Human Health Risks Associated with Antimicrobial Use in Animals

Guide to Antimicrobial Use in Animals

Volumn , Issue , 2009, Pages 13-26

  Jensen, Lars B ^a   Angulo, Frederick J ^b   Mølbak, Kåre ^c   Wegener, Henrik C ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b NATIONAL CENTER FOR EMERGING AND ZOONOTIC INFECTIOUS DISEASES   (United States)

^c STATENS SERUM INSTITUT   (Denmark)

Author keywords

Antimicrobial use and antimicrobial resistance occurrence in animals; Avilamycin use and avilamycin resistant enterococcus faecium prevalence in poultry; Environmental transmission of antimicrobial resistance from animals to humans; Food borne transmission of antimicrobial resistance from animals to humans; Human health risks associated with antimicrobial use in animals; Molecular typing avoparcin use in food animals and VRE occurrence in humans; Resistance and longer illness fluoroquinolone resistant campylobacter infections; Transmission by contact with companion animals; Treatment failures and severity of infection

Indexed keywords

EID: 77954734388     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1002/9781444302639.ch2     Document Type: Chapter

References (96)

1. Hughes, V. M. and Datta, N. (1983). Conjugative plasmids in bacteria of the pre-antibiotic era. Nature 302: 725-726.
2. Weisblum, B. (1995). Erythromycin resistance by ribosome modification. Antimicrob. Agents Chemother. 39(3): 577-585.
3. Guardabassi, L., Christensen, H., Hasman, H. and Dalsgaard, A. (2004). Members of the genera Paenibacillus and Rhodococcus harbor genes homologous to enterococcal glycopeptide resistance genes VanA and VanB. Antimicrob. Agents Chemother. 48(12): 4915-4918.
4. Bush, K. (2001). New beta-lactamases in Gram negative bacteria: diversity and impact on the selection of antimicrobial therapy. Clin. Infect. Dis. 32: 1085-1089.
5. Anonymous. (2006). DANMAP, 2005: Use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark. Available at http://www.dfvf.dk/Files/Filer/Zoonosecentret/Publikationer/Danmap/Danmap_2005.pdf
6. MARAN 2003 (2004). Monitoring of antimicrobial resistance and antibiotic usage in animals in The Netherlands. Available at http://www.cidc-lelystad.wur.nl/NR/rdonlyres/7F79ACE60-FD241-AB-81B2-BB17FA89603C/11381/MARAN2003web1.pdf
7. NORM/NORM-VET 2005 (2006). Consumption of antimicrobial agents and occurrence of resistance in Norway. Available at http://www.vetinst.no/zoo/index.asp?startID= &topExpand=&subExpand=&strUrl=1000586i
8. Hasman, H. and Aarestrup, F.M. (2003) Relationship between copper, glycopeptide, and macrolide resistance among Enterococcus faecium strains isolated from pigs in Denmark between 1997 and 2003. Antimicrob. Agents Chemother. 49(1): 454-456.
9. Endtz, H.P., Ruijs, G.J., van Klingeren, B., Jansen, W.H., van der Reyden, T. and Mouton, R. P. (1991). Quinolone resistance in campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. J. Antimicrob. Chemother. 27: 199-208.
10. Engberg, J., Aarestrup, F.M., Smidt, P.G., Nachamkin, I. and Taylor, D.E. (2001). Quinolone and macrolide resistance in Campylobacter jejuni and coli: a review of mechanisms and trends over time of resistance profiles in human isolates. Emerg. Infect. Dis. 7: 24-34.
11. Helmuth, R. (2000). Antibiotic resistance in Salmonella. In Wray, C. and Wray, A. (eds.), Salmonella in domestic animals. CAB International, Wallingford pp. 89-106.
12. Threlfall, E.J., Ward, L.R., Skinner, J.A. and Rowe, B. (1997). Increase in multiple antibiotic resistance in nontyphoidal salmonellas from humans in England and Wales: a comparison of data for 1994 and 1996. Microb. Drug Resist. 3: 263-266.
13. Hummel, R., Tschäpe, H. and Witte, W. (1986). Spread of plasmid-mediated nourseothricin resistance due to antibiotic use in animal husbandry. J. Basic Microbiol. 26: 461-466.
14. Witte, W., Tschäpe, H., Klare, I. and Werner, W. (2000). Antibiotics in animal feed. Acta Vet. Scand. 93(Suppl): 37-45.
15. Mølbak, K. (2005). Human health consequences of antimicrobial drug-resistant Salmonella and other foodborne pathogens. Clin. Infect. Dis. 4: 1613-1620.
16. Angulo, F.J., Nargund, V.N. and Chiller, T.C. (2004). Evidence of an association between use of antimicrobial agents in food animals and antimicrobial resistance among bacteria isolated from humans and the human health consequence of such resistance. J. Vet. Med. 51: 374-379.
17. Holmberg, S.D. Solomon, S.L. and Blake, A. (1987). Health and economic impacts of antimicrobial resistance. Rev. Infect. Dis. 9(6): 1065-1078.
18. Holmberg, S.D., Osterholm, M.T., Senger, K.A. and Cohen, M.L. (1984). Drug-resistant Salmonella from animals fed antimicrobials. N. Engl. J. Med. 311: 617-622.
19. Spika, J., Waterman, S., Hoo, G. et al. (1987). Chloramphenicol-resistant Salmonella Newport traced through hamburger to dairy farms: a major persisting source of human salmonellosis in California. N. Engl. J. Med. 316: 565-570.
20. Walker, R.A., Lawson, A.J., Lindsay, E.A. et al. (2000). Decreased susceptibility to ciprofloxacin in outbreak-associated multiresistant Salmonella Typhimurium DT104. Vet. Rec. 147(14): 395-396.
21. Mølbak, K., Baggesen, D.L., Aarestrup, F.M. et al. (1999). An outbreak of multi-drug resistant, quinolone-resistant Salmonella enterica serotype Typhimurium DT104. N. Engl. J. Med. 341: 1420-1425.
22. Ethelberg, S., Sørensen, G., Kristensen, B. et al. (2007). Outbreak with multi-resistant Salmonella Typhimurium DT104 linked to Carpaccio, Denmark, 2005. Epidemiol. Infect. 5: 1-8.
23. Glynn, M.K., Reddy, V. Hutwagner, L. et al. (2004). Prior antimicrobial agent use increases the risk of sporadic infections with multidrug-resistant Salmonella enterica serotype Typhimurium a FoodNet case-control study. Clin. Infect. Dis. 38(Suppl 3): S227-S236.
24. Varma, J.K., Marcus, R., Stenzel, S.A. et al. (2006). Highly resistant Salmonella Newport-MDRAmpC transmitted through the domestic US food supply: a FoodNet case-control study of sporadic Salmonella Newport infections, 2002-2003. J. Infect. Dis. 194(2): 222-230.
25. Kassenborg, H.D., Smith, K.E., Vugia, D.J. et al. (2004). Emerging Infections Program FoodNet Working Group, 2004: Fluoroquinolone-resistant Campylobacter infections: eating poultry outside the home and foreign travel are risk factors. Clin. Infect. Dis. 38 (Suppl 3): S279-S284.
26. Levy, S., Fitzerald, G. and Macone, A. (1976). Changes in intestinal flora of farm personell after introduction of a tetracycline-supplemented feed on a farm. N. Engl. J. Med. 295: 583-588.
27. Fey, P.D., Safranek, T.J., Rupp, M.E., et al. (2000). Ceftriaxone-resistant salmonella infection acquired by a child from cattle. N. Engl. J. Med. 342: 1242-1249.
28. Duran, G.M. and Marshall, D.L. (2005). Ready to eat shrimps as an international vehicle of antibiotic resistant bacteria. J. Food Prot. 68: 2395-2401.
29. Adams, C.A., Austin, B., Meaden, P.G. and McIntosh, D. (1998). Molecular characterization of plasmid mediated oxytetracycline resistance in Aeromonas salmonicida. Appl. Environ. Microbiol. 64: 4194-4201.
30. Rhodes, G., Huys, G., Swings, J. et al. (2000). Distribution of oxytetracycline resistance plasmids between Aeromonas in hospitals and aquaculture environments: implication of Tn1721 in dissemination of the tetracycline resistant determinant TetA. Appl. Environ. Microbiol. 66: 2883-3890.
31. Smith, K.E., Besser, J.M., Hedberg, C.W. et al. (1999). Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992-1998. N. Engl. J. Med. 340(20): 1525-1532.
32. Unicomb, L., Ferguson, J., Riley, T.V. and Collignon, P. (2003). Fluoroquinolone resistance in Campylobacter absent from isolates, Australia. Emerg. Infect. Dis. 9(11): 1482-1483.
33. Norström, M., Hofshagen, M., Stavnes, T., Schau, J., Lassen, J. and Kruuse, H. (2006). Antimicrobial resistance in Campylobacter jejuni from humans and broilers in Norway. Epidemiol. Infect. 134(1): 127-130.
34. Klare, I., Badstubner, D., Konstabel, C., Bohme, G., Claus, H. and Witte, W. (1999). Decreased incidence of VanA-type vancomycin-resistant enterococci isolated from poultry meat and from fecal samples of humans in the community after discontinuation of avoparcin usage in animal husbandry. Microb. Drug Resist. 5(1): 45-53.
35. van den Bogaard, A.E., Mertens, P., London, N.H. and Stobberingh, E.E. (1997). High prevalence of colonization with vancomycin-and pristinamycin-resistant enterococci in healthy humans and pigs in The Netherlands: is addition of antibiotics to animal feed to blame? J. Antimicrob. Chemother. 40: 454-456.
36. van den Bogaard, A.E., Bruinsma, N. and Stobberingh, E.E. (2000). The effect of banning avoparcin on VRE carraige in The Netherlands. J. Antimicrob. Chemother. 46: 146-148.
37. Bruinsma, N., Willems, R.J., van den Bogaard, A.E. et al. (2002). Different levels of genetic homogeneity in vancomycin-resistant and susceptible Enterococcus faecium isolates from different human and animal sources analysed by amplified-fragment length polymorphism. Antimicrob. Agents Chemother. 46: 2779-2783.
38. Willems, R. and Boten, M. (2007). Glycopeptide-resistant enterococci: deciphering virulence, resistance and epidemicity. Curr. Opin. Infect. Dis. 20(4): 384-390.
39. Jensen, L.B. (1998). Differences in the occurrence of two base-pair variants of Tn1546 from vancomycin resistant enterococci from humans, pigs and poultry. Antimicrob. Agents Chemother. 42: 2463-2464.
40. Chaslus-Dancla, E. and Lafont, J.P. (1985). Resistance to gentamicin and apramycin in Escherichia coli from calves in France. Vet. Rec. 117: 90-91.
41. Wray, C., Hedges, R.W., Shannon, K.P. and Bradley, D.E. (1986). Apramycin and gentamicin resistance in Escherichia coli and salmonellas isolated from farm animals. J. Hyg. 97(39): 445-456.
42. Hedges, R.W. and Shannon, K.P. (1984). Resistance to apramycin in Escherichia coli isolated from animals: detection of a novel aminoglycoside-modifying enzyme. J. Gen. Microbiol. 130: 473-482.
43. Chaslus-Dancla, E., Martel, J.L, Carlier, C., Lafont, J.P. and Courvalin, P. (1986). Emergence of aminoglycoside 3-Nacetyltransferase IV in Escherichia coli and Salmonella Typhimurium isolated from animals in France. Antimicrob. Agents Chemother. 29: 239-243.
44. Hunter, J.E., Shelley, J.C., Walton, J.R., Hart, C.A. and Bennett, M. (1992). Apramycin resistance plasmids in Escherichia coli: possible transfer to Salmonella Typhimurium in calves. Epidemiol. Infect. 108: 271-278.
45. Johnson, A.P., Burns, L., Woodford, N. et al. (1994). Gentamicin resistance in clinical isolates of Escherichia coli encoded by genes of veterinary origin. J. Med. Microbiol. 40: 221-226.
46. Donabedian, S.M., Thal, L.A, Hershberger, E. et al. (2003). Molecular characterization of gentamicin-resistant Enterococci in the United States: evidence of spread from animals to humans through food. J. Clin. Microbiol. 41(3): 1109-1113.
47. Chiu, C.H., Wu, T.L., Su, L.H., et al. (2002). The emergence in Taiwan of fluoroquinolone resistance in Salmonella enterica serotype Choleraesuis. N. Engl. J. Med. 346(6): 413-419.
48. Clark, G.M., Kaufmann, A.F. and Gangarosa, E.J. (1973). Epidemiology of an international outbreak of Salmonella Agona. The Lancet 2: 490-493.
49. Bender, J.B. and Shulman, S.A. (2004). Anomalies in public contact subcommittee and National Association of State Public Health Veterinarians. Reports of zoonotic disease outbreaks associated with animal exhibits and availability of recommendations for preventing zoonotic disease transmission from animals to people in such settings. J. Am. Vet. Med. Assoc. 224: 1105-1109.
50. Heuvelink, A.E., van Heerwaarden, C., Zwartkruis-Nahuis, J.T. et al. (2002). Escherichia coli O157 infection associated with a petting zoo. Epidemiol. Infect. 129: 295-302.
51. Hendriksen, S.W.M., Orsel, K., Wagenaar, J.A., Miko, A. and van Duijkeren, E. (2004). Animal to human transmission of Salmonella Typhimurium DT104A variant. Emerg. Infect. Dis. 12: 2225-2227.
52. Wright, J.G., Tengelsen, L.A., Smith, K.E. et al. (2005). Multidrug-resistant Salmonella Typhimurium in four animal facilities. Emerg. Infect. Dis. 11: 1235-1241.
53. Voss, A., Loeffen, F., Bakker, J., Klaassen, C. and Wulf, M. (2005). Methicillin-resistant Staphylococcus aureus in pig farming. Emerg. Infect. Dis. 11: 1965-1966.
54. Akwar, T.H., Poppe, C., Wilson, J. et al. (2007). Risk factors for antimicrobial resistance among fecal Escherichia coli from residents on forty-three swine farms. Microb. Drug Resist. 13: 69-76.
55. Guardabassi, L., Schwarz, S. and Lloyd, D. (2004). Pet animals as reservoirs of antimicrobial resistant bacteria. J. Antimicrob. Chemother. 54: 321-332.
56. Centers for Disease Control and Prevention (CDC). (2003). Reptile-associated salmonellosis-selected states 1998-2002. MMWR 52: 1206-1209.
57. Woodward, D.L., Khakhria, R. and Johnson, W.M. (1997). Human Salmonellosis associated with exotic pets. J. Clin. Microbiol. 35: 2786-2790.
58. Mermin, J., Hoar, B. and Angulo, F.J. (1997). Iguanas and Salmonella Marina infection in children: a reflection of the increasing incidence of reptile-associated Salmonellosis in the United States. Pediatrics 99: 399-402.
59. Centers for Disease Control and Prevention (CDC) (2003). Outbreak of multidrug-resistant Salmonella Typhimurium associated with rodents purchase in retail pet stores-United States, December 2003-October 2004. MMWR 54: 429-433.
60. Centers for Disease Control and Prevention (CDC) (2005). Salmonellosis associated with pet turtles-Wisconsin and Wyoming 2004. MMWR 54: 223-236.
61. Centers for Disease Control and Prevention (2001). Outbreaks of multidrug-resistant Salmonella Typhimurium associated with veterinary facilities-Idaho, Minnesota and Washington, 1999. MMWR 50: 701-704.
62. Tenkate, T.D. and Stafford, R.J. (2001). Risk factors for campylobacter infection in infants and young children: a matched case-control study. Epidemiol. Infect. 127: 399-404.
63. Carrique-Mas, J., Andersson, Y., Hjertqvist, M. et al. (2005). Risk factors for domestic sporadic campylobacteriosis among young children in Sweden. Scand. J. Infect. Dis. 37: 101-110.
64. Damborg, P., Olsen, K.E., Møller Nielsen, E. and Guardabassi, L. (2004). Occurrence of Campylobacter jejuni in pets living with human patients infected with C. jejuni. J. Clin. Microbiol. 42: 1363-1364.
65. Wolfs, T.F.W., Duim, B., Geelen, S.P.M. et al. (2001). Neonathal septis by Campylobacter jejuni: genetically proven transmission from a household puppy. Clin. Infect. Dis. 32: 97-99.
66. Leonard, F.C. and Markay, B.K. (2007). Methicillinresistant Staphylococcus aureus in animal: a review. Vet. J. (in press). doi: 10.1016/j.tvjl.2006.11.008
67. Manian, F.A. (2003). Asymptomatic nasal carriage of mupirocin-resistant, methicillin-resistant Staphylococcus aureus (MRSA) in pet dog associated with MRSA infections in household contact. Clin. Infect. Dis. 36: 26-28.
68. van Duijkeren, E., Wolfhagen, M.J., Heck, M.E. and Wannet, W.J. (2005). Transmission of panton-valentine leucocidin-positive methicillin-resistant Staphylococcus aureus strain between humans and a dog. J. Clin. Microbiol. 43(12): 6209-6211.
69. Weese, J.S., Dick, H., Willey, B.M. et al. (2006). Suspected transmission of methicillin-resistant Staphylococcus aureus between domestic pets and humans in veterinary clinics and in the household. Vet. Microbiol. 115: 148-155.
70. Weese, J.S., Rousseau, J., Traub-Darfatz, J.L., Willey, B.M., McGeer, A.J. and Low, D.E. (2005). Communityassociated methicillin-resistant Staphylococcus aureus in horses and humans who work with horses. J. Am. Vet. Med. Assoc. 226: 580-583.
71. Moodley, A., Stegger, M., Bagcigil, A.F. et al. (2006). PFGE and spa typing of methicillin-resistant Staphylococcus aureus isolated from domestic animals and veterinary staff in the UK and Ireland. J. Antimicrob. Chemother. 58: 1118-1123.
72. Hanselman, B.A., Kruth, S.A., Rousseau, J. et al. (2006). Methicillin-resistant Staphylococcus aureus colonization in veterinary personnel. Emerg. Infect. Dis. 12: 1933-1938.
73. Harvey, R.G., Marples, R.R. and Noble, W.C. (1994). Nasal carriage of Staphylococcus intermedius in humans in contact with dogs. Microb. Ecol. Health Dis. 7: 225-227.
74. Guardabassi, L., Loeber, M.E. and Jacobson, A. (2004). Transmission of multiple antimicrobial resistant Staphylococcus intermedius between dogs affected by deep pyoderma and their owners. Vet. Microbiol. 98: 23-27.
75. Agersø, Y., Sengeløv, G. and Jensen, L.B. (2004). Development of a rapid method for direct detection of tet(M) genes in soil from Danish farmland. Environ. Int. 30: 117-122.
76. Sengeløv, G., Agersø, Y., Halling-Sørensen, B., Andersen, J.S. and Jensen, L.B. (2003). Bacterial antibiotic resistance levels in Danish farmland as a result of treatment with pig manure slurry. Environ. Int. 28: 587-595.
77. Chee-Sanford, J.C., Aminov, R.I., Krapac, I.J. et al. (2001). Occurrence and diversity of tetracycline resistance genes in lagoons and groundwater underlying two swine production facilities. Appl. Environ. Microbiol. 67: 1494-1502.
78. Petersen, A., Andersen, J.S., Kaawmak, T. et al. (2002). Impact of integrated fish farming on antimicrobial resistance in a pond environment. Appl. Environ. Microbiol. 68: 6036-6042.
79. Lee, T.X., Munekage, Y. and Kato, S.-I. (2005). Antibiotic resistance in bacteria from shrimp farming in mangrove areas. Sci. Total Environ. 349: 95-105.
80. Chapin, A., Rule, A., Gibson, K., Buckley, T. and Schwab, K. (2005). Airborne multidrug resistant bacteria isolated from a concentrated swine feeding operation. Environ. Health Perspect. 113: 137-142.
81. Green, C.F., Gibbs, S.G., Tarwater, P.M. et al. (2006). Bacterial plume emanating from the air surrounding swine confinement operations. J. Occup. Environ. Hyg. 3: 9-15.
82. Hamscher, G., Pawelzick, H.T., Sczesny, S. et al. (2003). Antibiotics in dust originating from a pig-fattening farm: a new source of health hazard for farmers. Environ. Health Perspect. 111: 1590-1594.
83. Gibbs, S.G., Green, C.F., Tarwater, P.M. et al. (2006). Isolation of antibiotic resistant bacteria from air plume downwind of a swine confined and concentrated animal feeding operation. Environ. Health Perspect. 114: 1032-1037.
84. Barza, M. and Travers, K. (2002). Excess infections due to antimicrobial resistance: the 'attributable fraction'. Clin. Infect. Dis. 34: 126-130.
85. Ryan, C.A., Nickels, M.K., Hargrett-Bean, N.T. et al. (1987). Massive outbreak of antimicrobial-resistant salmonellosis traced to pasteurized milk. J. Am. Med. Assoc. 258: 3269-3274.
86. Bohnhoff, M. and Miller, C.P. (1962). Enhanced susceptibility to Salmonella infection in streptomycin-treated mice. J. Infect. Dis. 111: 117-127.
87. Cohen, M.L. and Tauxe, R.V. (1986). Drug-resistant Salmonella in the United States: an epidemiologic perspective. Science 234: 964-969.
88. Varma, J.K., Green, K.D., Ovitt, J. et al. (2005). Hospitalization and antimicrobial resistance in Salmonella outbreaks, 1984-2002. Emerg. Infect. Dis. 11: 943-946.
89. Lee L.A., Puhr, N.D., Maloney, E.K. et al. (1994). Increase in antimicrobial-resistant Salmonella infections in the United States 1989-1990. J. Infect. Dis. 170: 128-134.
90. Varma, J.K., Mølbak, K., Barrett, et al. (2005). Antimicrobial-resistant nontyphoidal Salmonella is associated with excess bloodstream infections and hospitalizations. J. Infect. Dis. 191(4): 554-561.
91. Helms M., Simonsen J. and Mølbak K. (2004). Quinolone resistance is associated with increased risk of invasive illness or death during infection with Salmonella serotype Typhimurium. J. Infect. Dis. 190: 1652-1654.
92. Helms M., Vastrup, P., Gerner-Smidt, P. and Mølbak, K. (2002). Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium. Emerg. Infect. Dis. 8: 490-495.
93. Crump, J.A., Barrett, T.J., Nelson, J.T. and Angulo, F.J. (2003). Reevaluating fluoroquinolone breakpoints for Salmonella enterica serotype Typhi and for non-Typhi salmonellae. Clin. Infect. Dis. 37: 75-81.
94. Nelson, J.M., Chiller, T.M., Powers, J.H. and Angulo, F.J. (2007). Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clin. Infect. Dis. 44: 977-980.
95. Neimann, J., Engberg, J., Mølbak, K. and Wegener, H.C. (2003). A case-control study of risk factors for sporadic campylobacter infections in Denmark. Epidemiol. Infect. 130: 353-366.
96. Engberg J., Neimann, J., Nielsen, E.M. et al. (2004). Quinolone-resistant Campylobacter infections: risk factors and clinical consequences. Emerg. Infect. Dis. 10: 1056-1063.