Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples

K.A. Scanlon, C. Cagney, D. Walsh, E. B. McNamara, A. M. Carroll, D.A. McDowell, G. Duffy

    Research output: Contribution to journalArticlepeer-review

    22 Citations (Scopus)

    Abstract

    study investigated the prevalence and characteristics of Campylobacteraceae including a range of fastidious species in porcine samples. Over a thirteen month period caecal contents (n=402) and pork carcass swabs (n=401), were collected from three pork abattoirs and pork products (n=399) were purchased at point of sale in the Republic of Ireland.Campylobacteraceae isolates were recovered by enrichment, membrane filtration and incubation in antibiotic free media under a modified atmosphere (3 % O2, 5 % H2, 10 % CO2 and 82 % N2). Campylobacteraceae isolates were identified as genus Campylobacter or Arcobacter and then selected species were identified by Polymerase Chain Reaction (PCR).Campylobacteraceae were isolated from 103 (26 %) caecal samples, 42 (10 %) carcass swabs,and 59 (15 %) pork products. C. coli was the most commonly isolated species found in (37 %) all sample types but many fastidious species were also isolated including C. concisus (10 %), A. utzleri (8 %), C. helveticus (8 %), C. mucosalis (6 %), A. cryaerophilus (3 %), C. fetus subsp. fetus (1 %), C. jejuni subsp. jejuni, (1 %), C. lari (0.5 %), C. curvus (0.5 %) and A. skirrowii (0.5 %). Among all isolates, 83 % contained cadF and 98 % flaA. In this study 35 % of porcine C. coli were resistant to ciprofloxacin but none of the fastidious species demonstrated any resistance to this drug. The level of resistance to erythromycin was very high (up to 100 %) in C. concisus and C. helveticus and this is a real concern as this is the current empiric drug of choice for treatment of severe gastroenteritic Campylobacter infections. The study shows that there is a much wider range of fastidious Campylobacteraceae present in porcine samples than previously assumed with C. concisus the second most common species isolated. The majority of fastidious ampylobacteraceaeisolates obtained contained virulence genes and antibiotic resistance indicating potential publichealth significance.
    Original languageEnglish
    Pages (from-to)6-13
    JournalInternational Journal of Food Microbiology
    Volume163
    DOIs
    Publication statusPublished - 2013

    Bibliographical note

    Reference text: Aabenhus, R., Permin, H., On, S.L., Andersen, L.P., 2002. Prevalence of Campylobacter concisus in diarrhoea of immunocompromised patients. Scandanvian Journal of Infectious Diseases 34, 248–252.
    Agerholm, J.S., Aalbaek, B., Fog-Larsen, A., Boye, M., Holm, E., Jensen, T.K., Lindhardt, T., Larsen, L.E., Buxton, D., 2006. Veterinary and medical aspects of abortion in Danish sheep. Acta Pathologica, Microbiologica, et Immunologica Scandinavica 114 (2), 146–152.
    Bastyns, K., Chapelle, S., Vandamme, P., Goossens, H., De Wachter, R., 1995a. Specific detection of Campylobacter concisus by PCR amplification of 23SrDNA areas. Molecular and Cellular Probes 9, 247–250.
    Bastyns, K., Cartuyvels, D., Chapelle, S., Vandamme, P., Goossens, H., De Wachter, R., 1995b. A variable 23S rDNA region is a useful discriminating target for genus specific and species-specific PCR amplification in Arcobacter species. Systematic and Applied Microbiology 18, 353–356.
    Decousser, J.W., Prouzet-Mauléon, V., Bartizel, C., Gin, T., Colin, J.P., Fadel, N., Holler, C., Pollet, J.,Megraud, F., 2007. Fatal relapse of a purulent pleurisy caused by Campylobacter fetus subsp. fetus. Journal of Clinical Microbiology 45 (7), 2334–2336.
    Ekkapobyotin, C., Padungtod, P., Chuanchuen, R., 2008. Antimicrobial resistance of campylobacter coli isolates from swine. International Journal of Food Microbiology 128 (2), 325–328.
    Engberg, J., On, S.L.W., Harrington, C.S., Gerner-Smidt, P., 2000. Prevalence of Campylobacter,
    Arcobacter, Helicobacter and Sutterella spp. in human fecal samples as estimated by a
    re-evaluation of isolation methods for Campylobacters. Journal of Clinical Microbiology 38 (1), 286–291.
    Fouts, D.E., Mongodin, E.F., Mandrell, R.E., Miller, W.G., Rasko, D.A., Ravel, J., Brinkac, L.M., DeBoy, R.T., Parker, C.T., Daugherty, S.C., Dodson, R.J., Durkin, A.S., Madupu, R., Sullivan, S.A., Shetty, J.U., Ayodeji, M.A., Shvartsbeyn, A., Schatz, M.C., Badger, J.H., Fraser, C.M., Nelson, K.E., 2005. Major structural differences and novel potential virulence mechanisms from the genomes of multiple Campylobacter species. PLoS Biology 3 (1), e15 (72-85).
    Gebhart, C.J., Edmonds, P., Ward, G.E., Kurtz, H.J., Brenner, D.J., 1985. “Campylobacter hyointestinalis” sp. nov.: a new species of Campylobacter found in the intestines of pigs and other animals. Journal of Clinical Microbiology 21 (5), 715–720.
    George, H.A., Hoffman, P.S., Krieg, N.R., Smibert, R.M., 1978. Development of an improved
    culture medium for Campylobacter fetus. Journal of Clinical Microbiology 8, 36–41.
    Griggs, D.J., Johnson, M.M., Frost, J.A., Humphrey, T., Jørgensen, F., Piddock, L.J., 2005.
    Incidence and mechanism of ciprofloxacin resistance in Campylobacter spp. isolated from commercial poultry flocks in the United Kingdom before, during, and after fluoroquinolone treatment. Antimicrobial Agents and Chemotherapy 49 (2), 699–707.
    Guerry, P., Logan, S.M., Thornton, S., Trust, T.J., 1990. Genomic organization and expression
    of Campylobacter flagellin genes. Journal of Bacteriology 172 (4), 1853–1860.
    Halebian, S., Harris, B., Finegold, S.M., Rolfe, R.D., 1981. Rapid method that aids in distinguishing Gram-positive from Gram-negative anaerobic bacteria. Journal of Clinical Microbiology 13, 444–448.
    Hirayama, J., Sekizuka, T., Tazumi, A., Taneike, I., Moore, J.E., Millar, B.C., Matsyda, M., 2009. Structural analysis of the full-length gene encoding a fibronectin-binding like protein (CadF) and its adjacent genetic loci within Campylobacter lari. Biomedical Central Microbiology 9 (192).
    Houf, K., Tutenel, A., De Zutter, L., Van Hoof, J., Vandamme, P., 2000. Development of a multiplex PCR assay for the simultaneous detection of Arcobacter butzleri, Arcobacter cryaerophilus and Arcobacter skirrowii. FEMS Microbiology Letters 193, 89–94.
    Kabeya, H., Maruyama, S., Morita, Y., Ohsuga, T., Ozawa, S., Kobayashi, Y., Abe, M., Katsube,
    Y.,Mikami, T., 2004. Prevalence of Arcobacter species in retail meats and antimicrobial susceptibility of the isolates in Japan. International Journal of Food Microbiology 90, 303–308.
    Klena, J.D., Parker, C.T., Knibb, K., Ibbit, I.C., Devane, P.M.L., Horn, S.T., Miller, W.G., Konkel, M.E., 2004. Differentiation of Campylobacter coli, Campylobacter jejuni, Campylobacter lari and Campylobacter upsaliensis by a multiplex PCR developed from nucleotide sequence of the lipid A gene lpxA. Journal of Clinical Microbiology 42 (12), 5549–5557.
    Konkel, M.E., Gray, S.A., Kim, B.J., Garvis, S.G., Yoon, J., 1999. Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence
    gene and its product. Journal of Clinical Microbiology 37 (3), 510–517.
    Kramer, J.M., Frost, J.A., Bolton, F.J., Wareing, D.R.A., 2000. Campylobacter contamination
    of raw meat and poultry at retail sale: identification of multiple types and comparison with isolates from human infection. Journal of Food Protection 63 (12), 1654–1659.
    Krause-Gruszczynska, M., van Alphen, L.B., Oyarzabal, O.A., Alter, T., Hänel, I., Schliephake, A., König, W., van Putten, J.P., Konkel, M.E., Backert, S., 2007. Expression patterns and role of the CadF protein in Campylobacter jejuni and Campylobacter coli. FEMS Microbiology Letters 274 (1), 9–16.
    Lastovica, A.J., 2006. Emerging Campylobacter spp.: the tip of the iceberg. Clinical Microbiology
    Newsletter 28 (7), 49–55.
    Lastovica, A.J., Le Roux, E., 2000. Efficient isolation of Campylobacteria from stools. Journal
    of Clinical Microbiology 38 (7), 2798–2799.
    Lawson, G.H.K., Rowland, A.C., 1974. Intestinal adenomatosis in the pig: a bacteriological
    study. Research in Veterinary Science 17, 331–336.
    Le Roux, E., Lastovica, A.J., 1998. The Cape Town protocol: how to isolate the most
    Campylobacters for your dollar, pound, Franc, yen, etc. In: Lastovica, A.J., Newell,
    D., Lastovica, E.E. (Eds.), Proceedings of the 9th International Workshop on Campylobacter,
    Helicobacter and related organisms. Institute of Child Health, Cape Town, South Africa, pp. 31–33.
    Linton, D., Owen, R.J., Stanley, J., 1996. Rapid identification by PCR genus Campylobacter
    and of five Campylobacter species enteropathogenic for man and animals. Research in Microbiology 147, 707–718.
    Little, C.L., Richardson, J.F., Owen, R.J., de Pinna, E., Threlfall, E.J., 2008. Campylobacter
    and Salmonella in rawredmeats in the United Kingdom: prevalence, characterisation and antimicrobial resistance pattern, 2003–2005. Food Microbiology 25, 538–543.
    Luangtongkum, T., Jeon, B., Han, J., Plummer, P., Logue, C.M., Zhang, Q., 2009. Antibiotic
    resistance in Campylobacter: emergence, transmission and persistence. Future Microbiology
    4 (2), 189–200.
    Lynch, Ó.A., Cagney, C., McDowell, D.A., Duffy, G., 2010. A method for the growth of 17
    species of Campylobacter and their recovery from inoculated beef, using common cultural parameters. Journal of Microbiological Methods 83 (1), 1–7.
    Lynch, Ó.A., Cagney, C., McDowell, D.A., Duffy, G., 2011. Occurrence of fastidious Campylobacter spp. in fresh meat and poultry using an adapted cultural protocol. International Journal of Food Microbiology 150, 171–177.
    Malakauskas, M., Jorgensen, K., Nielsen, E.M., Ojeniyi, B., Olsen, J.E., 2006. Isolation of
    Campylobacter spp. from a pig slaughterhouse and analysis of cross contamination. International Journal of Food Microbiology 108, 295–300.
    Miller, W.G., Parker, C.T., Rubenfield, M., Mendz, G.L., Wösten, M.M., Ussery, D.W., Stolz, J.F., Binnewies, T.T., Hallin, P.F., Wang, G., Malek, J.A., Rogosin, A., Stanker, L.H., Mandrell, R.E., 2007. The complete genome sequence and analysis of the epsilon proteobacterium Arcobacter butzleri. PLoS One 26;2 (12), e1358.
    Monteville, M.R., Yoon, J.E., Konkel, M.E., 2003. Maximal adherence and invasion of INT 407 cells by Campylobacter jejuni requires the CadF outer-membrane protein and microfilament reorganization. Microbiology (Reading, England) 149 (1), 153–165.
    Moolhuijzen, P.M., Lew-Tabor, A.E., Wlodek, B.M., Agüero, F.G., Comerci, D.J., Ugalde, R.A., Sanchez, D.O., Appels, R., Bellgard, M., 2009. Genomic analysis of Campylobacter fetus subspecies: identification of candidate virulence determinants and diagnostic assay targets. Biomed Central Microbiology 9 (86).
    Murphy, C., Carroll, C., Jordan, K.N., 2006. Environmental survival mechanisms of the foodborne pathogen Campylobacter jejuni. Journal of Applied Microbiology 100 (4), 623–632.
    Nachamkin, I., Bohachick, K., Patton, C.M., 1993. Flagellin gene typing of Campylobacter jejuni by restriction fragment length polymorphism analysis. Journal of Clinical Microbiology 31 (6), 1531–1536.
    Nuijten, P.J., van Asten, F.J., Gaastra, W., van der Zeust, B.A., 1990. Structural and functional
    analysis of two Campylobacter jejuni flagellin genes. The Journal of Biological Chemistry 265, 17798–17804.
    On, S.L.W., Bloch, B., Holmes, B., Hoste, B., Vandamme, P., 1995. Campylobacter hyointestinalis
    subsp. lawsonii subsp. nov., isolated fromporcine stomach and an emended description
    of Campylobacter hyointestinalis. International Journal of Systematic Bacteriology 45 (4),767–774.
    On, S.L.W., Jensen, T.K., Billie-Hansen, V., Jorsal, S.E., Vandamme, P., 2002. Prevalence and diversity of Arcobacter spp., isolated from the internal organs of spontaneous porcine abortions in Denmark. Veterinary Microbiology 85, 159–167.
    Pearce, R.A., Wallace, F.M., Call, J.E., Dudley, R.L., Oser, A., Yoder, L., Sheridan, J.J., Lchansky, J.B., 2003. Prevalence of Campylobacter within a swine slaughter and processing facility. Journal of Food Protection 66 (9), 1550–1556.
    Pezzotti, G., Serafin, A., Luzzi, I., Mioni, R.,Milan,M., 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.
    Ripabelli, G., Tamburro, M., Minelli, F., Leone, A., Sammarco, M.L., 2009. Prevalence of virulence-associated genes and cytolethal distending toxin production in Campylobacter spp. isolated in Italy. Comparative Immunology, Microbiology and Infectious Diseases 33 (4), 355–364.
    Sasaki, Y., Fujisawa, T., Ogikubo, K., Ohzono, T., Isihihara, K., Takahashi, T., 2003. Characterisation of Campylobacter lanienae from pig faeces. Journal of Veterinary Medicine and Science 65 (1), 129–131.
    Schumacher, W., Kroneck, P.M.H., Pfennig, N., 1992. Comparative systematic study of ‘Spirillum’ 5175, Campylobacter and Wolinella species. Archives of Microbiology 158, 287–293.
    Schuppers, M.E., Stephan, R., Ledergerber, U., Danuser, J., Bissig-Choisat, B., Stärk, K.D.,
    Regula, G., 2005. Clinical herd health, farm management and antimicrobial resistance in Campylobacter coli on finishing pig farms in Switzerland. Preventive Veterinary Medicine 69 (3–4), 189–202.
    Scott, N.E.,Marzook, N.B., Deutscher, A., Falconer, L., Crossett, B., Djordjevic, S.P., Cordwell,
    S.J., 2010. Mass spectrometric characterization of the Campylobacter jejuni adherence factor CadF reveals post-translational processing that removes immunogenicity while retaining fibronectin binding. Proteomics 10 (2), 277–288.
    Sebald, M., Véron, M., 1963. Teneur en bases de l'AND et classification des vibrions. Annales de l'Institut Pasteur 105, 897–910.
    Skirrow, M.B., 1994. Diseases due to Campylobacter, Helicobacter and related bacteria. Journal of Comparative Pathology 111, 113–149.
    Suarez, D.L., Wesley, I.V., Larson, D.J., 1997. Detection of Arcobacter species in gastric samples from swine. Veterinary Microbiology 57, 325–336.
    Taylor, D.E., Chau, A.S., 1997. Cloning and nucleotide sequence of the gyrA gene from Campylobacter fetus subsp. fetus ATCC 27374 and characterization of ciprofloxacin resistant
    laboratory and clinical isolates. Antimicrobial Agents and Chemotherapy 41 (3), 665–671.
    Van Driessche, E., Houf, K., 2007. Characterization of the Arcobacter contamination on Belgian pork carcasses and raw retail pork. International Journal of Food Microbiology 118, 20–26.
    Vandamme, P., Falsen, E., Rossau, R., Hoste, B., Segers, P., Tytgat, R., De Ley, J., 1991. Revision of Campylobacter, Helicobacter and Wolinella taxonomy: emendation of generic
    descriptions and proposal of Arcobacter gen. nov. International Journal of Systematic Biology 41 (1), 88–103.
    Vandenberg, O., Dediste, A., Houf, K., Ibekwem, S., Souayah, H., Cadranel, S., Douat, N., Zissis, G., 2004. Arcobacter species in humans. Emerging Infectious Diseases 10, 1863–1867.
    Vandenberg, O., Houf, K., Douat, N., Vlaes, L., Retore, P., Butzler, J.P., Dediste, A., 2006.
    Antimicrobial susceptibility of clinical isolates of non-jejuni/coli Campylobacter's and Arcobacters fromBelgium. The Journal of Antimicrobial Chemotherapy 57 (5), 908–913.
    Varela, N.P., Friendship, R., Dewey, C., 2007. Prevalence of resistance to 11 antimicrobials
    among Campylobacter coli isolated from pigs on 80 grower-finisher farms in Ontario. Canadian Journal of Veterinary Research 71, 189–194.
    Wassenaar, T.M., Bleumink-Pluym, N.M.C., van der Zeijst, B.A.M., 1991. Inactivation of Campylobacter jejuni flagellin genes by homologous recombination demonstrates that flaA but not flaB is required for invasion. The EMBO Journal 10 (8), 2055–2061.
    Wetsch, N.M., Somani, K., Tryell, G.J., Gebhart, C., Bailey, R.J., Taylor, D.E., 2006. Campylobacter
    curvus-associated hepatic abscesses: a case report. Journal of Clinical Microbiology 44 (5), 1901–1911.
    Whyte, P., McGill, K., Cowley, D., Madden, R.H., Moran, L., Scates, P., Carroll, C., O'Leary, A., Fanning, S., Collins, J.D., McNamara, E., Moore, J.E., Cormican, M., 2004. Occurrence of Campylobacter in retail foods in Ireland. International Journal of Food Microbiology 95, 111–118.K

    Keywords

    • Campylobacter
    • Arcobacter
    • carcass
    • caeca
    • pork

    Fingerprint

    Dive into the research topics of 'Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples'. Together they form a unique fingerprint.

    Cite this