Brief Communication October 2017 | Volume 125 | Issue 10
Small-Scale Food Animal Production and Antimicrobial Resistance: Mountain, Molehill, or Something in-between?
1Public Health Institute, Oakland, California, USA
2Department of Epidemiology, University of Michigan, Ann Arbor, Michigan, USA
3Instituto de Microbiologia, Colegio de Ciencias Biologicas y Ambientales, Universidad San Francisco de Quito, Quito, Ecuador
4Department of Epidemiology and Biostatistics, Michigan State University, East Lansing, Michigan, USA
5Department of Microbiology and Molecular Genetics, Michigan State University, East Lansing, Michigan, USA
6Department of Veterinary and Biomedical Sciences, University of Minnesota, St. Paul, Minnesota, USA
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- Small-scale food animal production is widely practiced around the globe, yet it is often overlooked in terms of the environmental health risks. Evidence suggests that small-scale food animal producers often employ the use of antimicrobials to improve the survival and growth of their animals, and that this practice leads to the development of antimicrobial resistance (AMR) that can potentially spread to humans. The nature of human–animal interactions in small-scale food animal production systems, generally practiced in and around the home, likely augments spillover events of AMR into the community on a scale that is currently unrecognized and deserves greater attention. https://doi.org/10.1289/EHP2116
Received: 27 April 2017
Revised: 05 September 2017
Accepted: 14 September 2017
Published: 16 October 2017
Address correspondence to J.P. Graham, 555 12th Street, 10th Floor, Oakland, CA 94607 USA. Telephone: (510) 285-5537. Email: Jay.Graham@phi.org
The authors declare they have no actual or potential competing financial interests.
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Small-scale food animal production is increasingly practiced throughout the world (Moges et al. 2010; Okeno et al. 2012; Robinson et al. 2014). Evidence suggests that small-scale food animal production can provide households with a means to reduce poverty, reduce food insecurity, and improve gender equity, especially in low- and middle-income countries (LMICs) (Herrero et al. 2014; Iannotti et al. 2014; Kafle 2014; Kristjanson et al. 2014; Leroy and Frongillo 2007; Miller et al. 2014). It is estimated that more than 80% of the chicken population worldwide occurs in small-scale production systems, producing up to 90% of the total poultry products in many LMICs (Mack et al. 2005). Of growing concern, however, is that small-scale food animals are often reported to receive antimicrobials to enhance their survival and growth. Although current information is insufficient to estimate the scale of unregulated antimicrobial use in the sector, this use appears to be common and creates a tension between development programs and public health.
To date, studies linking antimicrobial resistance (AMR) in humans with antimicrobial use in food animals has largely focused on commercial-scale production systems (Silbergeld et al. 2008). In these settings where animals are intensively raised, studies have shown that the intestinal microbiota of food animals can be a source of AMR in workers and humans living near the operations (Rinsky et al. 2013; Seiffert et al. 2013; Smith 2015). Small-scale systems can differ from commercial confinement operations in ways that may affect the transmission of AMR from animals to humans. In large commercial-scale production, the primary risk is likely associated with direct exposure of workers to animal feces, as well as consumer exposures to contaminated meat and poultry products that can be widely disseminated (Gieraltowski et al. 2016; Nordstrom et al. 2013; Wardyn et al. 2015). In small-scale systems that typically raise animals at lower density within the household environment, we suggest that the primary transmission pathways are environmental exposures that include direct contact with live animals and their wastes, especially among young children. For example, studies of young children in rural Zimbabwe and Bangladesh identified the ingestion of animal feces as an important route of childhood exposures to animal feces (Ngure et al. 2013). These environmental exposures increase the potential for spillover events; that is, they create situations where zoonotic microbiota, including drug-resistant bacteria and AMR genes, may spread to humans.
Here we report existing evidence on the use of antimicrobials in small-scale food animal production, which we hypothesize represents an important yet underappreciated reservoir of AMR. Additionally, because of the nature of human–animal interactions in these systems—often occurring in and around the home—the potential for spillover of AMR into the community may occur at a greater scale than is currently recognized (Figure 1).
Antimicrobial Use in Small-Scale Food Animals
In LMICs, antimicrobials are often available over the counter in animal agriculture shops (Katakweba et al. 2012). The practice of using antimicrobials in small-scale food animal production—whether for growth promotion, disease prevention, or disease treatment—has been documented in a diverse set of studies within LMICs (Andoh et al. 2016; Braykov et al. 2016; Katakweba et al. 2012; Lowenstein et al. 2016; Nguyen et al. 2015; Nonga et al. 2010; Roess et al. 2013) (Table 1). In rural Ecuador, for example, small-scale poultry farmers report that they regularly administer antimicrobials, including drugs from six different antimicrobial classes (Braykov et al. 2016). In southwestern Nigeria, a study of veterinary pharmacy shops found that tetracyclines, fluoroquinolones, and beta-lactams/aminoglycosides constituted the majority of antimicrobials used among small- to medium-scale food animal operations (Adesokan et al. 2015). In other studies of small- to medium-scale food animal operations, in Tanzania and Ghana, for example, researchers have documented the regular use of antimicrobials (Andoh et al. 2016; Nonga et al. 2010). Nguyen et al. (2015) have highlighted significant variability in the antimicrobial classes used in small food animal operations and have emphasized the potential for multidrug resistance to develop and be amplified. There is little information, however, regarding the doses or duration of antimicrobial use, further restricting the ability to assess the risks of AMR development within these operations. It is likely that households engaged in small-scale food animal production lack access to the necessary veterinary technical assistance required to appropriately determine antibiotic selection, dose, and duration. Future interventions that aim to reduce the misuse of antimicrobials in small-scale livestock may need to target veterinary pharmacy shops, an approach that has been used in human medicine to reduce misuse of drugs available over the counter (Chalker et al. 2005).
|Reference||Country||Setting||Animals studied||Scale of operations studied||Findings|
|Braykov et al. 2016||Ecuador||Rural||Chickens||Small to mediuma||Farmers reported using penicillin plus streptomycin, tetracycline, sulfonamide, sulfamethazine plus trimethoprim, piperacillin, erythromycin, sulbactam, and/or enrofloxacin. Sixteen of 20 farmers reported supplementation with antibiotics beyond what is already available in feed.|
|Katakweba et al. 2012||Tanzania||Rural||Mixed||Small to large||The most commonly reported antibiotics used were tetracycline, sulphadimidines, and penicillin-streptomycin and these were present at the farms. Livestock keepers gathered advice on antimicrobial use from veterinarians, sales shop agents, extension agents, or in some cases received no consultation.|
|Nonga et al. 2010||Tanzania||Rural||Chickens||Small (n=19) to medium (n=1)b||All farmers reported using drugs to either treat or prevent occurrence of diseases in their birds. Two-thirds (65%) of the farmers reported treating their chickens themselves after getting advice from the sales shop agents. A range of 10 different antimicrobials were used among the 20 farms; sulfonamides were used on all farms.|
|Roess et al. 2013||Bangladesh||Rural||Chickens||Small||Most respondents reported to use antimicrobial drugs and could name them by using local terms or the brand name. The most commonly used antibiotic was oxytetracyline. Medicines used for household members were sometimes provided to animals, when their symptoms were similar to illnesses observed in humans.|
|Lowenstein et al. 2016||Ecuador||Peri-urban||Mixed||Small||In-depth interviews with small-scale food animal producers found that antibiotics were considered an important strategy for helping animals grow faster and preventing parasites, especially when the animals are young.|
|Ström et al. 2017||Thailand||Rural||Pigs||Smallc (n=25) and medium (n=27)||All farms administered antimicrobials to their pigs. Small-scale farmers made decisions on when to administer antimicrobials and made purchases at local shops. Medium-scale farmers discussed antimicrobial treatment with a veterinarian. Medium-scale farms used a greater diversity of antimicrobials than small-scale farms.|
|Andoh et al. 2016||Ghana||Rural||Chickens||Mediumd||All 75 poultry keepers reported providing antimicrobials to their poultry based on advice of veterinarians and shop sales agents. The most common drugs used included oxytetracycline, penicillin, tylosin, ciprofloxacin, erythromycin, enrofloxacin, streptomycin, doxycycline, trimethoprim-sulfadozine, and neomycin. None of the 75 poultry keepers complied with withdrawal periods indicated on product labels.|
|Rugumisa et al. 2016||Tanzania||Rural||Chickens||Smalle||Chickens were generally provided feed and water that may contain antibiotics, including tetracycline, enrofloxacin, and sulfa-trimethoprim.|
|Nguyen et al. 2015||Vietnam||Rural||Chickens||Household chickens (n=104) to Small chicken farms (n=104)f||Household chickens and chickens from small farms were commonly fed antibiotics, including tetracyclines, macrolides, penicillins, and polymyxins.|
aThe range varied from high intensity (>500 chickens) to medium intensity (150–500 chickens) to low intensity (<150 chickens).
bThe range varied from 30 to 4,820 chickens. Nineteen of the 20 farms studied had <500 chickens.
cSmall farms had a maximum of 20 pigs, whereas medium-scale farms were defined as farms with 100–500 pigs.
dThis study included chicken farms with ≤1,000 chickens (n=15), 1,001–2,000 chickens (n=16), 2,001–4,000 chickens (n=17), and >4,000 chickens (n=26).
eIn this study, small was characterized as <200 chickens.
fHousehold chickens had 10–200 chickens and small chicken farms had 200–2,000 chickens.
Driving Factors for Antimicrobial Use in Small-Scale Food Animal Production
In Ghana, the stated drivers for using antimicrobials in poultry production—mainly prevention and treatment of diseases—did not vary significantly between small-scale and commercial-scale operations (Andoh et al. 2016). Nearly half of producers interviewed in a study in Ecuador perceived the use of antibiotics as an important strategy for helping animals grow faster and preventing disease, especially when the animals are young (Lowenstein et al. 2016). According to Lowenstein et al. (2016), one producer noted that the use of antimicrobials in animal feed is especially important when animals are raised indoors, “The [feed we use] has antibiotics, vitamins. Because of that the animals grow faster. We use medicines more because we raise them inside, because otherwise they die. The animals that are in the fields do not get sick.” A few study respondents claimed that their animals rarely get sick and credited antimicrobials with animal health (Lowenstein et al. 2016). At the same time, there is evidence that many producers have a limited understanding of AMR. None of the small-scale food animal producers mentioned above knew of specific health risks for themselves or their children related to drug-resistant infections, although many shared the perception that eating animals that had been raised with too many antibiotics could be harmful to health (Lowenstein et al. 2016). Research suggests that the fundamental driver for antimicrobial use in this sector is likely rooted in the intensification of food animal production that is increasing globally (Jones et al. 2013; Wiethoelter et al. 2015).
AMR in Small-Scale Food Animals
In a study of AMR comparing two types of small-scale poultry production systems, Braykov et al. (2016) found a higher prevalence of drug-resistant Escherichia coli (i.e., tetracycline and amoxicillin-clavulanic acid resistance) in household production chickens versus free-range chickens. In this study, production chickens were defined as a nonlocal breed that is designed to grow larger; these birds were generally raised in confinement and were raised to be sold, rather than for household consumption. The study highlighted that management practices for production-oriented chickens may result in more antimicrobial use to enhance their survival and growth (Braykov et al. 2016). Researchers in Ghana identified nearly a quarter of Salmonella isolates (24%) from poultry raised in small-scale settings that were resistant to four or more antimicrobials (Andoh et al. 2016). Further, a study of chicken fecal samples and milk samples from dairy cows in small- to medium-scale operations in Odisha, India, identified ESBL (extended-spectrum beta lactamase)-producing E. coli in 18 of 305 of the samples screened (5.9%) (Kar et al. 2015).
Spillover of AMR from Small-Scale Food Animals to Humans
Research has demonstrated spillover of zoonotic enteric pathogens into the household environment from small-scale food animals. Examples include atypical enteropathogenic E. coli (Vasco et al. 2016), Campylobacter spp. (El-Tras et al. 2015; Harvey et al. 2003; Vasco et al. 2016), and Giardia and Cryptosporidium (Berrilli et al. 2012). Transmission of zoonotic pathogens underscores that proximity to domestic food animals could also potentially increase the risk of AMR transmission if food animals are carrying drug-resistant bacteria. There are a large number of studies on the spillover of AMR between industrial food animals and humans (de Been et al. 2014; Huijbers et al. 2014; Seiffert et al. 2013; Silbergeld et al. 2008; van Hoek et al. 2016). Very few studies, however, have been conducted with small-scale operations, which are common in LMICs, but also increasingly common in high-income countries (Tobin et al. 2015). In a small study of the resistome (i.e., all the resistance determinants present in the gut) of household members, in Peru and Panama, which included 263 fecal samples from 115 individuals in 27 houses and 209 environmental samples, researchers identified chicken feces as an important source of AMR genes and that, on average, human fecal and chicken coop soil resistomes shared 10 antibiotic resistance-encoding proteins (Pehrsson et al. 2016). A study in Ecuador found an elevated risk of carrying resistance determinants (e.g., integrons) among households raising production chickens, described above, compared with households without chicken production operations (Moser et al. 2017).
Antimicrobial resistance is a major global health threat that is linked to antimicrobial use in both clinical and community settings (Finley et al. 2013). The attributable fraction of AMR due to antimicrobial use within agricultural systems is unknown, and within that, how much is due to small-scale food animal production is even less clear. Small-scale food animal production is an important livelihood that has the potential to improve the economy of households and communities (Gates 2016). Given their importance and the potential growth of this livelihood, there is a critical need to better understand the fraction of AMR in humans that is due to antimicrobial use in food animal production, specifically across the range of systems—from backyard to larger-scale operations. On one hand, antimicrobial use in large-scale operations is quantitatively large and exposures to AMR, due to food distribution systems, are likely to be global (Thornton 2010). On the other hand, antimicrobial use in small-scale systems generally occurs within the household environment in LMIC settings; these settings often result in intimate human–animal exposures as well as poor water, sanitation, and hygiene conditions, both of which may enhance AMR spread (Wuijts et al. 2017). Understanding the impact of small-scale food animals on AMR transmission will require better characterizations of the quantity and classes of antimicrobials used in different scales of production systems and the prevalence of specific types of AMR. There is also a need to clarify how different food animal species and management practices are associated with the spillover of AMR from small-scale food animals to human microbiota (Landers et al. 2012). A variety of actions will be needed to change the behaviors of antimicrobial producers, sales agents, farmers, and consumers (Chalker et al. 2005; Ferreira and Staerk 2017; Rojo-Gimeno et al. 2016). Moving forward, a supportive environment will be needed that includes regulations controlling use, improved systems for monitoring use, and financial incentives in tandem with programs that aim to improve farmers’ knowledge, attitudes, and practices (Lhermie et al. 2016).
Increasing the production of food animals can be an important contributor to food security and the resilience and productivity of people’s livelihoods; yet, at the same time, there is an understanding that if food animals are not carefully managed, adverse consequences can ensue. Ensuring that food animal production systems fully benefit the poor and do not further drive the spread of AMR is of critical importance to public health.
This research was supported by the Fogarty International Center of the National Institutes of Health under award K01 TW 009484, and by the National Science Foundation under award R0811934. The funders had no role in the research or the decision to submit the work for publication.
Adesokan HK, Akanbi IO, Akanbi IM, Obaweda RA. 2015. Pattern of antimicrobial usage in livestock animals in south-western Nigeria: the need for alternative plans. Onderstepoort J Vet Res 82(1):1–6, PMID: 26016985, 10.4102/ojvr.v82i1.816.
Andoh L, Dalsgaard A, Obiri-Danso K, Newman MJ, Barco L, Olsen JE. 2016. Prevalence and antimicrobial resistance of Salmonella serovars isolated from poultry in Ghana. Epidemiol Infect 144(15):3288–3299, PMID: 27334298, 10.1017/S0950268816001126.
Berrilli F, D’Alfonso R, Giangaspero A, Marangi M, Brandonisio O, Kaboré Y, et al. 2012. Giardia duodenalis genotypes and Cryptosporidium species in humans and domestic animals in Côte d’Ivoire: occurrence and evidence for environmental contamination. Trans R Soc Trop Med Hyg 106(3):191–195, PMID: 22265078, 10.1016/j.trstmh.2011.12.005.
Braykov NP, Eisenberg JN, Grossman M, Zhang L, Vasco K, Cevallos W, et al. 2016. Antibiotic resistance in animal and environmental samples associated with small-scale poultry farming in northwestern Ecuador. mSphere 1(1):e00021-15, PMID: 27303705, 10.1128/mSphere.00021-15.
Chalker J, Ratanawijitrasin S, Chuc N, Petzold M, Tomson G. 2005. Effectiveness of a multi-component intervention on dispensing practices at private pharmacies in Vietnam and Thailand—a randomized controlled trial. Soc Sci Med 60(1):131–141, PMID: 15482873, 10.1016/j.socscimed.2004.04.019.
de Been M, Lanza VF, de Toro M, Scharringa J, Dohmen W, Du Y, et al. 2014. Dissemination of cephalosporin resistance genes between Escherichia coli strains from farm animals and humans by specific plasmid lineages. PLoS Genet 10(12):e1004776, PMID: 25522320, 10.1371/journal.pgen.1004776.
El-Tras WF, Holt H, Tayel A, El-Kady N. 2015. Campylobacter infections in children exposed to infected backyard poultry in Egypt. Epidemiol Infect 143(2):308–315, PMID: 24774694, 10.1017/S095026881400096X.
Finley RL, Collignon P, Larsson DG, McEwen SA, Li XZ, Gaze WH, et al. 2013. The scourge of antibiotic resistance: the important role of the environment. Clin Infect Dis 57(5):704–710, PMID: 23723195, 10.1093/cid/cit355.
Gates B. 2016. Why I Would Raise Chickens. https://www.Gatesnotes.Com/development/why-i-would-raise-chickens [accessed 12 April 2017].
Gieraltowski L, Higa J, Peralta V, Green A, Schwensohn C, Rosen H, et al. 2016. National outbreak of multidrug resistant Salmonella heidelberg infections linked to a single poultry company. PloS One 11(9):e0162369, PMID: 27631492, 10.1371/journal.pone.0162369.
Harvey SA, Winch PJ, Leontsini E, Torres Gayoso CT, López Romero SL, Gilman RH, et al. 2003. Domestic poultry-raising practices in a Peruvian shantytown: implications for control of Campylobacter jejuni-associated diarrhea. Acta Trop 86(1):41–54, PMID: 12711102, 10.1016/S0001-706X(03)00006-8.
Herrero M, Havlik P, McIntire J, Palazzo A, Valin H. 2014. “African livestock futures: realizing the potential of livestock for food security, poverty reduction and the environment in Sub-Saharan Africa.” Geneva, Switzerland:Office of the Special Representative of the UN Secretary General for Food Security and Nutrition and the United Nations System Influenza Coordination. https://cgspace.cgiar.org/bitstream/handle/10568/41908/Livestock_Report_en.pdf?sequence=3&isAllowed=y [accessed 12 April 2017].
Huijbers PM, Graat EA, Haenen AP, van Santen MG, van Essen-Zandbergen A, Mevius DJ, et al. 2014. Extended-spectrum and AmpC β-lactamase-producing Escherichia coli in broilers and people living and/or working on broiler farms: prevalence, risk factors and molecular characteristics. J Antimicrob Chemother 69(10):2669–2675, PMID: 24879667, 10.1093/jac/dku178.
Iannotti LL, Lutter CK, Bunn DA, Stewart CP. 2014. Eggs: the uncracked potential for improving maternal and young child nutrition among the world’s poor. Nutr Rev 72(6):355–368, PMID: 24807641, 10.1111/nure.12107.
Jones BA, Grace D, Kock R, Alonso S, Rushton J, Said MY, et al. 2013. Zoonosis emergence linked to agricultural intensification and environmental change. Proc Natl Acad Sci U S A 110(21):8399–8404, PMID: 23671097, 10.1073/pnas.1208059110.
Kafle KR. 2014. Is there more than milk? The impact of Heifer International’s livestock donation program on rural livelihoods: preliminary findings from a field experiment in Zambia. In: Proceedings of the 2014 Annual Meeting of the Agricultural and Applied Economics Association, 27–29 July 2014, Milwaukee, WI:Agricultural and Applied Economics Association.
Kar D, Bandyopadhyay S, Bhattacharyya D, Samanta I, Mahanti A, Nanda PK, et al. 2015. Molecular and phylogenetic characterization of multidrug resistant extended spectrum beta-lactamase producing Escherichia coli isolated from poultry and cattle in Odisha, India. Infect Genet Evol 29:82–90, PMID: 25445661, 10.1016/j.meegid.2014.11.003.
Katakweba AAS, Mtambo MMA, Olsen JE, Muhairwa AP. 2012. Awareness of human health risks associated with the use of antibiotics among livestock keepers and factors that contribute to selection of antibiotic resistance bacteria within livestock in Tanzania. Livestock Res Rural Dev 24:170.
Kristjanson P, Waters-Bayer A, Johnson N, Tipilda A, Njuki J, Baltenweck I, et al. 2014. Livestock and women’s livelihoods. In: Gender in Agriculture. Quisumbing A, Meinzen-Dick R, Raney T, Croppenstedt A, Behrman J, Peterman A, eds. Dordrecht, Netherlands:Springer, 209–233.
Landers TF, Cohen B, Wittum TE, Larson EL. 2012. A review of antibiotic use in food animals: perspective, policy, and potential. Public Health Rep 127(1):4–22, PMID: 22298919, 10.1177/003335491212700103.
Leroy JL, Frongillo EA. 2007. Can interventions to promote animal production ameliorate undernutrition? J Nutr 137(10):2311–2316, PMID: 17885016.
Lhermie G, Gröhn YT, Raboisson D. 2016. Addressing antimicrobial resistance: an overview of priority actions to prevent suboptimal antimicrobial use in food-animal production. Front Microbiol 7:2114, PMID: 28111568, 10.3389/fmicb.2016.02114.
Lowenstein C, Waters WF, Roess A, Leibler JH, Graham JP. 2016. Animal husbandry practices and perceptions of zoonotic infectious disease risks among livestock keepers in a rural parish of Quito, Ecuador. Am J Trop Med Hyg 95(6):450–1458, PMID: 27928092, 10.4269/ajtmh.16-0485.
Mack S, Hoffmann D, Otte J. 2005. The contribution of poultry to rural development. Worlds Poult Sci J 61(01):7–14, 10.1079/WPS200436.
Miller LC, Joshi N, Lohani M, Rogers B, Loraditch M, Houser R. 2014. Community development and livestock promotion in rural Nepal: effects on child growth and health. Food Nutr Bull 35(3):312–326, PMID: 25902591, 10.1177/156482651403500304.
Moges F, Tegegne A, Dessie T. 2010. “Indigenous chicken production and marketing systems in Ethiopia: characteristics and opportunities for market-oriented development.” Working Paper No. 24. IPMS (Improving Productivity and Market Success) of Ethiopian Farmers Project Working Paper 24. Nairobi, Kenya:International Livestock Research Institute (ILRI). https://cgspace.cgiar.org/bitstream/handle/10568/2685/WorkingPaper_24.pdf?sequence=4&isAllowed=y [accessed 12 April 2017].
Moser KA, Zhang L, Spicknall I, Braykov NP, Levey K, Marrs CF, et al. 2017. The role of mobile genetic elements in the spread of antimicrobial resistant Escherichia coli from chickens to humans in small-scale production poultry operations in rural Ecuador. Am J Epidemiol, 10.1093/aje/kwx286.
Ngure FM, Humphrey JH, Mbuya MNN, Majo F, Mutasa K, Govha M, et al. 2013. Formative research on hygiene behaviors and geophagy among infants and young children and implications of exposure to fecal bacteria. Am J Trop Med Hyg 89(4):709–716, PMID: 24002485, 10.4269/ajtmh.12-0568.
Nguyen VT, Carrique-Mas JJ, Ngo TH, Ho HM, Ha TT, Campbell JI, et al. 2015. Prevalence and risk factors for carriage of antimicrobial-resistant Escherichia coli on household and small-scale chicken farms in the Mekong Delta of Vietnam. J Antimicrob Chemother 70(7):2144–2152, PMID: 25755000, 10.1093/jac/dkv053.
Nonga H, Simon C, Karimuribo E, Mdegela R. 2010. Assessment of antimicrobial usage and residues in commercial chicken eggs from smallholder poultry keepers in Morogoro municipality, Tanzania. Zoonoses Public Health 57(5):339–344, PMID: 19486498, 10.1111/j.1863-2378.2008.01226.x.
Pehrsson EC, Tsukayama P, Patel S, Mejía-Bautista M, Sosa-Soto G, Navarrete KM, et al. 2016. Interconnected microbiomes and resistomes in low-income human habitats. Nature 533(7602):212–216, PMID: 27172044, 10.1038/nature17672.
Rinsky JL, Nadimpalli M, Wing S, Hall D, Baron D, Price LB, et al. 2013. Livestock-associated methicillin and multidrug resistant Staphylococcus aureus is present among industrial, not antibiotic-free livestock operation workers in North Carolina. PLoS One 8(7):e67641, PMID: 23844044, 10.1371/journal.pone.0067641.
Roess AA, Winch PJ, Ali NA, Akhter A, Afroz D, El Arifeen S, et al. 2013. Animal husbandry practices in rural Bangladesh: potential risk factors for antimicrobial drug resistance and emerging diseases. Am J Trop Med Hyg 89(5):965–970, PMID: 24062478, 10.4269/ajtmh.12-0713.
Rojo-Gimeno C, Postma M, Dewulf J, Hogeveen H, Lauwers L, Wauters E. 2016. Farm-economic analysis of reducing antimicrobial use whilst adopting improved management strategies on farrow-to-finish pig farms. Prev Vet Med 129:74–87, PMID: 27317325, 10.1016/j.prevetmed.2016.05.001.
Rugumisa BT, Call DR, Mwanyika GO, Subbiah M, Buza J. 2016. Comparison of the prevalence of antibiotic-resistant Escherichia coli isolates from commercial-layer and free-range chickens in Arusha district, Tanzania. Afr J Microbiol Res 10(34):1422–1429, 10.5897/ajmr2016.8251.
Seiffert SN, Hilty M, Perreten V, Endimiani A. 2013. Extended-spectrum cephalosporin-resistant Gram-negative organisms in livestock: an emerging problem for human health? Drug Resist Updat 16(1–2):22–45, PMID: 23395305, 10.1016/j.drup.2012.12.001.
Silbergeld EK, Graham J, Price LB. 2008. Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health 29:151–169, PMID: 18348709, 10.1146/annurev.publhealth.29.020907.090904.
Ström G, Halje M, Karlsson D, Jiwakanon J, Pringle M, Fernström L-L, et al. 2017. Antimicrobial use and antimicrobial susceptibility in Escherichia coli on small- and medium-scale pig farms in north-eastern Thailand. Antimicrob Resist Infect Control 6:75, PMID: 28725421, 10.1186/s13756-017-0233-9.
Tobin MR, Goldshear JL, Price LB, Graham JP, Leibler JH. 2015. A framework to reduce infectious disease risk from urban poultry in the United States. Public Health Rep 130(4):380–391, PMID: 26346104, 10.1177/003335491513000417.
van Hoek AH, Stalenhoef JE, van Duijkeren E, Franz E. 2016. Comparative virulotyping of extended-spectrum cephalosporin-resistant E. coli isolated from broilers, humans on broiler farms and in the general population and UTI patients. Vet Microbiol 194:55–61, PMID: 27106522, 10.1016/j.vetmic.2016.04.008.
Vasco K, Graham JP, Trueba G. 2016. Detection of zoonotic enteropathogens in children and domestic animals in a semi-rural community in Ecuador. Appl Environ Microbiol 82(14):4218–4224, PMID: 27208122, 10.1128/AEM.00795-16.
Wardyn SE, Forshey BM, Farina SA, Kates AE, Nair R, Quick MK, et al. 2015. Swine farming is a risk factor for infection with and high prevalence of carriage of multidrug-resistant Staphylococcus aureus. Clin Infect Dis 61(1):59–66, PMID: 25931444, 10.1093/cid/civ234.
Wiethoelter AK, Beltrán-Alcrudo D, Kock R, Mor SM. 2015. Global trends in infectious diseases at the wildlife–livestock interface. Proc Natl Acad Sci U S A 112(31):9662–9667, PMID: 26195733, 10.1073/pnas.1422741112.
Wuijts S, van den Berg HH, Miller J, Abebe L, Sobsey M, Andremont A, et al. 2017. Towards a research agenda for water, sanitation and antimicrobial resistance. J Water Health 15(2):175–184, PMID: 28362299, 10.2166/wh.2017.124.
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