Antibiotic Susceptibility of Salmonella, Campylobacter coli, and Campylobacter jejuni Isolated from Northern German Fattening Pigs

Journal of Food Protection

Volumn 75, Issue 10, 2012, Pages 1839-1845

  Dohne S ^a   Merle, R ^a   Altrock, A V ^a   Waldmann, K H ^a   Verspohl, J ^a   Gruning P ^a   Hamedy, A ^b   Kreienbrock, L ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84904680991     PISSN: 0362028X     EISSN: 19449097     Source Type: Journal    
DOI: 10.4315/0362-028X.JFP-12-051     Document Type: Article

References (70)

1. Aarestrup, F.M., McDermott, P.F., Wegener, H.C., Transmission of antibiotic resistance from food animals to humans. Nachamkin, I., Szymanski, C.M., Blaser, M.J., (eds.) Campylobacter, 3rd ed, 2008, ASM Press, Washington, DC, 645–665.
2. Alter, T., Gaull, F., Kasimir, S., Gurtler, M., Mielke, H., Linnebur, M., Fehlhaber, K., Prevalences and transmission routes of Campylobacter spp. strains within multiple pig farms. Vet. Microbiol. 108 (2005), 251–261.
3. Anderson, E.S., Ward, L.R., Saxe, M.J., de Sa, J.D., Bacteriophage-typing designations of Salmonella typhimurium. J. Hyg. 78 (1977), 297–300.
4. Anonymous, Verordnung (EG) Nr 2160/2003 des europäischen Parlaments und des Rates vom 17 November 2003 zur Bekämpfung von Salmonellen und bestimmten anderen durch Lebensmittel übertragbaren Zoonoseerregern. Amtsblatt Europäischen Union L 325 (2003), 1–15.
5. Anonymous, DANMAP 2007—use of antimicrobial agents and occurrence of antimicrobial resistance in bacteria from food animals, foods and humans in Denmark, 2007, National Food Institute Technical University of Denmark, Danish Zoonosis Centre, Soborg.
6. Anonymous, Verordnung zur Verminderung der Salmonellenver-breitung durch Schlachtschweine (Schweine-Salmonellen-Verordnung). Bundesgesetzbl.I (ed.), Schweine-Salmonellen-Verordnung vom 13. März 2007 (BGBl. I S. 322), 2007, Bundesministerium für Justiz, Bonn, 322.
7. Bahnson, P., Damman, D., Isaacson, R., Miller, G., Weigel, R., Troutt, F., Prevalence and serovars of Salmonella enterica isolated from ileocolic lymph nodes of market pigs reared in selected Midwest US swine herds. J. Swine Health Prod. 14 (2006), 182–188.
8. Bengtsson, B., Greko, C., Grönlund-Andersson, U., SVARM 2007—Swedish Veterinary Antimicrobial Resistance Monitoring, 2007, National Veterinary Institute, Uppsala Available at www.sva.se, Accessed 21 May 2009.
9. Blaser, M.J., Engberg, J., Clinical aspects of Campylo-bacter jejuni and Campylobacter coli infections. Nachamkin, I., Szymanski, C.M., Blaser, M.J., (eds.) Campylobac-ter, 3rd ed, 2008, ASM Press, Washington, DC, 99–121.
10. Botteldoorn, N., Heyndrickx, M., Rijpens, N., Grijspeerdt, K., Herman, L., Salmonella on pig carcasses: positive pigs and cross contamination in the slaughterhouse. J. Appl. Microbiol. 95 (2003), 891–903.
11. Busani, L., Graziani, C., Battisti, A., Franco, A., Ricci, A., Vio, D., Digiannatale, E., Paterlini, F., D'Incau, M., Owczarek, S., Caprioli, A., Luzzi, I., Antibiotic resistance in Salmonella enterica serotypes Typhimurium, Enteritidis and Infantis from human infections, foodstuffs and farm animals in Italy. Epidemiol. Infect. 132 (2004), 245–251.
12. Carlson, A., Blaha, T., In-herd prevalence of Salmonella in 25 selected Minnesota swine farms. J. Swine Health Prod. 9 (2001), 7–10.
13. Clinical and Laboratory Standards Institute (CLSI), Methods for antimicrobial dilution and disk susceptibility testing of infrequently isolated or fastidious bacteria. Approved guideline. Document M45-A, 2006, CLSI, Wayne, PA.
14. Clinical and Laboratory Standards Institute (CLSI), Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. Approved standard, 8th ed. Document M07-A8, 2009, CLSI, Wayne, PA.
15. Clinical and Laboratory Standards Institute (CLSI), Performance standards for antimicrobial susceptibility testing. Nineteenth informational supplement. Document M100-S19, 2009, CLSI, Wayne, PA.
16. Cloeckaert, A., Schwarz, S., Molecular characterization, spread and evolution of multidrug resistance in Salmonella enterica typhimurium DT104. Vet. Res. 32 (2001), 301–310.
17. De Busser, E.V., Dewulf, J., Nollet, N., Houf, K., Schwarzer, K., De Sadeleer, L., De Zutter, L., Maes, D., Effect of organic acids in drinking water during the last 2 weeks prior to slaughter on Salmonella shedding by slaughter pigs and contamination of carcasses. Zoonoses Public Health 56 (2009), 129–136.
18. De Jong, A., Bywater, R., Butty, P., Deroover, E., Godinho, K., Klein, U., Marion, H., Simjee, S., Smets, K., Thomas, V., Valle, M., Wheadon, A., A pan-European survey of antimicrobial susceptibility towards human-use antimicrobial drugs among zoonotic and commensal enteric bacteria isolated from healthy food-producing animals. J. Antimicrob. Chemother. 63 (2009), 733–744.
19. De Jong, A., S. Simjee, A. Wheadon, P. Butty, K. Goddinho, U. Klein, H. Marion, T. Shryock, K. Smets, V. Thomas, and M. Vallé. 2009. Antimicrobial susceptibility of food-borne bacteria (Salmonella, Campylobacter) from cattle, pigs and chickens (2002–2004) recovered from 8 EU countries (EASSA program). Presented at the 19th European Congress of Clinical Microbiology and Infectious Diseases, Helsinki, Finland, 16 to 19 May 2009.
20. Devine, R., Meat consumption trends in the world and the European Union. Natl. Renderers Assoc. Prod. Anim. 16 (2003), 325–327.
21. European Food Safety Authority, The community summary report on trends and sources of zoonoses, zoonotic agents, antimicrobial resistance and foodborne outbreaks in the European Union in 2005. EFSA J. 94 (2006), 76–288.
22. European Food Safety Authority, Report including a proposal for a harmonized monitoring scheme of antimicrobial resistance in Salmonella in fowl (Gallus gallus), turkeys, and pigs and Campylobacter jejuni and C. coli in broilers and turkeys. EFSA J. 96 (2007), 1–46.
23. European Food Safety Authority, Harmonised monitoring of antimicrobial resistance in Salmonella and Campylobacter isolates from food animals in the European Union. Clin. Microbiol. Infect. 14 (2008), 522–533.
24. European Food Safety Authority, The Community Summary Report: trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in the European Union in 2008. EFSA J., 8, 2010, 1496.
25. Fosse, J., Oudot, A., Rossero, M., Laroche, M., Contamination de produits primaires porcins par Campylobacter spp., Clostridium perfringens et Salmonella enterica. J. Rech. Porc. France 40 (2008), 55–60.
26. Fosse, J., Seegers, H., Magras, C., Prevalence and risk factors for bacterial food-borne zoonotic hazards in slaughter pigs: a review. Zoonoses Public Health 56 (2009), 429–454.
27. Gebreyes, W.A., Thakur, S., Davies, P.R., Funk, J.A., Altier, C., Trends in antimicrobial resistance, phage types and integrons among Salmonella serotypes from pigs, 1997–2000. J. Antimicrob. Chemother. 53 (2004), 997–1003.
28. Gillespie, I.A., O'Brien, S.J., Frost, J.A., Adak, G.K., Horby, P., Swan, A.V., Painter, M.J., Neal, K.R., A case-case comparison of Campylobacter coli and Campylobacter jejuni infection: a tool for generating hypotheses. Emerg. Infect. Dis. 8 (2002), 937–942.
29. Gonzalez, I., Grant, K.A., Richardson, P.T., Park, S.F., Collins, M.D., Specific identification of the enteropathogens Campylobacter jejuni and Campylobacter coli by using a PCR test based on the ceuE gene encoding a putative virulence determinant. J. Clin. Microbiol. 35 (1997), 759–763.
30. Görgen, M., Kirpal, G., Bisping, W., Untersuchungen zum Vorkommen von Keimen der Gattung Campylobacter beim Schwein Teil I: Kulturelle Untersuchungen von Kot, Darminhalt und Gallenblasen sowie Infektionsversuche. Berl. Münch. Tierärztl. Wochenschr. 96 (1983), 86–89.
31. Guevremont, E., Higgins, R., Quessy, S., Characterization of Campylobacter isolates recovered from clinically healthy pigs and from sporadic cases of campylobacteriosis in humans. J. Food Prot. 67 (2004), 228–234.
32. Guevremont, E., Nadeau, E., Sirois, M., Quessy, S., Antimicrobial susceptibilities of thermophilic Campylobacter from humans, swine, and chicken broilers. Can. J. Vet. Res. 70 (2006), 81–86.
33. Gurtler, M., Alter, T., Kasimir, S., Fehlhaber, K., The importance of Campylobacter coli in human campylobacteriosis: prevalence and genetic characterization. Epidemiol. Infect. 133 (2005), 1081–1087.
34. Hänel, I., Alter, T., Backert, S., 25. Jenaer Symposium: Campylobacter-Infektionen. Bundesgesundheitsblatt Gesundheits-forschung Gesundheitsschutz 51 (2008), 1347–1352.
35. Harvey, R.B., Anderson, R.C., Young, C.R., Hume, M.E., Genovese, K.J., Ziprin, R.L., Farrington, L.A., Stanker, L.H., Nisbet, D.J., Prevalence of Campylobacter, SalmonellaArcobacter species at slaughter in market age pigs. Adv. Exp. Med. Biol. 473 (1999), 237–239.
36. Helms, M., Ethelberg, S., Molbak, K., International Salmonella Typhimurium DT104 infections, 1992–2001. Emerg. Infect. Dis. 11 (2005), 859–867.
37. Helms, M., Simonsen, J., Olsen, K.E., Molbak, K., Adverse health events associated with antimicrobial drug resistance in Campylobacter species: a registry-based cohort study. J. Infect. Dis. 191 (2005), 1050–1055.
38. Helms, M., Vastrup, P., Gerner-Smidt, P., Molbak, K., Excess mortality associated with antimicrobial drug-resistant Salmonella Typhimurium. Emerg. Infect. Dis. 8 (2002), 490–495.
39. Hohmann, E.L., Nontyphoidal salmonellosis. Clin. Infect. Dis. 32 (2001), 263–269.
40. Jacobs-Reitsma, W.F., Lyhs, U., Wagenaar, J., Campylo-bacter in the food supply. Nachamkin, I., Szymanski, C.M., Blaser, M.J., (eds.) Campylobacter, 3rd ed, 2008, American Society for Microbiology, Washington, DC, 627–644.
41. Kaesbohrer, A., Protz, D., Helmuth, R., Noeckler, K., Blaha, T., Conraths, F.J., Geue, L., Salmonella in slaughter pigs of German origin: an epidemiological study. Eur. J. Epidemiol. 16 (2000), 141–146.
42. Kahlmeter, G., Brown, D.F., Goldstein, F.W., MacGowan, A.P., Mouton, J.W., Osterlund, A., Rodloff, A., Steinbakk, M., Urbaskova, P., Vatopoulos, A., European harmonization of MIC break-points for antimicrobial susceptibility testing of bacteria. J. Antimicrob. Chemother. 52 (2003), 145–148.
43. Litrup, E., Torpdahl, M., Nielsen, E.M., Multilocus sequence typing performed on Campylobacter coli isolates from humans, broilers, pigs and cattle originating in Denmark. J. Appl. Microbiol. 103 (2007), 210–218.
44. Luangtongkum, T., Jeon, B., Han, J., Plummer, P., Logue, C.M., Zhang, Q., Antibiotic resistance in Campylobacter: emergence, transmission and persistence. Future Microbiol. 4 (2009), 189–200.
45. Maguire, H.C.F., Codd, A.A., Mackay, V.E., Rowe, B., Mitchell, E., A large outbreak of human salmonellosis traced to a local pig farm. Epidemiol. Infect. 110 (1993), 239–246.
46. Marshall, S.M., Melito, P.L., Woodward, D.L., Johnson, W.M., Rodgers, F.G., Mulvey, M.R., Rapid identification of Campylobacter, ArcobacterHelicobacter isolates by PCR-restriction fragment length polymorphism analysis of the 16S rRNA gene. J. Clin. Microbiol. 37 (1999), 4158–4160.
47. Merle, R., Hajek, P., Hegger-Gravenhorst, C., Mollenhauer, Y., Robanus, M., Käsbohrer, A., Ungemach, F.R., Kreienbrock, L., Consumption of antibiotics in livestock in Germany: feasibility and outlook. Zoonosen und Lebensmittelsicherheit, 2009, BfR-Symposium, Berlin, 87–92 2 to 3 November 2009.
48. Molbak, K., Baggesen, D.L., Aarestrup, F.M., Ebbesen, J.M., Engberg, J., Frydendahl, K., Gerner-Smidt, P., Petersen, A.M., Wegener, H.C., An outbreak of multidrug-resistant, quinolone-resistant Salmonella enterica serotype typhimurium DT104. N. Engl. J. Med. 341 (1999), 1420–1425.
49. Moore, J.E., Corcoran, D., Dooley, J.S.G., Fanning, S., Lucey, B., Matsuda, M., McDowell, D.A., Megraud, F., Millar, B.C., O'Mahony, R., O'Riordan, L., O'Rourke, M., Rao, J.R., Rooney, P.J., Sails, A., Whyte, P., Campylobacter. Vet. Res. 36 (2005), 351–382.
50. Nesbakken, T., Eckner, K., Hoidal, H.K., Rotterud, O.J., Occurrence of Yersinia enterocolitica and Campylobacter spp. in slaughter pigs and consequences for meat inspection, slaughtering, and dressing procedures. Int. J. Food Microbiol. 80 (2003), 231–240.
51. Nollet, N., Maes, D., De Zutter, L., Duchateau, L., Houf, K., Huysmans, K., Imberechts, H., Geers, R., de Kruif, A., Van Hoof, J., Risk factors for the herd-level bacteriologic prevalence of Salmonella in Belgian slaughter pigs. Prev. Vet. Med. 65 (2004), 63–75.
52. Nowak, B., von Muffling, T., Chaunchom, S., Hartung, J., Salmonella contamination in pigs at slaughter and on the farm: a field study using an antibody ELISA test and a PCR technique. Int. J. Food Microbiol. 115 (2007), 259–267.
53. Oosterom, J., Dekker, R., Dewilde, G.J.A., Vankempendetroye, F., Engels, G.B., Prevalence of Campylobacter jejuni und Salmonella during pig slaughtering. Vet. Q. 7 (1985), 31–34.
54. Payot, S., Dridi, S., Laroche, M., Federighi, M., Magras, C., Prevalence and antimicrobial resistance of Campylobacter coli isolated from fattening pigs in France. Vet. Microbiol. 101 (2004), 91–99.
55. Popoff, M.Y., Bockemühl, J., Gheesling, L.L., Supplement 2002 (no. 46) to the Kauffmann-White scheme. Res. Microbiol. 155 (2004), 568–570.
56. Saenz, Y., Zarazaga, M., Lantero, M., Gastanares, M.J., Baquero, F., Torres, C., Antibiotic resistance in Campylobacter strains isolated from animals, foods, and humans in Spain in 1997–1998. Antimicrob. Agents Chemother. 44 (2000), 267–271.
57. Salyers, A.A., Amabile-Cuevas, C.F., Why are antibiotic resistance genes so resistant to elimination? Antimicrob. Agents Chemother. 41 (1997), 2321–2325.
58. Schneidereit, M., Antibiotikaverbrauch in der Veterinärmedizin, sect. 3. GERMAP 2008: Antibiotika-Resistenz und -Verbrauch. Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, Paul-Ehrlich-Gesellschaft für Chemotherapie e.V., 2008, Institut für Infektiologie, Freiburg, Germany.
59. Schuppers, M.E., Stephan, R., Ledergerber, U., Danuser, J., Bissig-Choisat, B., Stark, K.D., Regula, G., Clinical herd health, farm management and antimicrobial resistance in Campylobacter coli on finishing pig farms in Switzerland. Prev. Vet. Med. 69 (2005), 189–202.
60. Schwarz, S., Chaslus-Dancla, E., Use of antimicrobials in veterinary medicine and mechanisms of resistance. Vet. Res. 32 (2001), 201–225.
61. Shin, E., Lee, Y., Antimicrobial resistance of 114 porcine isolates of Campylobacter coli. Int. J. Food Microbiol. 118 (2007), 223–227.
62. Sorensen, L., Alban, L., Nielsen, B., Dahl, J., The correlation between Salmonella serology and isolation of Salmonella in Danish pigs at slaughter. Vet. Microbiol. 101 (2004), 131–141.
63. Steinacker, U., Salmonella enterica subspezies enterica, sect. 5.222. GERMAP 2008: Antibiotika-Resistenz und -Verbrauch. Bundesamt für Verbraucherschutz und Lebensmittelsicherheit, Paul-Ehrlich-Gesellschaft für Chemotherapie e.V., 2008, Institut für Infektiologie, Freiburg, Germany.
64. Steinbach, G., Hartung, M., Versuch einer Schätzung des Anteils menschlicher Salmonella erkrankungen, die auf vom Schwein stammende Salmonellen zurückzuführen sind. Berl. Münch. Tierärztl. Wochenschr. 112 (1999), 296–300.
65. Tam, C.C., O'Brien, S.J., Adak, G.K., Meakins, S.M., Frost, J.A., Campylobacter coli—an important foodborne pathogen. J. Infect. 47 (2003), 28–32.
66. Thakur, S., Gebreyes, W.A., Campylobacter coli in swine production: antimicrobial resistance mechanisms and molecular epidemiology. J. Clin. Microbiol. 43 (2005), 5705–5714.
67. Van Doorn, L.J., Verschuuren-Van Haperen, A., Van Belkum, A., Endtz, H.P., Vliegenthart, J.S., Vandamme, P., Quint, W.G., Rapid identification of diverse Campylobacter lari strains isolated from mussels and oysters using a reverse hybridization line probe assay. J. Appl. Microbiol. 84 (1998), 545–550.
68. Van Looveren, M., Daube, G., De Zutter, L., Dumont, J.M., Lammens, C., Wijdooghe, M., Vandamme, P., Jouret, M., Cornelis, M., Goossens, H., Antimicrobial susceptibilities of Campylobacter strains isolated from food animals in Belgium. J. Antimicrob. Chemother. 48 (2001), 235–240.
69. Vieira-Pinto, M., Temudo, P., Martins, C., Occurrence of Salmonella in the ileum, ileocolic lymph nodes, tonsils, mandibular lymph nodes and carcasses of pigs slaughtered for consumption. J. Vet. Med. 52 (2005), 476–481.
70. Wegener, H.C., Hald, T., Lo Fo Wong, D., Madsen, M., Korsgaard, H., Bager, F., Gerner-Smidt, P., Molbak, K., Salmonella control programs in Denmark. Emerg. Infect. Dis. 9 (2003), 774–780.