Advertisement

Quantitative Risk Assessment of Human Risks of Methicillin-Resistant Staphylococcus aureus (MRSA) from Swine Operations

  • Louis Anthony Cox Jr.
  • Douglas A. Popken
  • Richard X. Sun
Chapter
Part of the International Series in Operations Research & Management Science book series (ISOR, volume 270)

Abstract

Describing quantitatively how large a risk is provides crucial information for helping to set risk management priorities. This chapter applies descriptive analytics to assess the size of the human health risks from a particular source. It continues the theme begun in Chap.  5 of examining human health risks from antibiotic-resistant infectious bacteria, but focuses specifically on long-standing concerns expressed by the public health community, news media, and members of the general public that methicillin-resistant Staphylococcus aureus (MRSA) transmitted from pigs to humans may harm human health. For readers not interested in details of this application, a brief summary is that previous studies of the prevalence and dynamics of swine-associated (ST398) MRSA have sampled MRSA at discrete points in the presumed causal chain leading from swine to human patients, including sampling bacteria from live pigs, retail meats, farm workers, and hospital patients. This chapter integrates available data from several sources to construct a conservative (plausible upper-bound) probability estimate for the quantitative human health harm (MRSA infections and fatalities) arising from ST398-MRSA from pigs. The estimated plausible upper bounds are approximately one excess human infection per year among all U.S. pig farm workers, and one human infection per 31 years among the remaining total population of the U.S., assuming that bacteria transmission events not yet observed are possible. The true risks may be smaller (possibly zero for members of the general population). Putting rough numerical bounds on the size of the risk such as “less than one case per 300 million people per decade” can help to engage System 2 thinking (cognitive, slow, deliberative; see Chap.  12) about costs and benefits of risk-reducing interventions; whereas leaving the risk unquantified is more likely to engage System 1 thinking (intuitive, quick, emotional; see Chap.  12), which typically reacts very strongly and adversely to the qualitative idea of contamination of food with invisible, harmful microbes.

References

  1. Argudin MA, Fetsch A, Tenhagen BA, Kowall J, Hammerl J, Kaempe U, Hertwig S, Schroter A, Braunig J, Kasbohrer A, Appel B, Nockler K, Helmuth R, Mendoza MC, Rodicio MR, Guerra B (2009) Virulence and resistance determinants in methicillin-resistant Staphylococcus aureus ST398 isolates. In: 19th European congress of clinical microbiology and infectious diseases. Diseases, ESCMID Helsinki, Finland, Blackwell Publishing Google Scholar
  2. Boost M, Ho J, Guardabassi L, O’Donoghue M (2012) Colonization of Butchers with livestock-associated methicillin-resistant Staphylococcus aureus. Zoonoses Public Health.  https://doi.org/10.1111/zph.12034 [epub ahead of print] (Available at Last accessed on 1/28/2013)
  3. Bootsma MC, Wassenberg MW, Trapman P, Bonten MJ (2011) The nosocomial transmission rate of animal-associated ST398 meticillin-resistant Staphylococcus aureus. J R Soc Interface 8(57):578–584CrossRefGoogle Scholar
  4. CBS (2010, 6/16/2010) Animal antibiotic overuse hurting humans? Katie Couric Investigates feeding healthy farm animals antibiotics. Is it creating new drug-resistant bacteria? CBS Special News Report: Katie Couric Investigates. http://www.cbsnews.com/stories/2010/02/09/eveningnews/main6191530.shtml
  5. Cox LA, Popken DA, Berman DW (2013) Causal versus spurious spatial exposure–response associations in health risk analysis. Crit Rev Toxicol 43(S1):26–38CrossRefGoogle Scholar
  6. Cuny C, Nathaus R, Layer F, Strommenger B, Altmann D, Witte W (2009) Nasal colonization of humans with methicillin-resistant Staphylococcus aureus (MRSA) CC398 with and without exposure to pigs. PLoS One 4(8):e6800CrossRefGoogle Scholar
  7. Davies P (2009) Methicillin Resistant Staphylococcus aureus in pigs, pork products and swine veterinarians. National Pork Board - NPB Final Research Grant Report, #NPB 07-196Google Scholar
  8. Davies P (2010) Prevalence and characterization of Methicillin-resistant Staphylococcus aureus (MRSA) in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. #08-178Google Scholar
  9. de Boer E, Zwartkruis-Nahuis JTM, Wit B, Huijsdens XW, de Neeling AJ, Bosch T, van Oosterom RAA, Vila A, Heuvelink AE (2009) Prevalence of methicillin-resistant Staphylococcus aureus in meat. Int J Food Microbiol 134(1–2):52–56CrossRefGoogle Scholar
  10. de Jonge R, Verdier JE, Havelaar AH (2010) Prevalence of meticillin-resistant Staphylococcus aureus amongst professional meat handlers in the Netherlands, March-July 2008. Euro Surveill 15(46) Google Scholar
  11. Declercq P, Petre D, Gordts B, Voss A (2008) Complicated community-acquired soft tissue infection by MRSA from porcine origin. Infection 36(6):590–592CrossRefGoogle Scholar
  12. Denis O, Suetens C, Hallin M, Catry B, Ramboer I, Dispas M, Willems G, Gordts B, Butaye P, Struelens MJ (2009) Methicillin-resistant Staphylococcus aureus ST398 in swine farm personnel, Belgium. Emerg Infect Dis 15(7):1098–1101CrossRefGoogle Scholar
  13. EFSA (2009) Scientific Opinion of the Panel on Biological Hazards on a request from the European Commission on Assessment of the Public Health significance of meticillin resistant Staphylococcus aureus (MRSA) in animals and foods. EFSA J 993(1):1–73Google Scholar
  14. Feingold BJ, Silbergeld EK, Curriero FC, van Cleef BA, Heck ME, Kluytmans JA (2012) Livestock density as risk factor for livestock-associated methicillin-resistant Staphylococcus aureus, the Netherlands. Emerg Infect Dis 18(11):1841–1849CrossRefGoogle Scholar
  15. Frana TS, Beahm AR, Hanson BM, Kinyon JM, Layman LL, Karriker LA, Ramirez A, Smith TC (2013) Isolation and characterization of methicillin-resistant Staphylococcus aureus from pork farms and visiting veterinary students. PLoS One 8(1):e53738CrossRefGoogle Scholar
  16. Gilbert MJ, Bos MEH, Duim B, Urlings BAP, Heres L, Wagenaar JA, Heederik DJJ (2012) Livestock-associated MRSA ST398 carriage in pig slaughterhouse workers related to quantitative environmental exposure. Occup Environ Med 69(7):472–478CrossRefGoogle Scholar
  17. Gorwitz RJ, Kruszon-Moran D, McAllister SK, McQuillan G, McDougal LK, Fosheim GE, Jensen BJ, Killgore G, Tenover FC, Kuehnert MJ (2008) Changes in the prevalence of nasal colonization with Staphylococcus aureus in the United States, 2001-2004. J Infect Dis 197(9):1226–1234CrossRefGoogle Scholar
  18. Graham PL 3rd, Lin SX, Larson EL (2006) A U.S. population-based survey of Staphylococcus aureus colonization. Ann Intern Med 144(5):318–325CrossRefGoogle Scholar
  19. Graveland H, Wagenaar JA, Bergs K, Heesterbeek H, Heederik D (2011) Persistence of livestock associated MRSA CC398 in humans is dependent on intensity of animal contact. PLoS One 6(2):e16830CrossRefGoogle Scholar
  20. Guardabassi L, O’Donoghue M, Moodley A, Ho J, Boost M (2009) Novel lineage of methicillin-resistant Staphylococcus aureus, Hong Kong. Emerg Infect Dis 15(12):1998–2000CrossRefGoogle Scholar
  21. IARTF (2011) Report of the Iowa antibiotic resistance task force, a public health guide. http://publications.iowa.gov/17707/1/antibioticreport.pdf. Last accessed on 2-9-18
  22. Kelman A, Soong YA, Dupuy N, Shafer D, Richbourg W, Johnson K, Brown T, Kestler E, Li Y, Zheng J, McDermott P, Meng J (2011) Antimicrobial susceptibility of Staphylococcus aureus from retail ground meats. J Food Prot 74(10):1625–1629CrossRefGoogle Scholar
  23. Khanna T, Friendship R, Dewey C, Weese JS (2008) Methicillin resistant Staphylococcus aureus colonization in pigs and pig farmers. Vet Microbiol 128(3–4):298–303CrossRefGoogle Scholar
  24. Kluytmans JAJW (2010) Methicillin-resistant Staphylococcus aureus in food products: cause for concern or case for complacency? Clin Microbiol Infect 16(1):11–15CrossRefGoogle Scholar
  25. Limbago B (2010) Methicillin-resistant Staphylococcus aureus in the United States—is there a connection between retail foods and human infection? In: 2010 scientific meeting of the national antimicrobial resistance monitoring system, US-FDA, Atlanta, GAGoogle Scholar
  26. Lozano C, Aspiroz C, Ezpeleta AI, Gomez-Sanz E, Zarazaga M, Torres C (2011) Empyema caused by MRSA ST398 with atypical resistance profile, Spain [letter]. Emerg Infect Dis 17(1):138–140CrossRefGoogle Scholar
  27. Molla B, Byrne M, Abley M, Mathews J, Jackson C, Fedorka-Cray PJ, Sreevatsan S, Wang P, Gebreyes W (2012) Epidemiology and genotypic characteristics of methicillin-resistant Staphylococcus aureus strains of porcine origin. J Clin Microbiol 50(11):3687–3693CrossRefGoogle Scholar
  28. NPB (2010) Pork quick facts—the pork industry at a glance. Pork CheckoffGoogle Scholar
  29. O’Brien AM, Hanson BM, Farina SA, Wu JY, Simmering JE, Wardyn SE, Forshey BM, Kulick ME, Wallinga DB, Smith TC (2012) MRSA in conventional and alternative retail pork products. PLoS One 7(1):e30092CrossRefGoogle Scholar
  30. O’Donoghue M, Boost M (2004) The prevalence and source of methicillin-resistant Staphylococcus aureus (MRSA) in the community in Hong Kong. Epidemiol Infect 132(6):1091–1097CrossRefGoogle Scholar
  31. Otto D, Orazem P, Huffman W (1998) Community and economic impacts of the Iowa Hog industry. In: Miranowski J (ed) Iowa’s Pork industry—dollars and scents. ISU-CAIS, Iowa CityGoogle Scholar
  32. Smith TC, Male MJ, Harper AL, Moritz-Korolev ED, Diekema D, Herwaldt LA (2008) Isolation of methicillin-resistant Staphylococcus aureus (MRSA) from swine in the midwestern United States. In: International conference on emerging infectious diseases, Atlanta, GAGoogle Scholar
  33. Smith TC, Male MJ, Harper AL, Kroeger JS, Tinkler GP, Moritz ED, Capuano AW, Herwaldt LA, Diekema DJ (2009) Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS One 4(1):e4258CrossRefGoogle Scholar
  34. Smith TC, Gebreyes WA, Abley MJ, Harper AL, Forshey BM, Male MJ, Martin HW, Molla BZ, Sreevatsan S, Thakur S, Thiruvengadam M, Davies PR (2013) Methicillin-resistant Staphylococcus aureus in pigs and farm workers on conventional and antibiotic-free swine farms in the USA. PLoS One 8(5):e63704CrossRefGoogle Scholar
  35. USBLS (2012) Employment by Detailed Occupation—2010 and Projected 2020. Empoyment by Occupation Retrieved 2/27/2013, 2013. http://www.bls.gov/emp/ep_table_102.htm
  36. USCB (2012) Statistical Abstract of the United States: 2012, Table 1377. Meat Consumption by Type and Country: 2009 and 2010, U.S. Census BureauGoogle Scholar
  37. USDA (2008) Swine 2006 - Part IV: changes in the U.S. Pork Industry, 1990-2006. USDA - #N520.1108. http://www.aphis.usda.gov/animal_health/nahms/swine/downloads/swine2006/Swine2006_dr_PartIV.pdf. Last accessed on 12/16/2009
  38. USDA-NASS (2009) 2007 Census of Agriculture, USDA National Agricultural Statistical ServicesGoogle Scholar
  39. van Cleef B, Haenen A, van den Broek M, Huijsdens XW, Mulders M, Kluytmans J (2009) Acquisition and persistence of methicillin-resistant Staphylococcus aureus Clonal Complex 398 during occupational exposure. In: 19th European congress of clinical microbiology and infectious diseases, Helsinki, Finland Google Scholar
  40. Van Cleef BA, Broens EM, Voss A, Huijsdens XW, Zuchner L, Van Benthem BH, Kluytmans JA, Mulders MN, Van De Giessen AW (2010) High prevalence of nasal MRSA carriage in slaughterhouse workers in contact with live pigs in The Netherlands. Epidemiol Infect 138(5):756–763CrossRefGoogle Scholar
  41. Van De Griend P, Herwaldt LA, Alvis B, DeMartino M, Heilmann K, Doern G, Winokur P, Vonstein DD, Diekema D (2009) Community-associated methicillin-resistant Staphylococcus aureus, Iowa, USA. Emerg Infect Dis 15(10):1582–1589CrossRefGoogle Scholar
  42. van Rijen MM, Van Keulen PH, Kluytmans JA (2008) Increase in a Dutch hospital of methicillin-resistant Staphylococcus aureus related to animal farming. Clin Infect Dis 46(2):261–263CrossRefGoogle Scholar
  43. Wassenberg MW, Bootsma MC, Troelstra A, Kluytmans JA, Bonten MJ (2011) Transmissibility of livestock-associated methicillin-resistant Staphylococcus aureus (ST398) in Dutch hospitals. Clin Microbiol Infect 17(2):316–319CrossRefGoogle Scholar
  44. Waters AE, Contente-Cuomo T, Buchhagen J, Liu CM, Watson L, Pearce K, Foster JT, Bowers J, Driebe EM, Engelthaler DM, Keim PS, Price LB (2011) Multidrug-resistant Staphylococcus aureus in US meat and poultry. Clin Infect Dis 52(10):1227–1230CrossRefGoogle Scholar
  45. Webb GF, Horn MA, D’Agata EM, Moellering RC, Ruan S (2009) Competition of hospital-acquired and community-acquired methicillin-resistant Staphylococcus aureus strains in hospitals. J Biol Dyn 48:271–284Google Scholar
  46. Weese JS, Gow SP, Friendship R, Booker C, Reid-Smith R (2009) Methicillin-resistant Staphylococcus aureus (MRSA) surveillance in slaughter-age pigs and feedlot cattle. In: ASM-ESCMID conference on MRSA in animals: veterinary and public health implications, LondonGoogle Scholar
  47. Weese JS, Rousseau J, Deckert A, Gow S, Reid-Smith R (2011) Clostridium difficile and methicillin-resistant Staphylococcus aureus shedding by slaughter-age pigs. BMC Vet Res 7(1):41CrossRefGoogle Scholar
  48. Wulf M, Markestein A, van der Linden F, Voss A, Klaassen C, Verduin C (2007) First outbreak of methicillin-resistant Staphylococcus aureus ST398 in a Dutch hospital, June 2007. Euro Surveill 13(9):8051Google Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Louis Anthony Cox Jr.
    • 1
  • Douglas A. Popken
    • 2
  • Richard X. Sun
    • 3
  1. 1.Cox AssociatesDenverUSA
  2. 2.Cox AssociatesLittletonUSA
  3. 3.Cox AssociatesEast BrunswickUSA

Personalised recommendations