Risk of Antibiotic-Resistant Staphylococcus aureus Dispersion from Hog Farms: A Critical Review
Alexandra N. George
Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA
Search for more papers by this authorJill R. Stewart
Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA
Search for more papers by this authorJessica C. Evans
Department of Environmental and Occupational Health, School of Public Health, Indiana University, Bloomington, IN, USA
Search for more papers by this authorCorresponding Author
Jacqueline MacDonald Gibson
Department of Environmental and Occupational Health, School of Public Health, Indiana University, Bloomington, IN, USA
Address correspondence to Jacqueline MacDonald Gibson, Department of Environmental and Occupational Health, School of Public Health, Indiana University, 1025 East Seventh Street, Suite 025, Bloomington, IN 47405, USA; tel: 812-856-2448; jacmgibs@iu.edu
Search for more papers by this authorAlexandra N. George
Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA
Search for more papers by this authorJill R. Stewart
Department of Environmental Sciences and Engineering, Gillings School of Global Public Health, University of North Carolina, Chapel Hill, NC, USA
Search for more papers by this authorJessica C. Evans
Department of Environmental and Occupational Health, School of Public Health, Indiana University, Bloomington, IN, USA
Search for more papers by this authorCorresponding Author
Jacqueline MacDonald Gibson
Department of Environmental and Occupational Health, School of Public Health, Indiana University, Bloomington, IN, USA
Address correspondence to Jacqueline MacDonald Gibson, Department of Environmental and Occupational Health, School of Public Health, Indiana University, 1025 East Seventh Street, Suite 025, Bloomington, IN 47405, USA; tel: 812-856-2448; jacmgibs@iu.edu
Search for more papers by this authorAbstract
The World Health Organization has declared antibiotic resistance “one of the biggest threats to global health.” Mounting evidence suggests that antibiotic use in industrial-scale hog farming is contributing to the spread of antibiotic-resistant Staphylococcus aureus. To capture available evidence on these risks, we searched peer-reviewed studies published before June 2017 and conducted a meta-analysis of these studies’ estimates of the prevalence of swine-associated, antibiotic-resistant S. aureus in animals, humans, and the environment. The 166 relevant studies revealed consistent evidence of livestock-associated methicillin-resistant S. aureus (MRSA) in hog herds (55.3%) raised with antibiotics. MRSA prevalence was also substantial in slaughterhouse pigs (30.4%), industrial hog operation workers (24.4%), and veterinarians (16.8%). The prevalence of swine-associated, multidrug-resistant S. aureus (MDRSA)—with resistance to three or more antibiotics—is not as well documented. Nonetheless, sufficient studies were available to estimate MDRSA pooled prevalence in conventional hog operation workers (15.0%), workers’ household members (13.0%), and community members (5.37%). Evidence also suggests that antibiotic-resistant S. aureus can be present in air, soil, water, and household surface samples gathered in or near high-intensity hog operations. An important caveat is that prevalence estimates for humans reflect colonization, not active infection, and the health risks of colonization remain poorly understood. In addition, these pooled results may not represent risks in specific locations, due to wide geographic variation. Nonetheless, these results underscore the need for additional preventive action to stem the spread of antibiotic-resistant pathogens from livestock operations and a streamlined reporting system to track this risk.
Supporting Information
| Filename | Description |
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| risa13495-sup-0001-SuppMat.pdf466.7 KB |
Table SI. Studies Included in This Review Table SII. Results of Meta-Analysis of MRSA and MDRSA Prevalence in Various Reservoirs Table SIII. Reservoirs with Fewer Than Three Studies Included in This Review Table SIV. Papers Included in Qualitative Synthesis |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Alt, K., Fetsch, A., Schroeter, A., Guerra, B., Hammerl, J. A., Hertwig, S., … Tenhagen, B. A. (2011). Factors associated with the occurrence of MRSA CC398 in herds of fattening pigs in Germany. BMC Veterinary Research, 7, 69. https://doi.org/10.1186/1746-6148-7-69
- Becker, K., Ballhausen, B., Kahl, B. C., & Köck, R. (2017). The clinical impact of livestock-associated methicillin-resistant Staphylococcus aureus of the clonal complex 398 for humans. Veterinary Microbiology, 200, 33–38. https://doi.org/10.1016/j.vetmic.2015.11.013
- Boost, M., Ho, J., Guardabassi, L., & O.Donoghue, M (2013). Colonization of butchers with livestock-associated methicillin-resistant staphylococcus aureus. Zoonoses and Public Health, 60(8), 572–576.
- Bos, M. E. H., Verstappen, K. M., van Cleef, B. A. G. L., Dohmen, W., Dorado-García, A., Graveland, H., … Heederik, D. J. J. (2016). Transmission through air as a possible route of exposure for MRSA. Journal of Exposure Science and Environmental Epidemiology, 26(3), 263–269. https://doi.org/10.1038/jes.2014.85
- Broens, E. M., Graat, E. A. M., Van Der Wolf, P. J., Van De Giessen, A. W., & De Jong, M. C. M. (2011). Prevalence and risk factor analysis of livestock associated MRSA-positive pig herds in The Netherlands. Preventive Veterinary Medicine, 102(1), 41–49. https://doi.org/10.1016/j.prevetmed.2011.06.005
- Broens, E. M., Graat, E. A. M., Van der Wolf, P. J., Van de Giessen, A. W., Van Duijkeren, E., Wagenaar, J. A., … de Jong, M. C. M. (2011). MRSA CC398 in the pig production chain. Preventive Veterinary Medicine, 98(2–3), 182–189. https://doi.org/10.1016/j.prevetmed.2010.10.010
- CDC. (2013). Antibiotic resistance threats in the United States, 2013. Current, 114, Retrieved fromhttps://doi.org/10.CS239559-B
- Chuang, Y. Y., & Huang, Y. C. (2015). Livestock-associated methicillin-resistant Staphylococcus aureus in Asia: An emerging issue? International Journal of Antimicrobial Agents, 45(4), 334–340. https://doi.org/10.1016/j.ijantimicag.2014.12.007
- Conly, J. M. (2004). Antimicrobial resistance—Judicious use is the key. The Canadian Journal of Infectious Diseases & Medical Microbiology(Journal Canadien Des Maladies Infectieuses et de La Microbiologie Medicale/AMMI Canada), 15(5), 249–251.
- Cook, T. D., Cooper, H., Cordray, D. S., Hartmann, H., Hedges, L. V., Light, R. J., … Mosteller, F. (1992). Meta-analysis for explanation: A casebook. Russell: Sage Foundation.
- Cox, L. A. T., & Popken, D. A. (2014). Quantitative assessment of human MRSA risks from Swine. Risk Analysis, 34(9), 1639–1650. https://doi.org/10.1111/risa.12255
- Davies, J., & Davies, D. (2010). Origins and evolution of antibiotic resistance. Microbiology and Molecular Biology Reviews, 74(3), 417–433. https://doi.org/10.1128/MMBR.00016-10
- Davis, K. A., Stewart, J. J., Crouch, H. K., Florez, C. E., & Hospenthal, D. R. (2004). Methicillin-resistant Staphylococcus aureus (MRSA) nares colonization at hospital admission and its effect on subsequent MRSA infection. Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 39(6), 776–782. https://doi.org/10.1086/422997
- Denis, O., Suetens, C., Hallin, M., Catry, B., Ramboer, I., Dispas, M., … Struelens, M. J. (2009), Methicillin-resistant staphylococcus aureus ST398 in swine farm personnel, Belgium. Emerging Infectious Diseases, 15(7), 1098–1101.
- Deiters, C., Günnewig, V., Friedrich, A. W., Mellmann, A., & Köck, R. (2015). Are cases of methicillin-resistant Staphylococcus aureus clonal complex (CC) 398 among humans still livestock-associated? International Journal of Medical Microbiology, 305(1), 110–113. https://doi.org/10.1016/j.ijmm.2014.11.007
- Donham, K. J. (2010). Community and occupational health concerns in pork production: A review. Journal of Animal Science, 88(13 Suppl), 102–111. https://doi.org/10.2527/jas.2009-2554
- Dorado-García, A., Dohmen, W., Bos, M. E. H., Verstappen, K. M., Houben, M., Wagenaar, J. A., & Heederik, D. J. J. (2015). Dose-response relationship between antimicrobial drugs and livestock-associated MRSA in pig farming. Emerging Infectious Diseases, 21(6), 950. https://doi.org/10.3201/eid2106.140706
- Flodgren, G., Eccles, M. P., Shepperd, S., Scott, A., Parmelli, E., & Beyer, F. R. (2011). An overview of reviews evaluating the effectiveness of financial incentives in changing healthcare professional behaviours and patient outcomes. Cochrane Database of Systematic Reviews, 7(7), CD009255. https://doi.org/10.1002/14651858.CD009255
- Friedrich, A. W., Jurke, A., Schaumburg, F., Köck, R., Köksal, M., Mellmann, A., & Becker, K. (2013). Livestock-associated methicillin-resistant Staphylococcus aureus (MRSA) as causes of human infection and colonization in Germany. PLoS ONE, 8(2), e55040. https://doi.org/10.1371/journal.pone.0055040
- Garcia-Graells, C., van Cleef, B. A. G. L., Larsen, J., Denis, O., Skov, R., & Voss, A. (2013). Dynamic of livestock-associated methicillin-resistant Staphylococcus aureus CC398 in pig farm households: A pilot study. PLoS ONE, 8(5), 6–11. https://doi.org/10.1371/journal.pone.0065512
- Gerrard, M., Gibbons, F. X., & Bushman, B. J. (1996). Relation between perceived vulnerability to HIV and precautionary sexual behavior. Psychological Bulletin, 119(3), 390–409.
- Grave, K., Torren-Edo, J., & Mackay, D. (2010). Comparison of the sales of veterinary antibacterial agents between 10 European countries. Journal of Antimicrobial Chemotherapy, 65, 2037–2040. https://doi.org/10.1093/jac/dkq247
- Graveland, H., Duim, B., van Duijkeren, E., Heederik, D., & Wagenaar, J. A. (2011). Livestock-associated methicillin-resistant Staphylococcus aureus in animals and humans. International Journal of Medical Microbiology, 301(8), 630–634. https://doi.org/10.1016/j.ijmm.2011.09.004
- Hatcher, S. M., Myers, K. W., Heaney, C. D., Larsen, J., Hall, D., Miller, M. B., & Stewart, J. R. (2016). Occurrence of methicillin-resistant Staphylococcus aureus in surface waters near industrial hog operation spray fields. Science of the Total Environment, 565, 1028–1036. https://doi.org/10.1016/j.scitotenv.2016.05.083
- Hatcher, S. M., Rhodes, S. M., Stewart, J. R., Silbergeld, E., Pisanic, N., Larsen, J., … Heaney, C. D. (2017). The prevalence of antibiotic-resistant Staphylococcus aureus nasal carriage among industrial hog operation workers, community residents, and children living in their households: North Carolina, USA. Environmental Health Perspectives, 125(4), 560–569. https://doi.org/10.1289/EHP35
- Hölzel, L., Härter, M., Reese, C., & Kriston, L. (2011). Risk factors for chronic depression—A systematic review. Journal of Affective Disorders, 129(1–3), 1–13. https://doi.org/10.1016/j.jad.2010.03.025
- Kochanek, K., Murphy, S., Xu, J., & Tejada-Vera, B. (2014). Deaths: Final Data for 2014. National Vital Statistics Reports, 65(4), 1-122.
- Larsen, J., Petersen, A., Sørum, M., Stegger, M., Van Alphen, L., Valentiner-Branth, P., … Skov, R. L. (2015). Methicillin-resistant Staphylococcus aureus CC398 is an increasing cause of disease in people with no livestock contact in Denmark, 1999 to 2011. Eurosurveillance, 20(37). https://doi.org/10.2807/1560-7917.ES.2015.20.37.30021
- Lewis, J., & Pattanayak, S. (2012). Who adopts improved fuels and cookstoves? A systematic review. Environmental Health Perspectives, 120(5), 637–645. https://doi.org/10.1289/ehp.1104194
- Liu, W., Liu, Z., Yao, Z., Fan, Y., Ye, X., & Chen, S. (2015). The prevalence and influencing factors of methicillin-resistant Staphylococcus aureus carriage in people in contact with livestock: A systematic review. American Journal of Infection Control, 43(5), 469–475.
- Masclaux, F. G., Sakwinska, O., Charrière, N., Semaani, E., & Oppliger, A. (2013). Concentration of airborne staphylococcus aureus (MRSA and MSSA), total bacteria, and endotoxins in pig farms. Annals of Occupational Hygiene, 57(5), 550–557. https://doi.org/10.1093/annhyg/mes098
- Moher, D., & Liberati A. (2009). Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. Annals of Internal Medicine, 151(4), 264–269.
- Monaco, M., Pedroni, P., Sanchini, A., Bonomini, A., Indelicato, A., & Pantosti, A. (2013). Livestock-associated methicillin-resistant Staphylococcus aureus responsible for human colonization and infection in an area of Italy with high density of pig farming. BMC Infectious Diseases, 13(1), 258. https://doi.org/10.1186/1471-2334-13-258
- Mutters, N. T., Bieber, C. P., Hauck, C., Reiner, G., Malek, V., & Frank, U. (2016). Comparison of livestock-associated and health care–associated MRSA—genes, virulence, and resistance. Diagnostic Microbiology and Infectious Disease, 86(4), 417–421. https://doi.org/10.1016/j.diagmicrobio.2016.08.016
- Nadimpalli, M., Rinsky, J. L., Wing, S., Hall, D., Stewart, J., Larsen, J., … Heaney, C. D. (2015). Persistence of livestock-associated antibiotic-resistant Staphylococcus aureus among industrial hog operation workers in North Carolina over 14 days. Occupational and Environmental Medicine, 72(2), 90–99. https://doi.org/10.1136/oemed-2014-102095
- Nadimpalli, M., Stewart, J. R., Pierce, E., Pisanic, N., Love, D. C., Hall, D., … Heaney, C. D. (2016). Livestock-associated, antibiotic-resistant Staphylococcus aureus nasal carriage and recent skin and soft tissue infection among industrial HOG operation workers. PLoS ONE, 11(11), 1–16. https://doi.org/10.1371/journal.pone.0165713
- Neyeloff, J. L., Fuchs, S., & Moreira, B. L. (2012). Meta-analysis and forest plots using a Microsoft excel spreadsheet: Step-by-step guide focusing on descriptive data analysis. BMC Research Notes, 5(52). https://doi.org/10.1186/1756-0500-5-52.
- O'Brien, A. M., Hanson, B. M., Farina, S. A., Wu, J. Y., Simmering, J. E., Wardyn, S. E., … Smith, T. C. (2012). MRSA in conventional and alternative retail pork products. PLoS ONE, 7(1), 3–8. https://doi.org/10.1371/journal.pone.0030092
- Omland, Ø., & Homann, L. (2012). Occupational acquisition of methicillin-resistant Staphylococcus aureus in humans—A description of MRSA carrier and infected cases from the region of north jutland in Denmark. Annals of Agricultural and Environmental Medicine, 19(4), 637–640.
- Oppliger, A., Moreillon, P., Charrière, N., Giddey, M., Morisset, D., & Sakwinska, O. (2012). Antimicrobial resistance of Staphylococcus aureus strains acquired by pig farmers from pigs. Applied and Environmental Microbiology, 78(22), 8010–8014. https://doi.org/10.1128/AEM.01902-12
- Rinsky, J. L., Nadimpalli, M., Wing, S., Hall, D., Baron, D., Price, L. B., … Heaney, C. D. (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), 1–11.
- Sabtu, N., Enoch, D. A., & Brown, N. M. (2015). Antibiotic resistance: What, why, where, when and how? British Medical Bulletin, 116(1), 105–113. https://doi.org/10.1093/bmb/ldv041
- Safdar, N., & Bradley, E. A. (2008). The risk of infection after nasal colonization with Staphylococcus aureus. American Journal of Medicine, 121(4), 310–315. https://doi.org/10.1016/j.amjmed.2007.07.034
- Schulz, J., Friese, A., Klees, S., Tenhagen, B. A., Fetsch, A., Rösler, U., & Hartung, J. (2012). Longitudinal study of the contamination of air and of soil surfaces in the vicinity of pig barns by livestock-associated methicillin-resistant Staphylococcus aureus. Applied and Environmental Microbiology, 78(16), 5666–5671.
- Slifierz, M. J., Friendship, R. M., & Scott Weese, J. (2015). Methicillin-resistant Staphylococcus aureus in commercial swine herds is associated with disinfectant and zinc usage. Applied and Environmental Microbiology, 81(8), 2690–2695. https://doi.org/10.1128/AEM.00036-15
- Smith, T. C. (2015). Livestock-associated Staphylococcus aureus: The United States Experience. PLOS Pathogens, 11(2), e1004564. https://doi.org/10.1371/journal.ppat.1004564
- Smith, T. C., & Wardyn, S. E. (2015). Human Infections with Staphylococcus aureus CC398. Current Environmental Health Reports, 2(1), 41–51. https://doi.org/10.1007/s40572-014-0034-8
- Uhlemann, A.-C., DeLeo, F. R., McCarthy, A. J., Lipkin, W. I., Street, C., Porcella, S. F., … Hirschberg, D. L. (2012). Identification of a highly transmissible animal-independent Staphylococcus aureus ST398 clone with distinct genomic and cell adhesion properties. MBio, 3(2), e00027–12. https://doi.org/10.1128/mbio.00027-12
- USDA-NASS. (2015). Overview of the United States Hog Industry. Retrieved from https://www.nass.usda.gov/Publications/Todays_Reports/reports/hogsan09.pdf.
- Valentin-Domelier, A. S., Girard, M., Bertrand, X., Violette, J., François, P., Donnio, P. Y., … van der Mee-Marquet, N. (2011). Methicillin-susceptible ST398 Staphylococcus aureus responsible for bloodstream infections: An emerging human-adapted subclone? PLoS ONE, 6(12), e28369. https://doi.org/10.1371/journal.pone.0028369
- van de Sande-Bruinsma, N., Leverstein van Hall, M. A., Janssen, M., Nagtzaam, N., Leenders, S., de Greeff, S. C., & Schneeberger, P. M. (2015). Impact of livestock-associated MRSA in a hospital setting. Antimicrobial Resistance and Infection Control, 4(1), 11. https://doi.org/10.1186/s13756-015-0053-8
- van de Vijver, L. P. L., Tulinski, P., Bondt, N., Mevius, D., & Verwer, C. (2014). Prevalence and molecular characteristics of methicillin-resistant Staphylococcus aureus (MRSA) in organic pig herds in the Netherlands. Zoonoses and Public Health, 61(5), 338–345. https://doi.org/10.1111/zph.12076
- Van Rijen, M. M. L., Bosch, T., Verkade, E. J. M., Schouls, L., & Kluytmans, J. A. J. W. (2014). Livestock-associated MRSA carriage in patients without direct contact with livestock. PLoS ONE, 9(6), 2–7. https://doi.org/10.1371/journal.pone.0100294
- Vilamala, A., Puigoriol, E., Garcia-Nuñez, M., Reynaga, E., Navarro, M., Sabrià, M., … Torres, C. (2017). Clinical impact and prevalence of MRSA CC398 and differences between MRSA-TetR and MRSA-TetS in an area of Spain with a high density of pig farming: A prospective cohort study. Clinical Microbiology and Infection, 23(9), 678.e1-678.e4. https://doi.org/10.1016/j.cmi.2017.03.019
- Voss, A., Loeffen, F., Bakker, J., Klaassen, C., & Wulf, M. (2005). Methicillin-resistant Staphylococcus aureus in pig farming. Emerging Infectious Diseases, 11(12), 1965–1966. https://doi.org/10.3201/eid1112.050428
- Walter, J., Espelage, W., Adlhoch, C., Cuny, C., Schink, S., Jansen, A., … Hermes, J. (2017). Persistence of nasal colonisation with methicillin resistant Staphylococcus aureus CC398 among participants of veterinary conferences and occurrence among their household members: A prospective cohort study, Germany 2008–2014. Veterinary Microbiology, 200(2015), 13–18. https://doi.org/10.1016/j.vetmic.2016.03.015
- Wan, M. T., & Chou, C. C. (2014). Spreading of beta-lactam resistance gene (mecA) and methicillin-resistant Staphylococcus aureus through municipal and swine slaughterhouse wastewaters. Water Research, 64, 288–295. https://doi.org/10.1016/j.watres.2014.07.014
- Wardyn, S. E., Forshey, B. M., Farina, S. A., Kates, A. E., Nair, R., Quick, M. K., … Smith, T. C. (2015). Swine farming is a risk factor for infection with and high prevalence of carriage of multidrug-resistant Staphylococcus aureus. Clinical Infectious Diseases, 61(1), 59–66. https://doi.org/10.1093/cid/civ234
- World HealthOrganization. (2018). Antibiotic resistance. Retrieved from https://www.who.int/news-room/fact-sheets/detail/antibiotic-resistance
