methods to achieve solution
Seek ways to make resistant microbes less fit in their environment (Zhang et al. 2006)
Follow the example of Daigle and colleagues (1997) who have inhibited bacterial resistance
enzymes using a modified protein kinase inhibitor, taking advantage of structural similarities
between resistance enzymes and some protein kinases
Encourage an effective immune
response in the host
Remember that cells involved in immune response, like the microbes they combat, exist in large,
rapidly multiplying populations
Recognize that the adaptive immune system uses an education model to create antibodies that
bind to specific foreign antigens (McDade & Worthman 1999).
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syndrome (SARS) and the avian flu. Strains of
resistant bacteria that spread rapidly force us
to rethink borders and the need for concerted
global action in the area of pharmaceutical
practice (Fidler 2003). A global sentinel
surveillance system is called for to monitor
antibiotic sensitivity/specificity as well as drug
supply and patterns of use. It is becoming increasingly clear that it is in the best interests of
wealthy countries to ensure that less developed
countries have access to supplies of essential
medicines to treat infectious disease, despite
the perception that these diseases are “tropical”
and distant from their shores (Nichter 2008).
The same is true for the use of antibiotics
in agriculture. The biology of how animals acquire resistant bacteria and how those bacteria
may be transferred from plants and animals to
humans is becoming increasingly evident. Yet
private industry has been notoriously ineffective at regulating its use of antibiotics except
when forced to do so. Consumers play their own
roles through their purchasing habits and willingness to acquire foods grown under globally
irresponsible conditions. Knowledge and perception are beginning to change, however, in
countries where quality of food has become a
matter of growing public interest and concern.
A final question remains: “Is the oftendiscussed tragedy of the commons a good
metaphor for understanding antibiotic resistance?” Our answer is yes and no. Antibiotics
are not a “global public good” because they are
privately developed, manufactured, sold, and
managed according to the profit motives of
pharmaceutical companies. These companies
also influence prescribing habits of doctors and
government policies. Despite this reservation,
however, the tragedy of the commons metaphor
brings needed attention to the issue of resistance and encourages patients and practitioners to think beyond their own personal benefit
from using (or misusing) antibiotics.
The key to human resilience lies in the
unique ability to collect information about microorganisms in an ever-changing environment
and the capability to engage in the judicious use
276
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and monitoring of antibiotics. Furthermore, we
must involve the public in active strategies that
enhance global health in ways that make ecological sense. For meaningful change to take place,
transnational attention needs to be turned to
global trends of medicine use that indirectly
but powerfully affect pharmaceutical effectiveness. Global responsibility for health demands
changes in government policy as it pertains to
allocation of resources. In addition, global policies need to address pharmaceutical industry
marketing practices that encourage antibiotic
resistance.
The global elements of a successful strategy against antibiotic resistance include consumer and practitioner education, technical development, legal regulation, and international
surveillance of antibiotic use (Khachatourians
1998). We also need to address health care disparities by making essential drugs readily available to the poor at an affordable price. These
elements require a coordinated international effort, with some central body providing oversight and accountability so as to minimize conflicts in policy agendas (Fidler 2007).
At least two factors will transform the reality of antibiotic resistance from a biological
concern into a biopolitical problem. First, our
increasing inability to treat widespread diseases
such as TB and malaria with a single drug will
make it obvious to various stakeholders that a
change in how we view antibiotics is overdue.
Second, subpolitics (Beck 1996), which entails
political engagement outside and beyond the
institutions of the political system of nationstates, encourages conscientious consumption
and examination of global commodity chains
(Hughes & Reimer 2004). This focus helps individuals realize that by putting pressure on
multinational corporations, they can affect how
food is grown and raised, to the ultimate benefit of all. Some measure of antibiotic resistance
is related to poverty and inappropriate drug
use. Far more antibiotic resistance, however, is
caused by noncompliance of people and corporations in the agricultural and medical fields and
by the pricing of products beyond the reach of
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those people who would use such products effectively. This kind of biopolitical problem also
opens up many issues for anthropologists because the global scope of antibiotic resistance
forces us to think on many interconnected levels instead of thinking of individuals, states, or
global corporations as isolated causes of this
phenomenon.
SUMMARY POINTS
1. A variety of factors, related to both biology and human behavior, impact levels of
antibiotic-resistant bacteria in a given area of the world.
2. Although we may think natural selection should operate for the benefit of humans, in
reality, selection fits organisms to their environments and makes no distinction between
humans and bacteria.
3. Humans worldwide engage in overuse and misuse of antibiotics, for a variety of reasons.
4. Use of antibacterial products in the home may encourage the development of resistant
organisms, but more research is needed to determine how detrimental this practice may
be to human health.
5. Antibiotic use in animals and plants is an often-overlooked part of the antibiotic resistance
equation.
6. Parallels may be drawn between solutions to the longer-standing problem of pesticide
resistance and the newer problem of widespread antibiotic resistance.
7. Potential solutions to rising rates of antibiotic resistance may be found at the biological,
social, and evolutionary levels.
8. Truly making strides toward solving the antibiotic resistance problem will require a high
degree of foresight and international cooperation among the world’s governments.
FUTURE ISSUES
1. How do individual patients and community health care workers presently understand
antibiotic resistance: as an individual problem related to noncompliance or compatibility,
or as a population-based issue? Translational research is needed to improve understanding
of public perceptions of antibiotic resistance.
2. How might information about antibiotic resistance rates best be circulated among networks of health practitioners; what might motivate them to alter their prescription practices as members of a community of practice, and why bother?
3. What role might pharmaceutical companies play in national/regional efforts to monitor
trends in antibiotic use and emerging antibiotic resistance? What governmental policies
and incentives might be introduced to encourage them to share information with health
planners and epidemiologists?
4. Research into the political economy of antibiotic use is needed. To begin, researchers
might conduct a commodity chain assessment focused on the push-pull dynamics
(Fabricant & Hirschhorn 1987) of antibiotic production, marketing, demand, use, and
oversight among stakeholders at each node in the chain.
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277
DISCLOSURE STATEMENT
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The authors are not aware of any biases that might be perceived as affecting the objectivity of this
review.
ACKNOWLEDGMENTS
We offer our thanks to the many colleagues whose scholarship contributed to this review. We
apologize in advance to those whose research may have been left out owing to space constraints.
Thanks go to Paul Orzech for his initial design work on Figure 2.
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antibiotic effectiveness
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B. Economic
symptoms in the
United States
C. Specific
antibiotic-use
practices in the
United States
D. Local
stakeholders for
antibiotic use
Rising rates of antibiotic-resistant bacteria
Growing ineffectiveness of cheap
generic antibiotics
Switch to more expensive second
or third-line drugs
Overuse and inappropriate use of
antibiotics
Overuse of antibacterial products
in the home
Use of subtherapeutic doses of antibiotics on
animals
Individuals/patients
Health practitioners
Farmers and growers
Widely available antibiotics
E. Nature of the
U.S. health care
system
F. National-level
realities
G. Multinational
realities
"Quick fix" mentality
Patients in hospitals increasingly very sick and on antibiotics
Health care system
encourages pills as solutions
to a multitude of ills
Factory farming increases pressure to
treat animals with antibiotics
Consumer marketing campaigns
encourage use of antibacterial
products in the home
National legislation to restrict
agricultural use of medically important
antibiotics has stalled
International travel spreads
resistant strains of bacteria fast
Pharmaceutical companies influence
which drugs practitioners recommend
and patients request
Agrochemical companies
influence which antibiotics are
available for animal and plant uses
Corporations signal the acceptability
of consuming animals and plants
treated with antibiotics
Figure 1
Chain of explanation for antibiotic resistance in the United States.
www.annualreviews.org
●
Antibiotic and Pesticide Resistance
C-1
Orzech.qxd 10/23/09 12:39 PM Page C-2 pinnacles AR:Users:pinnacles:Desktop:AR_PROBLEM:ANRV355-AN37-16:COLOR FIGURE:
Acquiring resistance
Expressing resistance
Transformation
Thickened cell wall
wards off antibiotics
that attack cell walls
Conspecific
microbial sex
Annu. Rev. Anthropol. 2008.37:267-282. Downloaded from www.annualreviews.org
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Pump transports
antibiotics
from cell
Plasmid
transfer
Exchange
of genetic
material
across
species
Mutation
CTG
CTC
Antibiotic
Enzyme
degrades
or alters
antibiotic
Figure 2
Ways bacteria acquire and express antibiotic resistance.
C-2
Orzech
●
Nichter
Altered
antibiotic
AR355-FM
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14 August 2008
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Annual Review of
Anthropology
Annu. Rev. Anthropol. 2008.37:267-282. Downloaded from www.annualreviews.org
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Contents
Volume 37, 2008
Prefatory Chapter
The Human Brain Evolving: A Personal Retrospective
Ralph L. Holloway p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 1
Archaeology
Evolution in Archaeology
Stephen Shennan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p75
The Archaeology of Childhood
Jane Eva Baxter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 159
The Archaeological Evidence for Social Evolution
Joyce Marcus p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 251
Sexuality Studies in Archaeology
Barbara L. Voss p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Biological Anthropology
The Effects of Kin on Primate Life Histories
Karen B. Strier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p21
Evolutionary Models of Women’s Reproductive Functioning
Virginia J. Vitzthum p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p53
Detecting the Genetic Signature of Natural Selection in Human
Populations: Models, Methods, and Data
Angela M. Hancock and Anna Di Rienzo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 197
Linguistics and Communicative Practices
Linguistic Anthropology of Education
Stanton Wortham p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p37
A Historical Appraisal of Clicks: A Linguistic and Genetic Population
Perspective
Tom Güldemann and Mark Stoneking p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p93
vii
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Linguistic Diversity in the Caucasus
Bernard Comrie p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 131
Evolutionary Linguistics
William Croft p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 219
Annu. Rev. Anthropol. 2008.37:267-282. Downloaded from www.annualreviews.org
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Reproduction and Preservation of Linguistic Knowledge: Linguistics’
Response to Language Endangerment
Nikolaus P. Himmelmann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 337
Sociocultural Anthropology
Evolutionary Perspectives on Religion
Pascal Boyer and Brian Bergstrom p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 111
Reproduction and Inheritance: Goody Revisited
Chris Hann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 145
Assisted Reproductive Technologies and Culture Change
Marcia C. Inhorn and Daphna Birenbaum-Carmeli p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177
Post-Post-Transition Theories: Walking on Multiple Paths
Manduhai Buyandelgeriyn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 235
From Resilience to Resistance: Political Ecological Lessons from
Antibiotic and Pesticide Resistance
Kathryn M. Orzech and Mark Nichter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 267
Violence, Gender, and Subjectivity
Veena Das p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 283
Demographic Transitions and Modernity
Jennifer Johnson-Hanks p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 301
The Anthropology of Crime and Criminalization
Jane Schneider and Peter Schneider p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 351
Alternative Kinship, Marriage, and Reproduction
Nancy E. Levine p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375
Theme 1: Evolution in Anthropology
Evolutionary Models of Women’s Reproductive Functioning
Virginia J. Vitzthum p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p53
Evolution in Archaeology
Stephen Shennan p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p75
viii
Contents
AR355-FM
ARI
14 August 2008
14:6
A Historical Appraisal of Clicks: A Linguistic and Genetic Population
Perspective
Tom Güldemann and Mark Stoneking p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p93
Annu. Rev. Anthropol. 2008.37:267-282. Downloaded from www.annualreviews.org
Access provided by RENSSELAER POLYTECHNIC INSTITUTE on 06/10/16. For personal use only.
Evolutionary Perspectives on Religion
Pascal Boyer and Brian Bergstrom p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 111
Detecting the Genetic Signature of Natural Selection in Human
Populations: Models, Methods, and Data
Angela M. Hancock and Anna Di Rienzo p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 197
Evolutionary Linguistics
William Croft p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 219
Post-Post-Transition Theories: Walking on Multiple Paths
Manduhai Buyandelgeriyn p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 235
The Archaeological Evidence for Social Evolution
Joyce Marcus p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 251
From Resilience to Resistance: Political Ecological Lessons from
Antibiotic and Pesticide Resistance
Kathryn M. Orzech and Mark Nichter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 267
Theme 2: Reproduction
The Effects of Kin on Primate Life Histories
Karen B. Strier p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p21
Reproduction and Inheritance: Goody Revisited
Chris Hann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 145
The Archaeology of Childhood
Jane Eva Baxter p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 159
Assisted Reproductive Technologies and Culture Change
Marcia C. Inhorn and Daphna Birenbaum-Carmeli p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 177
Demographic Transitions and Modernity
Jennifer Johnson-Hanks p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 301
Sexuality Studies in Archaeology
Barbara L. Voss p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 317
Reproduction and Preservation of Linguistic Knowledge: Linguistics’
Response to Language Endangerment
Nikolaus P. Himmelmann p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 337
Alternative Kinship, Marriage, and Reproduction
Nancy E. Levine p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p p 375
Contents
ix