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Prevalence, Molecular Characterization and Antimicrobial Resistance of Thermophilic Campylobacter Isolates from Cattle, Hens, Broilers and Broiler Meat in South-eastern Italy

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Abstract

Eleven cattle farms, 8 layer farms, 7 broiler farms and 30 broiler meat samples were investigated in south-eastern Italy throughout 2003 to evaluate the prevalence, the molecular type and antimicrobial resistance of thermophilic Campylobacters. A total of 398 samples were analysed. One Campylobacter isolate for each positive faecal swab and three isolates per positive broiler meat sample were selected for further analysis. Multiplex PCR was performed for species-level identification and PCR-RFLP of the flagellin A gene for genotyping. Resistance to 14 antimicrobials was studied in 188 Campylobacter isolates. Prevalence of campylobacters was high both on farms (100%) and in food samples (73%). On 4/11 cattle farms and on 10/15 poultry farms more than one species was isolated. The presence of more than one genotype was found on 8/11 cattle farms, on 10/15 poultry farms and in 8/22 Campylobacter-positive food samples. High rates of resistance to quinolone were observed: 9/31 (29%) C. jejuni bovine isolates, 4/22 (18%) C. jejuni poultry isolates, and 14/26 (54%) C. coli poultry isolates. Resistance to sulphamethoxazole-trimethoprim was also observed frequently: 18/26 (69%) of the avian C. coli strains, 25/31 (80%) of the C. jejuni strains isolated from poultry and 15/22 (68%) of those isolated from cattle were resistant. There was a significant difference between the rate of resistance to macrolides of C. coli and C. jejuni isolated in poultry, which amounted to 23% and 3%, respectively. This study provided data on the prevalence and antimicrobial resistance of thermophilic campylobacters in south-eastern Italy and confirmed that flaA-typing is an efficient tool to study the epidemiology of Campylobacter strains in short-term investigations.

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Abbreviations

PCR-RFLP:

polymerase chain reaction–restriction fragment length polymorphism

bp:

base pair(s)

References

  • Aarestrup, F.M. and Wegener, H.K., 1999. The effects of antimicrobial usage in food animals on the development of antimicrobial resistance of importance in humans in Campylobacter and Escherichia coli. Microbes and Infection, 1, 639–644

    Article  PubMed  CAS  Google Scholar 

  • Aarestrup, F.M., Mielsen, E.M., Madsen, M. and Engberg, J., 1997. Antimicrobial susceptibility patterns of thermophilic Campylobacter spp. from humans, pigs, cattle, and broilers in Denmark. Antimicrobial Agents and Chemotherapy, 41, 2244–2250

    PubMed  CAS  Google Scholar 

  • Adler-Mosca, H., Lüthy-Hottenstein, J., Martinetti Lucchini, G., Burnens, A. and Altwegg, M., 1991. Development of resistance to quinolones in five patients with campylobacteriosis treated with norfloxacin or ciprofloxacin. European Journal of Clinical Microbiology and Infectious Diseases, 10, 953–957

    Article  CAS  Google Scholar 

  • Bager, F., (ed.), Danmap 98, 1999. Consumption of Antimicrobial Agents and Occurrence of Antimicrobial Resistance in Bacteria from Food Animals, Food and Humans in Denmark. Danish Zoonosis Centre, Copenhagen, 3

    Google Scholar 

  • CAMPYNET website: www.svs.dk/campynet

  • Charvalos, E., Peteinaki, E., Spyridaki, I., Manetas, S. and Tselentis, Y., 1996. Detection of ciprofloxacin resistance mutations in Campylobacter jejuni gyrA by nonradioisotopic single-strand conformation polymorphism and direct DNA sequencing. Journal of Clinical Laboratory Analysis, 10, 129–133

    Article  PubMed  CAS  Google Scholar 

  • Cogan, T.A., Bloomfield, S.F. and Humphrey, T.J., 1999 The effectiveness of hygiene procedures for prevention of cross-contamination from chicken carcasses in the domestic kitchen. Letters in Applied Microbiology 29, 354–358

    Article  PubMed  CAS  Google Scholar 

  • Endtz, H.P., Mouton, R.P., Van Der Reyden, T., Ruijs, G.J., Biever, M. and Van Klingeren, B., 1990. Fluoroquinolone resistance in Campylobacter spp. isolated from human stools and poultry products. Lancet, 335, 787

    Article  PubMed  CAS  Google Scholar 

  • Endtz, H.P., Ruijs, G.J., Van Klingeren, B., Jansen, W.H. and Van Der Reyden, T., 1991. Quinolone resistance in Campylobacter isolated from man and poultry following the introduction of fluoroquinolones in veterinary medicine. Journal of Antimicrobial Chemotherapy, 42, 199–208

    Article  Google Scholar 

  • Fahey, T., Morgan, D., Gunneburg, C., Adak, G.K., Majid, F. and Kaczmarski, E., 1995. An outbreak of Campylobacter jejuni enteritis associated with failed milk pasteurization. Journal of Infection, 31, 137–143

    Article  PubMed  CAS  Google Scholar 

  • Figura, N., Guglielmetti, P., Zanchi, A., Signori, R., Rossolini, A., Lior, H., Russi, M. and Musmanno, R.A., 1997. Species, biotype and serogroup of Campylobacter spp. Isolate from children with diarrhoea over a ten-year period. New Microbiologica, 20, 303–310

    PubMed  CAS  Google Scholar 

  • Gaunt, P.N. and Piddock, L.J., 1996. Ciprofloxacin resistant Campylobacter spp. in humans: an epidemiological and laboratory study. Journal of Antimicrobial Chemotherapy, 37, 47–57

    Google Scholar 

  • Ge, B., White, D.G., Mcdermott, P.F., Girard, W., Zhao, S., Hubert, S. and Meng, J., 2003. Antimicrobial-resistant Campylobacter species from retail raw meats. Applied and Environmental Microbiology, 69, 3005–3007

    Article  PubMed  CAS  Google Scholar 

  • Gibreel, A., Sjogren, E., Kaijser, B., Wretlind, B. and Skold, O., 1998. Rapid emergence of high-level resistance to quinolones in Campylobacter jejuni associated with mutational changes in gyrA and parC. Antimicrobial Agents and Chemotherapy, 42, 3276–3278

    PubMed  CAS  Google Scholar 

  • Griffiths, P.L. and Park, R.W.A., 1990. Campylobacters associated with human diarroheal disease. Journal of Applied Bacteriology, 69, 281–301

    PubMed  CAS  Google Scholar 

  • Husmann, M., Feddersen, A., Steitz, A., Freytag, C. and Bhakdi, S., 1997. Simultaneous identification of Campylobacters and prediction of quinolone resistance by comparative sequence analysis. Journal of Clinical Microbiology, 35, 2398–2400

    PubMed  CAS  Google Scholar 

  • Jiménez, A., Velazquez, J.B., Rodriguez, J., Tinajas, A. and Villa T, G., 1994. Prevalence of fluoroquinolone resistance in clinical resistance in clinical strains of Campylobacter jejuni isolated in Spain. Journal of Antimicrobial Chemotherapy, 33, 188–190

    Article  PubMed  Google Scholar 

  • Li, C.C., Chiu, C.H., Wu, J.L., Huang, Y.C. and Lin, T.Y., 1998. Antimicrobial susceptibilities of Campylobacter jejuni and coli by using E-test in Taiwan. Scandinavian Journal of Infectious Disease, 30, 39–42

    Article  CAS  Google Scholar 

  • Linton, D., Owen, R.J. and Stanley, J., 1996. Rapid identification by PCR of the genus Campylobacter and five Campylobacter species enteropathogenic for man and animals. Research in Microbiology, 147, 707–718

    Article  PubMed  CAS  Google Scholar 

  • Linton, D., Lawson, A.J., Owen, R.J. and Stanley, J., 1997. PCR detection, identification to species level, and fingerprinting of Campylobacter jejuni and Campylobacter coli direct from diarrheic samples. Journal of Clinical Microbiology, 35, 2568–2572

    PubMed  CAS  Google Scholar 

  • Nackamkin, I., Bohachick, K. and Patton, C.M., 1993. Flagellin gene typing of Campylbacter jejuni by restriction fragment length polymorphism analysis. Journal of Clinical Microbiology, 31, 1531–1536

    Google Scholar 

  • National Committee for Clinical Laboratory Standards. Performance Standards for Antimicrobial Disk Susceptibility Tests, Ninth informational supplement, NCCL document M100-S9, (National Committee for Clinical Laboratory Standards, Wayne, PA), 1999

    Google Scholar 

  • Newell, D.G., Shreeve, J.E., Toszeghy, M., Dominigue, G., Bull, S., Humphrey, T. and Mead, G., 2001. Changes in the carriage of Campylobacter strains by poultry carcasses during processing in abbattoirs. Applied and Environmental Microbiology, 67, 2626–2640

    Article  Google Scholar 

  • Nielsen, E.M. and Nielsen, N.L., 1999. Serotypes and typability of Campylobacter jejuni and Campylobacter coli isolated from poultry products. International Journal of Food Microbiology, 46, 199–205

    Article  PubMed  CAS  Google Scholar 

  • Nielsen, E.M., Engberg, J. and Madsen, M., 1997. Distribution of serotypes of Campylobacter jejuni and C. coli from Danish patients, poultry, cattle and swine. FEMS Immunology and Medical Microbiology, 19, 47–56

    Article  PubMed  CAS  Google Scholar 

  • On, S.L.W., Nielsen, E.M., Engberg, J. and Madsen, M., 1998. Validity of SmaI-defined genotypes of Campylobacter jejuni examined by SalI, KpnI, and BamHI polymorphisms: evidence of identical clones infecting humans, poultry, and cattle. Epidemiology and Infection, 120, 231–237

    Article  PubMed  CAS  Google Scholar 

  • Orr, K.E., Lightfoot, N.F., Sisson, P.R., Harkis, B.A., Tveddle, J.L. and Boyd P., 1995. Direct milk excretion of Campylobacter jejuni in a dairy cow causing cases of human enteritis. Epidemiology and Infection 114, 15–24

    PubMed  CAS  Google Scholar 

  • Owen, R.J. and Leeton, S., 1999. Restriction fragment length polymorphism analysis of the flaA gene of Campylobacter jejuni for subtyping human, animal and poultry isolates. FEMS Microbiology Letters, 176, 345–350

    Article  PubMed  CAS  Google Scholar 

  • Park, S.F., 2002. The physiology of Campylobacter species and its relevance to their role as foodborne pathogens. International Journal of Food Microbiology, 74, 177–188

    Article  PubMed  CAS  Google Scholar 

  • Pearson A.D., Greenwood, M.H., Donaldson, J., Healing, T.D., Jones, D.M. and Shahamat, M., 2000. Continuous source outbreak of campylobacteriosis traced to chicken. Journal of Food Protection, 63, 309–314

    PubMed  CAS  Google Scholar 

  • Petersen, L., Nielsen, E.M. and On, S.L.W., 2001. Serotype and genotype diversity and hatchery transmission of Campylobacter jejuni in commercial poultry flocks. Veterinary Microbiology, 82, 141–154

    Article  PubMed  CAS  Google Scholar 

  • Pezzotti, G., Serafin, A., Luzzi, I., Mioni, R., Milan, M. and Perin, R., 2003. Occurrence and resistance to antibiotics of Campylobacter jejuni and Campylobacter coli in animals and meat in northeastern Italy. International Journal of Food Microbiology, 82, 281–287

    Article  PubMed  CAS  Google Scholar 

  • Ruiz, J., Goni, P., Marco, F., Gallardo, F., Mirelis, B., De Anta, T.J. and Vila, J., 1998. Increased resistance to quinolones in Campylobacter jejuni: a genetic analysis of gyrA gene mutations in quinolone-resistant clinical isolates. Microbiology and Immunology, 42, 223–226

    PubMed  CAS  Google Scholar 

  • Sàenz, Y., Zarazaga, M., Lantero, M., Gastanares, M.J., Baquero, F. and Torres, C., 2000. Antimicrobial resistance in Campylobacter strains isolated from animals, foods, and humans in Spain in 1997–1998. Antimicrobial Agents and Chemotherapy, 44, 267–271

    Article  PubMed  Google Scholar 

  • Shane, S.M., 2000. Campylobacter infection of commercial poultry. Review in Science and Techology, 19, 376–395

    CAS  Google Scholar 

  • Smith, K.E., Besser, J.M., Hedberg, C.W., Leano, F.T., Bender, J.B. and Wicklund, J.H., 1999. Quinolone-resistant Campylobacter jejuni infections in Minnesota, 1992–1998. New England Journal of Medicine, 340, 1525–1532

    Article  PubMed  CAS  Google Scholar 

  • Studhal, A. and Andersson, Y., 2000. Risk factors for indigenous Campylobacter infection: a Swedish case-control study. Epidemiology and Infection, 125, 269–275

    Article  Google Scholar 

  • Svedhem, A., Kaijser, B. and Sjogren, E., 1981. Antimicrobial susceptibility of Campylobacter jejuni isolated from humans with diarrhoea and from healthy chickens. Journal of Antimicrobial Chemotherapy, 7, 301–305

    Article  PubMed  CAS  Google Scholar 

  • Thomas, L.M., Long, K.A., Good, R.T., Panaccio, M. and Widders, P.R., 1997. Genotypic diversity among Campylobacter jejuni isolates in a commercial broiler flock. Applied and Environmental Microbiology, 63, 1874–1877

    PubMed  CAS  Google Scholar 

  • Wang, Y., Huang, W.M. and Taylor, D.E., 1993. Cloning and nucleotide sequence of the Campylobacter jejuni gyrA gene and characterization of quinolone resistance mutations. Antimicrobial Agents and Chemotherapy, 37, 457–463

    PubMed  CAS  Google Scholar 

  • Wassenaar, T.M. and Newell, D.G., 2000. Genotyping of Campylobacter spp. Applied and Environmental Microbiology, 66, 1–9

    Article  PubMed  CAS  Google Scholar 

  • Wassenaar T.M., Geilhausen B. and Newell D.G., 1998. Evidence of genomic instability in Campylobacter jejuni isolated from poultry. Applied and Environmental Microbiology, 64, 1816–1821

    PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. Istituto Zooprofilattico Sperimentale della Puglia e Basilicata, Putignano, Bari

    A. Parisi, S. G. Lanzilotta, N. Addante & C. O. Montagna

  2. Dipartimento di Sanità e Benessere Animale, Università degli Studi di Bari, Valenzano, Bari, Italy

    G. Normanno, G. Di Modugno & A. Dambrosio

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  1. A. Parisi
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  2. S. G. Lanzilotta
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  3. N. Addante
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  4. G. Normanno
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  5. G. Di Modugno
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  6. A. Dambrosio
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  7. C. O. Montagna
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Correspondence to A. Parisi.

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Parisi, A., Lanzilotta, S.G., Addante, N. et al. Prevalence, Molecular Characterization and Antimicrobial Resistance of Thermophilic Campylobacter Isolates from Cattle, Hens, Broilers and Broiler Meat in South-eastern Italy. Vet Res Commun 31, 113–123 (2007). https://doi.org/10.1007/s11259-006-3404-3

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