Hostname: page-component-7479d7b7d-k7p5g Total loading time: 0 Render date: 2024-07-12T00:16:24.489Z Has data issue: false hasContentIssue false
  • English
  • Français

Molecular epidemiology of antimicrobial resistance in veterinary medicine: where do we go?

Published online by Cambridge University Press:  28 February 2007

Patrick Boerlin
Patrick Boerlin*
Affiliation:
Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario N1G 2W1, Canada
*
E-mail: pboerlin@uoguelph.ca
Get access Rights & Permissions [Opens in a new window]

Abstract

Molecular epidemiology allows us to trace specific microorganisms and mobile genetic elements and to assess their epidemiological and evolutionary relationships. Examples of molecular epidemiology investigations in veterinary hospitals are discussed. They demonstrate the great similarities with the situation in human medicine and the potential usefulness of molecular epidemiology in our fight against antimicrobial resistance and nosocomial infections in veterinary hospitals. A broad knowledge of the diversity of antimicrobial resistance determinants in some major groups of pathogens and commensals from animals such as Enterobacteriaceae, Pasteurellaceae, enterococci and staphylococci is emerging. However, there are important gaps in this knowledge, which are discussed here. Many more molecular epidemiology studies will be necessary to understand and follow the evolution of the problem in veterinary medicine and agriculture on a global scale. To be able to build useful surveillance programs and reliable epidemiological models, and to identify critical intervention points, we need to improve our understanding of antimicrobial resistance at the animal and farm levels. Studies assessing the dynamics of bacterial populations and of resistance determinants at these levels are desperately needed. Understanding the relationships between antimicrobial resistance, colonization factors, and virulence also represents a major issue for which molecular epidemiology investigations will be needed.

Keywords

molecular epidemiologyantimicrobial resistancenosocomial infectionsanimal
Type
Review Article
Information
Animal Health Research Reviews , Volume 5 , Issue 1 , June 2004 , pp. 95 - 102
Copyright
Copyright © CAB International 2004

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Bailar, JC and Travers, K (2002). Review of assessment of the human health risk associated with the use of antimicrobial agents in agriculture. Clinical Infectious Diseases 34 (Supplement 3): S135–143CrossRefGoogle ScholarPubMed
Barton, MD (2001). Is it reasonable to use third generation cephalosporins to treat animals? Australian Veterinary Journal 79: 620.CrossRefGoogle ScholarPubMed
Bass, L, Liebert, CA, Lee, MD, Sumers, AO, White, DG, Thayer, SG, and Maurer, JJ (1999). Incidence and characterization of integrons, genetic elements mediating multiple-drug resistance, in avian Escherichia coli. Antimicrobial Agents and Chemotherapy 43: 2925–2929.CrossRefGoogle ScholarPubMed
Bergogne-Bérézin, E and Towner, KJ (1996). Acinetobacter spp. as nosocomial pathogens: microbiological, clinical, and epidemiological features. Clinical Microbiology Reviews 9: 148–165.CrossRefGoogle ScholarPubMed
Björkman, J, Hughes, D and Andersson, DI (1998). Virulence of antibiotic-resistant Salmonella typhimurium. Proceedings of the National Academy of Sciences of the United States of America 95: 3949–3953.CrossRefGoogle ScholarPubMed
Boerlin, P and Kuhnert, P (2003). Characterization of class 1 integrons from clinical Escherichia coli isolates of different animal species. In: Annual Meeting of the Swiss Society for Microbiology March 6–7, 2003. Basel: Swiss Society for Microbiology. Abstract P18, p. 59.Google Scholar
Boerlin, P and McEwen, S (2000). Diversity of antibiotic resistant Escherichia coli from the normal flora of pigs. In: Fifth International Meeting on Bacterial Epidemiological Markers. Noordwijkerhout, The Netherlands, September 6–9, 2000. Abstract P009, p. 74.Google Scholar
Boerlin, P, Eugster, S, Gaschen, F, Straub, R and Schawalder, P (2001). Transmission of opportunistic pathogens in a veterinary teaching hospital. Veterinary Microbiology 82: 347–359.CrossRefGoogle Scholar
Bonten, MJ, Willems, R and Weinstein, RA (2001). Vancomycin-resistant enterococci: why are they here, and where do they come from? Lancet Infectious Diseases 1: 314–325.CrossRefGoogle ScholarPubMed
Böttger, EC, Springer, B, Pletschette, M and Sander, P (1998). Fitness of antibiotic-resistant microorganisms and compensator mutations. Nature Medicine 4: 1343–1344.CrossRefGoogle Scholar
Brun, E, Holstad, G, Kruse, H and Jarp, J (2002). Within-sample and between-sample variation of antimicrobial resistance in fecal Escherichia coli isolates from pigs. Microbial Drug Resistance 8: 385–391.CrossRefGoogle ScholarPubMed
Bushman, F (2002). Lateral DNA Transfer, Mechanisms and Consequences Cold Spring Harbor: Cold Spring Harbor Laboratory Press.Google Scholar
Carattoli, A (2001). Importance of integrons in the diffusion of resistance. Veterinary Research 32: 243–260.CrossRefGoogle ScholarPubMed
Catry, B, Laevens, H, Devriese, LA, Opsomer, G and De Kruif, A (2003). Antimicrobial resistance in livestock. Journal of Veterinary Pharmacology and Therapeutics 26: 81–93.CrossRefGoogle ScholarPubMed
Chavers, LS, Moser, SA, Benjamin, WH, Banks, SE, Steinhauer, JR, Smith, AM, Johnson, CN, Funkhouser, E, Chavers, LP, Stamm, AM and Waites, KB (2003). Vancomycin-resistant enterococci: 15 years and counting. Journal of Hospital Infection 53: 159–171.CrossRefGoogle Scholar
Courvalin, P and Trieu-Cuot, P (2001). Minimizing potential resistance: the molecular view. Clinical Infectious Diseases 33: (Supplement 3): S138–146CrossRefGoogle ScholarPubMed
Dunlop, RH, McEwen, SA, Meek, AH, Friendship, RM, Black, WD and Clarke, RC (1999). Sampling considerations for herd-level measurement of fecal Escherichia coli antimicrobial resistance in finisher pigs. Epidemiology and Infection 122: 485–496.CrossRefGoogle ScholarPubMed
Emborg, HD, Andersen, JS, Seyfarth, AM and Wegener, HC (2004) Relations between the consumption of antimicrobial growth promoters and the occurrence of resistance among Enterococcus faecium isolated from broilers. Epidemiology and Infection 132: 95–105.CrossRefGoogle ScholarPubMed
Fluit, AC and Schmitz, FJ (1999). Class 1 integrons, gene cassettes, mobility and epidemiology. European Journal of Clinical Microbiology and Infectious Diseases 18: 761–770.CrossRefGoogle ScholarPubMed
Franklin, A and Möllby, R (1983). Concurrent transfer and recombination between plasmids encoding for heat-stable enterotoxin and drug resistance in porcine enterotoxigenic Escherichia coli. Medical Microbiology and Immunology 172: 137–147.CrossRefGoogle ScholarPubMed
Gibrel, A, Sköld, O (1998). High-level resistance to trimethoprim in clinical isolates of Campylobacter jejuni by acquisition of foreign genes (dfr1 and dfr9) expressing drug-insensitive dihydrofolate reductases. Antimicrobial Agents and Chemotherapy 42: 3059–3064.CrossRefGoogle Scholar
Grape, M, Sunström, L and Kronvall, G (2003). Sulphonamide resistance gene sul3 found in Escherichia coli isolates from human sources. Journal of Antimicrobial Chemotherapy 52: 1022–1024.CrossRefGoogle ScholarPubMed
Guerra, B, Junker, E, Schroeter, A, Malorny, B, Lehman, S and Helmuth, R (2003). Phenotypic and genotypic characterization of antimicrobial resistance in German Escherichia coli isolates from cattle, swine and poultry. Journal of Antimicrobial Chemotherapy 52: 489–492.CrossRefGoogle ScholarPubMed
Gyles, CL, Palschauduri, S and Maas, WK (1977). Naturally occurring plasmid carrying genes for enterotoxin production and drug resistance. Science 198: 198–199.CrossRefGoogle ScholarPubMed
Harnett, NM and Gyles, CL (1985). Linkage of genes for heat-stable enterotoxin, drug resistance, K99 antigen, and colicin in bovine and porcine strains of enterotoxigenic Escherichia coli. American Journal of Veterinary Research 46: 428–433.Google ScholarPubMed
Hasegawa, K, Yamamoto, K, Chiba, N, Kobayashi, R, Nagai, K, Jacobs, MR, Appelbaum, PC, Sunakawa, K and Ubikata, K (2003). Diversity of ampicillin-resistance genes in Haemophilus influenzae in Japan and the United States. Microbial Drug Resistance 9: 39–46.CrossRefGoogle ScholarPubMed
Hirsch, DC, Kirkham, C and Wilson, WD (1993). Linkage of serum resistance, aerobactin production, and resistance to antimicrobial agents on conjugational plasmids in some strains of Escherichia coli isolated from septic foals. American Journal of Veterinary Research 54: 878–881.CrossRefGoogle Scholar
Holmes, AJ, Gillings, MR, Nield, BS, Mabbutt, BC, Nevalainen, KMH and Stokes, HW (2003). The gene cassette metagenome is a basic resource for bacterial genome evolution. Environmental Microbiology 5: 383–394.CrossRefGoogle ScholarPubMed
Jansson, C and Sköld, O (1991). Appearance of a new trimethoprim resistance gene, dhfrIX, in Escherichia coli from swine. Antimicrobial Agents and Chemotherapy 35: 1891–1890.CrossRefGoogle ScholarPubMed
Jansson, C, Franklin, A and Sköld, O (1992). Spread of a newly found trimethoprim resistance gene, dhfrIX, among porcine isolates and human pathogens. Antimicrobial Agents and Chemotherapy 36: 2704–2708.CrossRefGoogle ScholarPubMed
Johnson, JA (2002). Nosocomial infections. Veterinary Clinics of North America. Small Animal Practice 32: 1101–1126.CrossRefGoogle ScholarPubMed
Johnson, TJ, Giddings, CW, Horne, SM, Gibbs, PS, Wooley, RE, Skyberg, J, Olah, P, Kercher, R, Sherwood, JS, Foley, SL and Nolan, LK (2002). Location of increased serum survival gene and selected virulence traits on a conjugative R plasmid in an avian Escherichia coli isolate. Avian Diseases 46: 342–352.CrossRefGoogle Scholar
Karlowsky, JA, Verma, G, Zahnel, GG and Hoban, DJ (2000). Presence of ROB-1 beta-lactamase correlates with cefaclor resistance among recent isolates of Haemophilus influenzae. Journal of Antimicrobial Chemotherapy 45: 871–875.CrossRefGoogle ScholarPubMed
Kehrenberg, C, Schulze-Tanzil, G, Martel, J-L, Chaslus-Dancla, E and Schwarz, S (2001). Antimicrobial resistance in Pasteurella and Mannheimia: epidemiology and genetic basis. Veterinary Research 32: 323–339.CrossRefGoogle Scholar
Khachatryan, AR, Hancock, DD, Besser, TE and Call, DR (2004). Role of calf-adapted Escherichia coli in maintenance of antimicrobial drug resistance in dairy calves. Applied and Environmental Microbiology 70: 752–757.CrossRefGoogle ScholarPubMed
Lanz, R, Kuhnert, P and Boerlin, P (2003). Antimicrobial resistance and resistance gene determinants in clinical Escherichia coli from different animal species in Switzerland. Veterinary Microbiology 91: 73–84.CrossRefGoogle ScholarPubMed
Liebert, CA, Hall, RM and Summers, AO (1999). Transposon Tn21, flagship of the floating genome. Microbiology and Molecular Biology Reviews 63: 507–522.CrossRefGoogle ScholarPubMed
Linton, AH (1977). Animal to human transmission of Enterobacteriaceae. Royal Society of Health Journal 97: 115–118.CrossRefGoogle ScholarPubMed
Maguire, AJ, Brown, DFJ, Gray, JJ and Desselberger, U (2001). Rapid screening technique for class 1 integrons in Enterobacteriaceae and nonfermenting Gram-negative bacteria and its use in molecular epidemiology. Antimicrobial Agents and Chemotherapy 45: 1022–1029.CrossRefGoogle ScholarPubMed
Martin, SW, Meek, AH and Willeberg, P (1987). Veterinary Epidemiology. Principles and Methods. Ames: Iowa State University Press, pp. 121–148.Google Scholar
Martinez, JL and Baquero, F (2002). Interactions among strategies associated with bacterial infections: pathogenicity, epidemicity, and antibiotic resistance. Clinical Microbiology Reviews 15: 647–679.CrossRefGoogle ScholarPubMed
Maynard, C, Fairbrother, JM, Bekal, S, Sanschagrin, F, Levesque, RC, Brousseau, R, Masson, L, Lariviere, S and Harel, J (2003). Antimicrobial resistance genes in enterotoxigenic Escherichia coli O149: K91 isolates obtained over a 23-year period from pigs. Antimicrobial Agents and Chemotherapy 47: 3214–3221.CrossRefGoogle Scholar
Mazaitis, AJ, Maas, R and Maas, WK (1981). Structure of a naturally occurring plasmid with genes for enterotoxin production and drug resistance. Journal of Bacteriology 145: 97–105.CrossRefGoogle ScholarPubMed
McDermott, PF, Zhao, S, Wagner, DD, Simjee, S, Walke, RD and White, DG (2002). The food safety perspective of antibiotic resistance. Animal Biotechnology 13: 71–84.CrossRefGoogle ScholarPubMed
Murray, M (2002). Sampling bias in the molecular epidemiology of tuberculosis. Emerging Infectious Diseases 8: 363–369.CrossRefGoogle ScholarPubMed
Naas, T, Benaoudia, F, Lebrun, L and Nordmann, P (2001). Molecular identification of TEM-1 β-lactamase in a Pasteurella multocida isolate of human origin. European Journal of Clinical Microbiology and Infectious Diseases 20: 210–213.CrossRefGoogle Scholar
Ojeniyi, AA (1989). Direct transmission of Escherichia coli from poultry to humans. Epidemiology and Infection 103: 513–522.CrossRefGoogle ScholarPubMed
Oliveira, DC, Tomasz, A and de Lencastre, H (2002). Secrets of success of a human pathogen: molecular evolution of pandemic clones of methicillin-resistant Staphylococcus aureus. Lancet Infectious Disease 2: 180–189.CrossRefGoogle Scholar
O'Rourke, K (2003). Methicillin-resistant Staphylococcus aureus: an emerging problem in horses? Journal of the American Veterinary Medical Association 223: 1399–1400.Google ScholarPubMed
Perreten, V and Boerlin, P (2003). A new sulfonamide resistance gene (sul3) in Escherichia coli is widespread in the pig population of Switzerland. Antimicrobial Agents and Chemotherapy 47: 1169–1172.CrossRefGoogle ScholarPubMed
Roberts, MC (1996). Tetracycline resistance determinants: mechanisms of action, regulation of expression, genetic mobility, and distribution. FEMS Microbiology Reviews 19: 1–24.CrossRefGoogle ScholarPubMed
Rowe-Magnus, DA and Mazel, D (2002). The role of integrons in antibiotic resistance gene capture. International Journal of Medical Microbiology 292: 115–125.CrossRefGoogle ScholarPubMed
Salyers, AA and Shoemaker, NB (1996). Resistance gene transfer in anaerobes: new insights, new problems. Clinical Infectious Diseases 23 (Supplement 1): S36–43CrossRefGoogle ScholarPubMed
Sanchez, S, McCrackin, MA, Hudson, CR, Maier, M, Buffington, T, Dam, Q and Maurer, JJ (2002). Characterization of multidrug-resistant Escherichia coli isolates associated with nosocomial infections in dogs. Journal of Clinical Microbiology 40: 3586–3595.CrossRefGoogle ScholarPubMed
Schott, HC, Ewart, SL, Walker, RD, Dwyer, RM, Dietrich, S, Eberhart, SW, Kusey, J, Stick, JA and Derksen, FJ (2001). An outbreak of salmonellosis among horses at a veterinary teaching hospital. Journal of the American Veterinary Medical Association 218: 1152–1159.CrossRefGoogle Scholar
Schrag, SJ, Perrot, V and Levin, BR (1997). Adaptation to the fitness cost of antibiotic resistance in Escherichia coli. Proceedings of the Royal Society of London. Series B. Biological Sciences 264: 1287–1291.CrossRefGoogle Scholar
Seguin, JC, Walker, RD, Caron, JP, Kloss, WE, George, CG, Hollis, RJ, Jones, RN and Pfaller, MA (1999). Methicillin-resistant Staphylococcus aureus outbreak in a veterinary teaching hospital: Potential human-to-animal transmission. Journal of Clinical Microbiology 37: 1459–1463.CrossRefGoogle Scholar
Singer, RS, Atwill, ER, Carpenter, TE, Jeffrey, JS, Johnson, WO and Hirsch, DC (2001). Selection bias in epidemiological studies of infectious diseases using Escherichia coli and avian cellulitis as an example. Epidemiology and Infection 126: 139–145.CrossRefGoogle ScholarPubMed
Spratt, BG (1996). Antibiotic resistance: counting the cost. Current Biology 6: 1219–1221.CrossRefGoogle ScholarPubMed
Syvanen, M and Kado, CI (2002). Horizontal Gene Transfer. London: Academic Press.Google ScholarPubMed
Teale, CJ (2002). Antimicrobial resistance and the food chain. Journal of Applied Microbiology 92 (Supplement): 85S–89SCrossRefGoogle ScholarPubMed
Tomasz, A and de Lencastre, H (1997). Molecular microbiology and epidemiology: Coexistence or alliance? In: Wenzel, RP editor. Prevention and Control of Nosocomial Infections. Baltimore (MD): Williams & Wilkins, pp. 309–321.Google Scholar
van den Bogaard, AE and Stobberingh, EE (1999). Antibiotic usage in animals: impact on bacterial resistance and public health. Drugs 58: 589–607.CrossRefGoogle ScholarPubMed
Van den Bogaard, AE, Willems, R, London, N, Top, J and Stobberingh, EE (2002). Antibiotic resistance of faecal enterococci in poultry, poultry farmers and poultry slaughterers. Journal of Antimicrobial Chemotherapy 49: 497–505.CrossRefGoogle ScholarPubMed
Vandenesch, F, Naimi, T, Enright, MC, Lina, G, Nimmo, GR, Heffernan, H, Liassin, N, Bes, M, Greenland, T, Reverdy, M-E and Etienne, J (2003). Community-acquired methicillin-resistant Staphylococcus aureus carrying Panton–Valentine leukocidin genes: worldwide emergence. Emerging Infectious Diseases 9: 978–984.CrossRefGoogle ScholarPubMed
Wagner, BA, Dargatz, DA, Salman, MD, Morley, PS, Wittum, TE and Keefe, TJ (2002). Comparison of sampling techniques for measuring antimicrobial susceptibility of enteric Escherichia coli recovered from feedlot cattle. American Journal of Veterinary Research 63: 1662–1670.CrossRefGoogle ScholarPubMed
Wagner, B, Morley, PS, Dargatz, DA, Wittum, TE, Keefe, TJ and Salman, MD (2003). Short-term repeatability of measurements of antimicrobial susceptibility of Escherichia coli isolated from feces of feedlot cattle. Journal of Veterinary Diagnostic Investigation 15: 535–542.CrossRefGoogle ScholarPubMed
Wegener, HC, Aarestrup, FM, Jensen, LB, Hammerrum, AM and Bager, F (1999). Use of antimicrobial growth promoters in food animals and Enterococcus faecium resistance to therapeutic drugs in Europe. Emerging Infectious Diseases 5: 329–335.CrossRefGoogle ScholarPubMed
Werckenthin, C, Cardoso, M, Martel, J-L and Schwarz, S (2001) Antimicrobial resistance in staphylococci from animals with particular reference to bovine Staphylococcus aureus, porcine Staphylococcus hyicus, and canine Staphylococcus intermedius. Veterinary Research 32: 341–362.CrossRefGoogle ScholarPubMed
Whittle, G, Shoemaker, NB and Salyers, AA (2002). The role of Bacteroides conjugative transposons in the dissemination of antibiotic resistance genes. Cellular and Molecular Life Sciences 59: 2044–2054.CrossRefGoogle ScholarPubMed
Wu, J-R, Shieh, HK, Shien, J-H, Gong, S-R and Chang, P-C (2003). Molecular characterization of plasmids with antimicrobial resistant genes in avian isolates of Pasteurella multocida. Avian Diseases 47: 1384–1392.CrossRefGoogle ScholarPubMed