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 journalArticle

    15 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.
    LanguageEnglish
    Pages6-13
    JournalInternational Journal of Food Microbiology
    Volume163
    DOIs
    Publication statusPublished - 2013

    Fingerprint

    Campylobacteraceae
    Swine
    swine
    pork
    Fetus
    Arcobacter
    fetus
    Campylobacter concisus
    Campylobacter Infections
    sampling
    Abattoirs
    Campylobacter
    Erythromycin
    Ciprofloxacin
    Microbial Drug Resistance
    drugs
    campylobacteriosis
    Atmosphere
    Ireland
    pig carcasses

    Keywords

    • Campylobacter
    • Arcobacter
    • carcass
    • caeca
    • pork

    Cite this

    Scanlon, K. A., Cagney, C., Walsh, D., McNamara, E. B., Carroll, A. M., McDowell, D. A., & Duffy, G. (2013). Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples. International Journal of Food Microbiology, 163, 6-13. https://doi.org/10.1016/j.ijfoodmicro.2013.02.004
    Scanlon, K.A. ; Cagney, C. ; Walsh, D. ; McNamara, E. B. ; Carroll, A. M. ; McDowell, D.A. ; Duffy, G. / Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples. In: International Journal of Food Microbiology. 2013 ; Vol. 163. pp. 6-13.
    @article{973bc453f17c44b3a9aeed22b8f5376c,
    title = "Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples",
    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.",
    keywords = "Campylobacter, Arcobacter, carcass, caeca, pork",
    author = "K.A. Scanlon and C. Cagney and D. Walsh and McNamara, {E. B.} and Carroll, {A. M.} and D.A. McDowell and G. Duffy",
    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-Maul{\'e}on, 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., J{\o}rgensen, 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., H{\"a}nel, I., Schliephake, A., K{\"o}nig, 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. 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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",
    year = "2013",
    doi = "10.1016/j.ijfoodmicro.2013.02.004",
    language = "English",
    volume = "163",
    pages = "6--13",
    journal = "International Journal of Food Microbiology",
    issn = "0168-1605",
    publisher = "Elsevier",

    }

    Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples. / Scanlon, K.A.; Cagney, C.; Walsh, D.; McNamara, E. B.; Carroll, A. M.; McDowell, D.A.; Duffy, G.

    In: International Journal of Food Microbiology, Vol. 163, 2013, p. 6-13.

    Research output: Contribution to journalArticle

    TY - JOUR

    T1 - Occurrence and characteristics of fastidious Campylobacteraceae species in porcine samples

    AU - Scanlon, K.A.

    AU - Cagney, C.

    AU - Walsh, D.

    AU - McNamara, E. B.

    AU - Carroll, A. M.

    AU - McDowell, D.A.

    AU - Duffy, G.

    N1 - 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. 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    PY - 2013

    Y1 - 2013

    N2 - 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.

    AB - 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.

    KW - Campylobacter

    KW - Arcobacter

    KW - carcass

    KW - caeca

    KW - pork

    U2 - 10.1016/j.ijfoodmicro.2013.02.004

    DO - 10.1016/j.ijfoodmicro.2013.02.004

    M3 - Article

    VL - 163

    SP - 6

    EP - 13

    JO - International Journal of Food Microbiology

    T2 - International Journal of Food Microbiology

    JF - International Journal of Food Microbiology

    SN - 0168-1605

    ER -