Hostname: page-component-f554764f5-nwwvg Total loading time: 0 Render date: 2025-04-09T12:45:47.180Z Has data issue: false hasContentIssue false
  • English
  • Français

Antimicrobial resistance in selected bacteria from poultry

Published online by Cambridge University Press:  22 December 2008

Carlton L. Gyles
Carlton L. Gyles*
Affiliation:
Department of Pathobiology, University of Guelph, Guelph, ON, Canada
*
E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

This paper reviews the present state of antimicrobial resistance (AMR) in the zoonotic bacteria Salmonella, Campylobacter jejuni and Campylobacter coli, and in Escherichia coli from chickens and turkeys. For Salmonella, the frequencies and patterns of AMR vary depending on time, region, serovar, the particular farm, layers versus broilers, and the antimicrobial agent. There is usually a higher frequency of AMR in Salmonella from turkeys compared with Salmonella from chickens. Clonal and horizontal transmission of AMR occur and there is concern about the spread of transmissible plasmids that encode extended spectrum cephalosporinases. Resistance to fluoroquinolones is generally low. For Campylobacter, resistance to tetracycline is usually at moderate to high frequency, resistance to quinolones/fluoroquinolones varies from low to high, and resistance to macrolides is usually low. There are high levels of fluoroquinolone resistance in some countries. Avian pathogenic E. coli are often highly resistant, especially to tetracycline, streptomycin, and sulfonamides. Plasmid-mediated resistance is common. High levels of resistance to ciprofloxacin have been reported from China. Commensal E. coli from poultry have similar patterns of resistance but at lower frequencies. Integron associated resistance occurs commonly in Salmonella and E. coli but has not been detected in Campylobacter.

Keywords

SalmonellaCampylobacterEscherichia coliplasmidsintegrons
Type
Review Article
Information
Animal Health Research Reviews , Volume 9 , Issue 2: Symposium on Antimicrobial Resistance in Bacteria from Animals , December 2008 , pp. 149 - 158
Copyright
Copyright © Cambridge University Press 2008

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.)

Article purchase

Temporarily unavailable

References

Al-Zenki, S, Al-Nasser, A, Al-Safar, A, Alomirah, H, Al-Haddad, A, Hendriksen, RS and Aarestrup, FM (2007). Prevalence and antibiotic resistance of Salmonella isolated from a poultry farm and processing plant environment in the State of Kuwait. Foodborne Pathogens and Disease 4: 367–373.CrossRefGoogle ScholarPubMed
Andrysiak, AK, Olson, AB, Tracz, DM, Dore, K, Irwin, R, Ng, LK, Gilmour, MW and Canadian Integrated Program for Antimicrobial Resistance Surveillance Collaborative (2008). Genetic characterization of clinical and agri-food isolates of multi drug resistant Salmonella enterica serovar Heidelberg from Canada. BMC Microbiology 8: 89.Google Scholar
Asai, T, Esaki, H, Kojima, A, Ishihara, K, Tamura, Y and Takahashi, T (2006). Antimicrobial resistance in Salmonella isolates from apparently healthy food-producing animal from 2000 to 2003: the first stage of Japanese veterinary antimicrobial resistance monitoring (JVARM) [erratum appears in Journal of Veterinary Medical Sciences 2006; 68(10):2 p following 1141]. Journal of Veterinary Medical Sciences 68: 881–884.CrossRefGoogle Scholar
Avrain, L, Humbert, F, L'Hospitalier, R, Sanders, P, Vernozy-Rozand, C and Kempf, I (2003). Antimicrobial resistance in Campylobacter from broilers: association with production type and antimicrobial use. Veterinary Microbiology 96: 267–276.CrossRefGoogle ScholarPubMed
Boonmar, S, Morita, Y, Fujita, M, Sangsuk, L, Suthivarakom, K, Padungtod, P, Maruyama, S, Kabeya, H, Kato, M, Kozawa, K, Yamamoto, S and Kimura, H (2007). Serotypes, antimicrobial susceptibility, and gyrA gene mutation of Campylobacter jejuni isolates from humans and chickens in Thailand. Microbiology and Immunology 51: 531–537.CrossRefGoogle ScholarPubMed
Boscán-Duque, LA, Arzálluz-Fisher, AM, Ugarte, C, Sánchez, D, Wittum, TE and Hoet, AE (2007). Reduced susceptibility to quinolones among Salmonella serotypes isolated from poultry at slaughter in Venezuela. Journal of Food Protection 70: 2030–2035.CrossRefGoogle ScholarPubMed
Bywater, RJ (2005). Identification and surveillance of antimicrobial resistance dissemination in animal production. Poultry Science 84: 644–648.Google Scholar
Bywater, R, Deluyker, H, Deroover, E, de Jong, A, Marion, H, McConville, M, Rowan, T, Shryock, T, Shuster, D, Thomas, V, Vallé, M and Walters, J (2004). A European survey of antimicrobial susceptibility among zoonotic and commensal bacteria isolated from food-producing animals. Journal of Antimicrobial Chemotherapy 54: 744–754.CrossRefGoogle ScholarPubMed
Chuma, T, Ikeda, T, Maeda, T, Niwa, H and Okamoto, K (2001). Antimicrobial susceptibilities of Campylobacter strains isolated from broilers in the southern part of Japan from 1995 to 1999. Journal of Veterinary Medical Sciences 63: 1027–1029.CrossRefGoogle ScholarPubMed
CIPARS (2005). Canadian Integrated Program for Antimicrobial Resistance Surveillance (CIPARS) 2005. Available online at http://www.phac-aspc.gc.ca/cipars-picra/2005_pr-eng.php (Accessed 7 October 2008).Google Scholar
Cloeckaert, A, Praud, K, Doublet, B, Bertini, A, Carattoli, A, Butaye, P, Imberechts, H, Bertrand, S, Collard, JM, Arlet, G and Weill, FX (2007). Dissemination of an extended-spectrum-beta-lactamase blaTEM-52 gene-carrying IncI1 plasmid in various Salmonella enterica serovars isolated from poultry and humans in Belgium and France between 2001 and 2005. Antimicrobial Agents and Chemotherapy 51: 1872–1875.CrossRefGoogle ScholarPubMed
Douris, A, Fedorka-Cray, PJ and Jackson, CR (2008). Characterization of Salmonella enterica serovar Agona slaughter isolates from the animal arm of the National Antimicrobial Resistance Monitoring System-Enteric Bacteria (NARMS): 1997 through 2003. Microbial Drug Resistance 14: 55–63.Google Scholar
Frye, JG and Fedorka-Cray, PJ (2007). Prevalence, distribution and characterisation of ceftiofur resistance in Salmonella enterica isolated from animals in the USA from 1999 to 2003. International Journal of Antimicrobial Agents 30: 134–142.Google Scholar
Gallay, A, Prouzet-Mauléon, V, Kempf, I, Lehours, P, Labadi, L, Camou, C, Denis, M, de Valk, H, Desenclos, JC and Mégraud, F (2007). Campylobacter antimicrobial drug resistance among humans, broiler chickens, and pigs, France. Emerging Infectious Diseases 13: 259–266.CrossRefGoogle ScholarPubMed
Johnson, JR, Sannes, MR, Croy, C, Johnston, B, Clabots, C, Kuskowski, MA, Bender, J, Smith, KE, Winokur, PL and Belongia, EA (2007). Antimicrobial drug-resistant Escherichia coli from humans and poultry products, Minnesota and Wisconsin, 2002–2004. Emerging Infectious Diseases 13: 838–846.Google Scholar
Johnson, TJ, Siek, KE, Johnson, SJ and Nolan, LK (2005). DNA sequence and comparative genomics of pAPEC-O2-R, an avian pathogenic Escherichia coli transmissible R plasmid. Antimicrobial Agents and Chemotherapy 49: 4681–4688.CrossRefGoogle ScholarPubMed
Johnson, TJ, Wannemeuhler, YM, Scaccianoce, JA, Johnson, SJ and Nolan, LK (2006). Complete DNA sequence, comparative genomics, and prevalence of an IncHI2 plasmid occurring among extraintestinal pathogenic Escherichia coli isolates. Antimicrobial Agents and Chemotherapy 50: 3929–3933.CrossRefGoogle ScholarPubMed
Kaldhone, P, Nayak, R, Lynne, AM, David, DE, McDermott, PF, Logue, CM and Foley, SL (2008). Characterization of Salmonella enterica serovar Heidelberg from turkey-associated sources. Applied and Environmental Microbiology 74: 5038–5046.CrossRefGoogle ScholarPubMed
Kang, YS, Cho, YS, Yoon, SK, Yu, MA, Kim, CM, Lee, JO and Pyun, YR (2006). Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from raw chicken meat and human stools in Korea. Journal of Food Protection 69: 2915–2923.Google Scholar
Ladely, SR, Harrison, MA, Fedorka-Cray, PJ, Berrang, ME, Englen, MD and Meinersmann, RJ (2007). Development of macrolide-resistant Campylobacter in broilers administered subtherapeutic or therapeutic concentrations of tylosin. Journal of Food Protection 70: 1945–1951.Google Scholar
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.Google Scholar
Larkin, C, Van Donkersgoed, C, Mahdi, A, Johnson, P, McNab, B and Odumeru, J (2006). Antibiotic resistance of Campylobacter jejuni and Campylobacter coli isolated from hog, beef, and chicken carcass samples from provincially inspected abattoirs in Ontario. Journal of Food Protection 69: 22–26.Google Scholar
Lee, LA, Threatt, VL, Puhr, ND, Levine, P, Ferris, K and Tauxe, RV (1993). Antimicrobial-resistant Salmonella spp. isolated from healthy broiler chickens after slaughter. Journal of the American Veterinary Medical Association 202: 752–755.CrossRefGoogle ScholarPubMed
Li, X, Payne, JB, Santos, FB, Levine, JF, Anderson, KE and Sheldon, BW (2007a). Salmonella populations and prevalence in layer feces from commercial high-rise houses and characterization of the Salmonella isolates by serotyping, antibiotic resistance analysis, and pulsed field gel electrophoresis. Poultry Science 86: 591–597.Google Scholar
Li, XS, Wang, GQ, Du, XD, Cui, BA, Zhang, SM and Shen, JZ (2007b). Antimicrobial susceptibility and molecular detection of chloramphenicol and florfenicol resistance among Escherichia coli isolates from diseased chickens. Journal of Veterinary Science 8: 243–247.CrossRefGoogle ScholarPubMed
Lynne, AM, Rhodes-Clark, BS, Bliven, K, Zhao, S and Foley, SL (2008). Antimicrobial resistance genes associated with Salmonella enterica serovar Newport isolates from food animals. Antimicrobial Agents and Chemotherapy 52: 353–356.Google Scholar
Miflin, JK, Templeton, JM and Blackall, PJ (2007). Antibiotic resistance in Campylobacter jejuni and Campylobacter coli isolated from poultry in the South-East Queensland region. Journal of Antimicrobial Chemotherapy 59: 775–778.CrossRefGoogle ScholarPubMed
Moniri, R and Dastehgoli, K (2005). Fluoroquinolone-resistant Escherichia coli isolated from healthy broilers with previous exposure to fluoroquinolones: is there a link? Microbial Ecology in Health and Disease 17: 69–74.Google Scholar
Moore, JE, Barton, MD, Blair, IS, Corcoran, D, Dooley, JS, Fanning, S, Kempf, I, Lastovica, AJ, Lowery, CJ, Matsuda, M, McDowell, DA, McMahon, A, Millar, BC, Rao, JR, Rooney, PJ, Seal, BS, Snelling, WJ and Tolba, O (2006). The epidemiology of antibiotic resistance in Campylobacter. Microbes and Infection 8: 1955–1966.Google Scholar
Musgrove, MT, Jones, DR, Northcutt, JK, Cox, NA, Harrison, MA, Fedorka-Cray, PJ and Ladely, SR (2006). Antimicrobial resistance in Salmonella and Escherichia coli isolated from commercial shell eggs. Poultry Science 85: 1665–1669.CrossRefGoogle ScholarPubMed
NARMS (2006). 2006 NARMS Retail Meat Annual Report. National Antimicrobial Resistance Monitoring System. Available online at http://www.fda.gov/cvm/2006NARMSAnnualRpt.htm (Accessed 7 October 2008).Google Scholar
Nayak, R, Call, V, Kaldhone, P, Tyler, C, Anderson, G, Phillips, S, Kerdahi, K and Foley, SL (2007). Comparison of Salmonella enterica serovar Heidelberg susceptibility testing results. Clinical Medicine and Research 5: 98–105.Google Scholar
Nde, CW and Logue, CM (2008). Characterization of antimicrobial susceptibility and virulence genes of Salmonella serovars collected at a commercial turkey processing plant. Journal of Applied Microbiology 104: 215–223.Google Scholar
Nelson, JM, Chiller, TM, Powers, JH and Angulo, FJ (2007). Fluoroquinolone-resistant Campylobacter species and the withdrawal of fluoroquinolones from use in poultry: a public health success story. Clinical Infectious Diseases 44: 977–980.CrossRefGoogle ScholarPubMed
Nógrády, N, Tóth, A, Kostyák, A, Pászti, J and Nagy, B (2007). Emergence of multidrug-resistant clones of Salmonella Infantis in broiler chickens and humans in Hungary. Journal of Antimicrobial Chemotherapy 60: 645–648.Google Scholar
Padungton, P and Kaneene, JB (2003). Campylobacter spp. in human, chickens, pigs and their antimicrobial resistance. Journal of Veterinary Medical Sciences 65: 161–170.CrossRefGoogle ScholarPubMed
Parveen, S, Taabodi, M, Schwarz, JG, Oscar, TP, Harter-Dennis, J and White, DG (2007). Prevalence and antimicrobial resistance of Salmonella recovered from processed poultry. Journal of Food Protection 70: 2466–2472.Google Scholar
Petersen, A, Christensen, JP, Kuhnert, P, Bisgaard, M and Olsen, JE (2006). Vertical transmission of a fluoroquinolone-resistant Escherichia coli within an integrated broiler operation. Veterinary Microbiology 116: 120–128.CrossRefGoogle ScholarPubMed
Piddock, LJ, Griggs, D, Johnson, MM, Ricci, V, Elviss, NC, Williams, LK, Jørgensen, F, Chisholm, SA, Lawson, AJ, Swift, C, Humphrey, TJ and Owen, RJ (2008). Persistence of Campylobacter species, strain types, antibiotic resistance and mechanisms of tetracycline resistance in poultry flocks treated with chlortetracycline. Journal of Antimicrobial Chemotherapy 62: 303–315.Google Scholar
Poppe, C, Ayroud, M, Ollis, G, Chirino-Trejo, M, Smart, N, Quessy, S and Michel, P (2001). Trends in antimicrobial resistance of Salmonella isolated from animals, foods of animal origin, and the environment of animal production in Canada, 1994–1997. Microbial Drug Resistance 7: 197–212.Google Scholar
Poppe, C, Martin, L, Muckle, A, Archambault, M, McEwen, S and Weir, E (2006a). Characterization of antimicrobial resistance of Salmonella Newport isolated from animals, the environment, and animal food products in Canada. Canadian Journal of Veterinary Research 70: 105–114.Google ScholarPubMed
Poppe, C, Martin, LC, Gyles, CL, Reid-Smith, R, Boerlin, P, McEwen, SA, Prescott, JF and Forward, KR (2006b). Acquisition of resistance to extended-spectrum cephalosporins by Salmonella enterica subsp. enterica serovar Newport and Escherichia coli in the turkey poult intestinal tract. Applied and Environmental Microbiology 71: 1184–1192.Google Scholar
Price, LB, Graham, JP, Lackey, LG, Roess, A, Vailes, R and Silbergeld, E (2007). Elevated risk of carrying gentamicin-resistant Escherichia coli among U.S. poultry workers. Environmental Health Perspectives 115: 1738–1742.Google Scholar
Riaño, I, Moreno, MA, Teshager, T, Sáenz, Y, Domínguez, L and Torres, C (2006). Detection and characterization of extended-spectrum beta-lactamases in Salmonella enterica strains of healthy food animals in Spain. Journal of Antimicrobial Chemotherapy 58: 844–847.Google Scholar
Roasto, M, Juhkam, K, Tamme, T, Hörman, A, Häkkinen, L, Reinik, M, Karus, A and Hänninen, ML (2007). High level of antimicrobial resistance in Campylobacter jejuni isolated from broiler chickens in Estonia in 2005 and 2006. Journal of Food Protection 70: 1940–1944.CrossRefGoogle ScholarPubMed
Santos, FB, Dsouza, DH, Jaykus, L, Ferket, PR and Sheldon, BW (2007). Genotypes, serotypes, and antibiotic resistance profiles of Salmonella isolated from commercial North Carolina turkey farms. Journal of Food Protection 70: 1328–1333.Google Scholar
Shahada, F, Chuma, T, Tobata, T, Okamoto, K, Sueyoshi, M and Takase, K (2006). Molecular epidemiology of antimicrobial resistance among Salmonella enterica serovar Infantis from poultry in Kagoshima, Japan. International Journal of Antimicrobial Agents 28: 302–307.Google Scholar
Smet, A, Martel, A, Persoons, D, Dewulf, J, Heyndrickx, M, Catry, B, Herman, L, Haesebrouck, F and Butaye, P (2008). Diversity of extended-spectrum beta-lactamases and class C beta-lactamases among cloacal Escherichia coli Isolates in Belgian broiler farms. Antimicrobial Agents and Chemotherapy 52: 1238–1243.CrossRefGoogle Scholar
Snow, LC, Davies, RH, Christiansen, KH, Carrique-Mas, JJ, Wales, AD, O'Connor, JL, Cook, AJ and Evans, SJ (2007). Survey of the prevalence of Salmonella species on commercial laying farms in the United Kingdom. Veterinary Record 161: 471–476.CrossRefGoogle ScholarPubMed
Son, I, Englen, MD, Berrang, ME, Fedorka-Cray, PJ and Harrison, MA (2007). Antimicrobial resistance of Arcobacter and Campylobacter from broiler carcasses. International Journal of Antimicrobial Agents 29: 451–455.Google Scholar
Thorsteinsdottir, TR, Kristinsson, KG, Fridriksdottir, V and Gunnarsson, E (2008). Antimicrobial resistance of Campylobacter spp. isolated from broiler flocks in Iceland 2001–2005. Microbial Drug Resistance 14: 49–53.CrossRefGoogle ScholarPubMed
van Boven, M, Veldman, KT, de Jong, MC and Mevius, DJ (2003). Rapid selection of quinolone resistance in Campylobacter jejuni but not in Escherichia coli in individually housed broilers. Journal of Antimicrobial Chemotherapy 52: 719–723.Google Scholar
van Duijkeren, E, Wannet, WJ, Houwers, DJ and van Pelt, W (2003). Antimicrobial susceptibilities of salmonella strains isolated from humans, cattle, pigs, and chickens in the Netherlands from 1984 to 2001. Journal of Clinical Microbiology 41: 3574–3578.CrossRefGoogle ScholarPubMed
White, DG, Zhao, S, Singh, R and McDermott, PF (2004). Antimicrobial resistance among gram-negative foodborne bacterial pathogens associated with foods of animal origin. Foodborne Pathogens and Disease 1: 137–152.CrossRefGoogle ScholarPubMed
Yang, H, Chen, S, White, DG, Zhao, S, McDermott, P, Walker, R, and Meng, J (2004). Characterization of multiple-antimicrobial-resistant Escherichia coli isolates from diseased chickens and swine in China. Journal of Clinical Microbiology 42: 3483–3489.Google Scholar
Yue, L, Jiang, HX, Liao, XP, Liu, JH, Li, SJ, Chen, XY, Chen, CX, Lü, DH and Liu, YH (2008). Prevalence of plasmid-mediated quinolone resistance qnr genes in poultry and swine clinical isolates of Escherichia coli. Veterinary Microbiology. 132: 414–420.Google Scholar
Zaidi, MB, Calva, JJ, Estrada-Garcia, MT, Leon, V, Vazquez, G, Figueroa, G, Lopez, E, Contreras, J, Abbott, J, Zhao, S, McDermott, P and Tollefson, L (2008). Integrated food chain surveillance system for Salmonella spp. in Mexico. Emerging Infectious Diseases 14: 429–435.CrossRefGoogle ScholarPubMed
Zhang, Q, Lin, J and Pereira, S (2003). Fluoroquinolone-resistant Campylobacter in animal reservoirs: dynamics of development, resistance mechanisms and ecological fitness. Animal Health Research Reviews 4: 63–71.Google Scholar
Zhao, S, Fedorka-Cray, PJ, Friedman, S, McDermott, PF, Walker, RD, Qaiyumi, S, Foley, SL, Hubert, SK, Ayers, S, English, L, Dargatz, DA, Salamone, B and White, DG (2005a). Characterization of Salmonella Typhimurium of animal origin obtained from the National Antimicrobial Resistance Monitoring System. Foodborne Pathogens and Disease 2: 169–181.CrossRefGoogle ScholarPubMed
Zhao, S, Maurer, JJ, Hubert, S, De Villena, JF, McDermott, PF, Meng, J, Ayers, S, English, L and White, DG (2005b). Antimicrobial susceptibility and molecular characterization of avian pathogenic Escherichia coli isolates. Veterinary Microbiology 107: 215–224.Google Scholar
Zhao, S, McDermott, PF, White, DG, Qaiyumi, S, Friedman, SL, Abbott, JW, Glenn, A, Ayers, SL, Post, KW, Fales, WH, Wilson, RB, Reggiardo, C and Walker, RD (2007). Characterization of multidrug resistant Salmonella recovered from diseased animals. Veterinary Microbiology 123: 122–132.CrossRefGoogle ScholarPubMed
Zhao, S, White, DG, Friedman, SL, Glenn, A, Blickenstaff, K, Ayers, SL, Abbott, JW, Hall-Robinson, E and McDermott, PF (2008). Antimicrobial resistance in Salmonella enterica serovar Heidelberg from Retail Meat and Poultry, 2002–2006. Applied and Environmental Microbiology 74: 6656–6662.Google Scholar