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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. ANNUAL REVIEWS Further Click here for quick links to Annual Reviews content online, including: • Other articles in this volume • Top cited articles • Top downloaded articles • Our comprehensive search 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 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. 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 · Nichter 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 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. 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 www.annualreviews.org • Antibiotic and Pesticide Resistance 269 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. 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). 270 Orzech · Nichter 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). 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. 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 www.annualreviews.org • Antibiotic and Pesticide Resistance 271 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. 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- 272 Orzech · Nichter 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). 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. 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 www.annualreviews.org • Antibiotic and Pesticide Resistance 273 Table 2 Biological solutionsa Solution Methods to achieve solution 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. 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 274 Orzech · Nichter 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 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. 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). www.annualreviews.org • Antibiotic and Pesticide Resistance 275 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. 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 Orzech · Nichter 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 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. 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. www.annualreviews.org • Antibiotic and Pesticide Resistance 277 DISCLOSURE STATEMENT 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. 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. LITERATURE CITED 2000. Changing prescriber behaviour: Training and treatment guidelines improve prescribing in Uganda. Essent. Drugs Monit. 28/29:15, http://mednet2.who.int/edmonitor/edition/EDM2829en.pdf Aaby P. 1995. Assumptions and contradictions in measles and measles immunization research: Is measles good for something? Soc. Sci. Med. 41:673–86 Abellanosa I, Nichter M. 1996. 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Downloaded from www.annualreviews.org Access provided by RENSSELAER POLYTECHNIC INSTITUTE on 06/10/16. For personal use only. 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 Access provided by RENSSELAER POLYTECHNIC INSTITUTE on 06/10/16. For personal use only. 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 ARI 14 August 2008 14:6 Annual Review of Anthropology 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. 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 AR355-FM ARI 14 August 2008 14:6 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 Access provided by RENSSELAER POLYTECHNIC INSTITUTE on 06/10/16. For personal use only. 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