Open Access
Research (Published online: 19-12-2018)
9. Virulence typing and antibiotic susceptibility profiling of thermophilic Campylobacters isolated from poultry, animal, and human species
Neelam Rawat, Maansi, Deepak Kumar and A. K. Upadhyay
Veterinary World, 11(12): 1698-1705

Neelam Rawat: Department of Veterinary Public Health and Epidemiology, College of Veterinary and Animal Sciences, Govind Ballabh Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India.
Maansi: Department of Veterinary Public Health and Epidemiology, College of Veterinary and Animal Sciences, Govind Ballabh Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India.
Deepak Kumar: Department of Veterinary Public Health and Epidemiology, College of Veterinary and Animal Sciences, Govind Ballabh Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India.
A. K. Upadhyay: Department of Veterinary Public Health and Epidemiology, College of Veterinary and Animal Sciences, Govind Ballabh Pant University of Agriculture and Technology, Pantnagar, Uttarakhand, India.

doi: 10.14202/vetworld.2018.1698-1705

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Article history: Received: 09-06-2018, Accepted: 11-10-2018, Published online: 19-12-2018

Corresponding author: Maansi

E-mail: maansi2000@rediffmail.com

Citation: Rawat N, Maansi, Kumar D, Upadhyay AK (2018) Virulence typing and antibiotic susceptibility profiling of thermophilic Campylobacters isolated from poultry, animal, and human species, Veterinary World, 11(12): 1698-1705.
Abstract

Background and Aim: Campylobacteriosis finds its place among the four important global foodborne illnesses. The disease, though self-limiting, needs antibacterial therapy in extraintestinal complications. Therefore, the present study was designed to estimate the prevalence of thermophilic Campylobacters in poultry, animals, and humans of the Kumaon region of Uttarakhand.

Materials and Methods: A total of 609 samples comprising of poultry ceca (n=116), poultry droppings (n=203), and feces of pigs (n=71), cattle (n=61), sheep (n=19), goat (n=17), human beings (n=88), and laboratory animals (n=34) (rats, rabbits, and guinea pigs) were collected. The thermophilic Campylobacters, Campylobacter jejuni and Campylobacter coli were confirmed using multiplex polymerase chain reaction. The isolates were also screened for the presence of virulence genes, and their antibiotic susceptibility testing was done against eight antibiotics.

Results: An overall prevalence of 6.24% was revealed with highest from poultry ceca (15.52%), followed by poultry droppings (5.91%), cattle feces (4.92%), human stools (3.40%), and pig feces (2.82%). The virulence genes, namely cadF, flaA, virB11, and pldA, were present in 38 (100%), 37 (97.37%), 7 (18.42%), and 14 (36.84%) isolates, respectively. All the isolates were resistant to nalidixic acid, while all were sensitive to erythromycin and co-trimoxazole.

Conclusion: It was concluded that the animals and humans in the region harbored the thermophilic Campylobacters which may contribute to the human illness. Resistance shown among the isolates may complicate the antimicrobial therapy.

Keywords: antibiotic susceptibility, thermophilic Campylobacters, virulence.

References

1. Zhao, S., Young, S.R., Tong, E., Abbott, J.W., Womack, N., Friedman, S.L. and McDermott, P.F. (2010) Antimicrobial resistance of Campylobacter isolates from retail meat in the United States: 2002-2007. Appl. Environ. Microbiol., 76(24): 7949-7956. [Crossref] [PubMed] [PMC]

2. Khan, J.A., Rathore, R.S., Abulreesh, H.H., Qais, F.A. and Ahmad, I. (2018) Prevalence and antibiotic resistance profiles of Campylobacter jejuni isolated from poultry meat and related samples at retail shops in Northern India. Foodborne Pathog. Dis., 15(4): 218-225. [Crossref] [PubMed]

3. Stella, S., Soncini, G., Ziino, G., Panebianco, A., Pedonese, F., Nuvoloni, R., Di Gianntale, E., Colavita, G., Alberghini, L. and Giaccone, V. (2017) Prevalence and quantification of thermophilic Campylobacter spp. In Italian retail poultry meat: Analysis of influencing factors. Food Microbiol., 62(1): 232-238. [Crossref] [PubMed]

4. Duque, B., Daviaud, S., Guillou, S., Haddad, N. and Membre, J.M. (2017) Quantification of Campylobacter jejuni contamination on chicken carcasses in France. Food Res. Int., 106: 1077-1085. [Crossref] [PubMed]

5. Calva, J.J., Ruiz-Palacioz, G.M., Lopez-Vidal, A.B., Ramos, A. and Bojalil, R. (1988) Cohort study of intestinal infection with Campylobacter in Mexican children. Lancet, 1(8584): 503-506. [Crossref]

6. Salim, S.M., Mandal, J. and Parija, S.C. (2014) Isolation of Campylobacter from human stool samples. Indian J. Med. Microbiol., 32(1): 35-38. [Crossref] [PubMed]

7. Gorkiewicz, G., Feierl, G., Schober, C., Dieber, F., Kofer, J., Zechner, R. and Zechner, E.L. (2003) Species-specific identification of Campylobacters by partial 16SrRNA gene sequencing. J. Clin. Microbiol., 41(6): 2537-2546. [Crossref] [PMC]

8. Wieczorek, K. and Osek, J. (2013) Antimicrobial resistance mechanisms among Campylobacter. Biomed. Res. Int., 2013(6726): 340605. [PubMed] [PMC]

9. Corry, J.E.L., Atabay, H.I., Forsythe, S.J. and Mansfield, L.P. (2003) Culture media for the isolation of Campylobacters, Helicobacter and Arcobacters. In: Corry, J.E.L., Curtis, G.D.W. and Baird, R.M., editors. Handbook of Culture Media for Food Microbiology. 2nd ed. Elsevier, Amsterdam, The Netherlands. p271-315. [Crossref]

10. OIE Terrestrial Manual. (2008) C. jejuni and C. coli. OIE Terrestrial Manual, Paris. p1185-1191.

11. 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. J. Clin. Microbiol., 35(10): 2568-2572. [PubMed] [PMC]

12. Nayak, R., Stewart, T.M. and Nawaz, M.S. (2005) PCR identification of Campylobacter coli and Campylobacter jejuni by partial sequencing of virulence genes. Mol. Cell. Probes., 19(3): 187-193. [Crossref] [PubMed]

13. Oyofo, B.A., Thornton, S.A., Burr, D.H., Trust, T.J., Pavlovskis, O.R. and Guerry, P. (1992) Specific detection of C. jejuni and C. coli by using the polymerase chain reaction. J. Clin. Microbiol., 30(10): 2613-2619. [PubMed] [PMC]

14. Datta, S., Niwa, H. and Itoh, K. (2003) Prevalence of 11 pathogenic genes of C. jejuni by PCR in strains isolated from humans, poultry meat and broiler and bovine faeces. J. Med. Microbiol., 52(4): 345-348. [Crossref] [PubMed]

15. Biswas, D., Hannon, S.J., Townsend, H.G., Potter, A. and Allan, B.J. (2011) Genes coding for virulence determinants of C. jejuni in human clinical and cattle isolates from Alberta, Canada, and their potential role in colonization of poultry. Int. Microbiol., 14(1): 25-32. [PubMed]

16. Taremi, M., Mehdi, M., Dallal, S., Gachkar, L., MoezArdalan, S. and Zolfagharian, K. (2006) Prevalence and antimicrobial resistance of Campylobacter isolated from retail raw chicken and beef meat, Tehran, Iran. Int. J. Food Microbiol., 108(3): 401-403. [Crossref]

17. Rajagunalan, S. (2010) Isolation, PCR Based Identification and Fla Typing of Thermophilic Campylobacters. M.V.Sc. Thesis Submitted to G.B.P.U.A and T, Pantnagar.17. Rajagunalan, S. (2010) Isolation, PCR Based Identification and Fla Typing of Thermophilic Campylobacters. M.V.Sc. Thesis Submitted to G.B.P.U.A and T, Pantnagar.

18. Pandey, R. (2015) Biochemical and Molecular Characterization of Thermophilic Campylobacters Isolated from Man and Farm Animals. M.V.Sc. Thesis submitted to G.B.P.U.A and T, Pantnagar.

19. Pant, K. (2011) Isolation, Identification and Molecular Characterization of Campylobacter jejuni and C. coli. M.V.Sc. Thesis Submitted to G.B.P.U.A and T, Pantnagar.

20. Kumar, P. (2013) Isolation and Molecular Characterization of C. jejuni and C. coli from Human and Poultry Caeca as Well as Meat. M.V.Sc. Thesis Submitted to G.B.P.U.A and T, Pantnagar.

21. Monika, J. (2014) Isolation, Epidemiology, Molecular Characterization and Antibiogram of Campylobacter from meat. M.V.Sc. Thesis Submitted to G.B.P.U.A and T, Pantnagar.

22. Rajendran, P., Babji, S., George, A.T., Rajan, D.P., Kang, G. and Ajjampur, S.S. (2012) Detection and species identification of Campylobacter in stool samples of children and animals from Vellore, South India. Indian J. Med. Microbiol., 30(1): 85-88. [Crossref] [PubMed] [PMC]

23. Deckert, A., Valdivieso-Garcia, A., Reid-Smith, R., Tamblyn, S., Seliske, P., Irwin, R., Dewey, C., Boerlin, P. and McEwen, S.A. (2010) Prevalence and antimicrobial resistance in Campylobacter spp. Isolated from retail chicken in two health units in Ontario. J. Food Prot., 73(7): 1317-1312. [Crossref] [PubMed]

24. Desmonts, M.H., Dufour-Gesbert, F., Avrain, L. and Kempf, I. (2004) Antimicrobial resistance in Campylobacter strains isolated from French broilers before and after antimicrobial growth promoter bans. J. Antimicrob. Chemother., 54(6): 1025-1030. [Crossref] [PubMed]

25. Humphrey, T., O'Brien, S. and Madsen, M. (2007) Campylobacters as zoonotic pathogens: A food production perspective. Int. J. Food Microbiol., 117(3): 237-257. [Crossref] [PubMed]

26. Salihu, M.D., Junaidu, A.U., Oboegbulem, S.I., Egwu, G.O., Tambuwal, F.M. and Yakubu, Y. (2009) Prevalence of Campylobacter species in apparently healthy goats in Sokoto State (Northwestern) Nigeria. Afr. J. Microbiol. Res., 3(9): 572-574.

27. Zweifel, C., Zychowska, M.A. and Stephan, R. (2004) Prevalence and characteristics of Shiga toxin-producing Escherichia coli, Salmonella Spp., and Campylobacter spp. Isolated from slaughtered sheep in Switzerland. Int. J. Food Microbiol., 92(1): 45-53. [Crossref] [PubMed]

28. Cortes, C., de la Fuente, R., Contreras, A., Sanchez, A., Corrales, J.C., Martinez, S. and Orden, J.A. (2006) A survey of Salmonella Spp., and Campylobacter spp. In dairy goat faeces and bulk tank milk in the Murcia region of Spain. Ir. Vet. J., 59(7): 391-393. [Crossref] [PubMed] [PMC]

29. Lazou, T., Dovas, C., Houf, K., Soultos, N. and Iossifidou, E. (2014) Diversity of Campylobacter in retail meat and liver of lambs and goat kids. Foodborne Pathog. Dis., 11(4): 320-328. [Crossref] [PubMed]

30. Mpalang, R.K., Boreux, R., Melin, P., Bitiang, K.A.N., Daube, G. and Mol, P.D. (2014) Prevalence of Campylobacter among goats and retail goat meat in Congo. J. Infect. Dev. Ctries., 8(2): 168-175. [Crossref]

31. Karikari, A.B., Obiri-Danso, K., Frimpong, E.H. and Krogfelt, K.A. (2017) Antibiotic resistance of Campylobacter recovered from faeces and carcasses of healthy livestock. Bio. Med. Res. Int., 2017: 4091856. [Crossref] [PubMed] [PMC]

32. Jensen, A.N., Dalsgaard, A., Baggesen, D.L. and Nielsen, E.M. (2006) The occurrence and characterization of Campylobacter jejuni and C. coli in organic pigs and their outdoor environment. Vet. Microbiol., 116(1-3): 96-105. [Crossref] [PubMed]

33. Nkogwe, C., Raletobana, J., Stewart-Johnson, A., Suepaul, S. and Adesiyun, A. (2011) Frequency of detection of Escherichia coli, Salmonella Spp., and Campylobacter spp. In the faeces of wild rats (Rattus Spp.) in Trinidad and Tobago. Vet. Med. Int., 2011: 1-7. [Crossref] [PubMed] [PMC]

34. Konkel, M.E., Gray, S.A., Kim, B.J., Garvis, S.G. and Yoon, J. (1999) Identification of the enteropathogens Campylobacter jejuni and Campylobacter coli based on the cadF virulence gene and its product. J. Clin. Microbiol., 37(3): 510-517. [PubMed] [PMC]

35. Wieczorek, K., Denis, E., Lynch, O. and Osek, J. (2013) Molecular characterization and antibiotic resistance profiling of Campylobacter isolated from cattle in polish slaughterhouses. Food Microbiol., 34(1): 130-136. [Crossref] [PubMed]

36. Rozynek, E., Dzierzanowska-Fangrat, K., Jozwiak, P., Popowski, J., Korsak, D. and Dzierzanowska, D. (2005) Prevalence of potential virulence markers in polish Campylobacter jejuni and Campylobacter coli isolates obtained from hospitalized children and from chicken carcasses. J. Med. Microbiol., 54(7): 615-619. [Crossref] [PubMed]

37. Wieczorek, K. and Osek, J. (2011) Molecular characterization of Campylobacter spp. Isolated from poultry faeces and carcasses in Poland. Acta Vet. Brno, 80(1): 19-27. [Crossref]

38. Bang, D.D., Nielsen, E.M., Scheutz, F., Pedersen, K., Handberg, K. and Madsen, M. (2003) PCR detection of seven virulence and toxin genes of Campylobacter jejuni and Campylobacter coli isolates from Danish pigs and cattle and cytolethal distending toxin production of the isolates. J. Appl. Microbiol., 94(6): 1003-1014. [Crossref]

39. Talukder, K.A., Aslam, M., Islam, Z., Azmi, I.J., Dutta, D.K., Hossain, S., Nur-E-Kamal, A., Nair, G.B., Cravioto, A., Sack, D.A. and Endtz, H.P. (2008) Prevalence of virulence genes and cytolethal distending toxin production in C. jejuni isolates from diarrheal patients in Bangladesh. J. Clin. Microbiol., 46(4): 1485-1488. [Crossref] [PubMed] [PMC]

40. Koolman, L., Whyte, P., Burgess, C. and Bolton, D. (2015) Distribution of virulence-associated genes in a selection of Campylobacter isolates. Foodborne Pathog. Dis., 12(5): 424-432. [Crossref] [PubMed]

41. Jribi, H., Sellami, H., Hassena, A.B. and Gdoura, R. (2017) Prevalence of putative virulence genes in Campylobacter and Arcobacter species isolated from poultry and poultry by-products in Tunisia. J. Food Prot., 80(10): 1705-1710. [Crossref] [PubMed]

42. Melo, R.T., Nalevaiko, P.C., Mendonca, E.P., Borges, L.W., Fonseca, B.B., Marcelo, E., Beletti, M.E. and Rossi, D.A. (2013) Campylobacter jejuni strains isolated from chicken meat harbour several virulence factors and represent a potential risk to humans. Food Control, 33(1): 227-231. [Crossref]

43. Ruiz, J., Marco, F., Oliveira, I., Vila, J. and Gascon, J. (2007) Trends in antimicrobial resistance in Campylobacter spp. Causing traveler's diarrhea. Acta Pathol. Microbiol. Immunol. Scand., 115(3): 218-224. [Crossref] [PubMed]

44. Jain, D., Sinha, S., Prasad, K.N. and Pandey, C.M. (2005) Campylobacter species and drug resistance in a North Indian rural community. Trans. R. Soc. Trop. Med. Hyg., 99(3): 207-214. [Crossref] [PubMed]

45. Qin, S.S., Wu, C.M. and Wang, Y. (2011) Antimicrobial resistance in C. coli isolated from pigs in two provinces of China. Int. J. Food Microbiol., 146(1): 94-98. [Crossref] [PubMed]

46. Sonnevend, A., Rotimi, V.O., Kolodziejek, J., Usmani, A., Nowotny, N. and Pal, T. (2006) High level of ciprofloxacin resistance and its molecular background among C. jejuni strains isolated in the United Arab Emirates. J. Med. Microbiol., 55(11): 1533-1538. [Crossref] [PubMed]

47. Bester, L.A. and Essack, S.Y. (2008) Prevalence of antibiotic resistance in Campylobacter isolates from commercial poultry suppliers in KwaZulu-Natal, South Africa. J. Antimicrob. Chemother., 62(6): 1298-1300. [Crossref] [PubMed]

48. Szczepanska, B., Andrzejewska, M., Spica, D. and Klawe, J.J. (2017) Prevalence and antimicrobial resistance of Campylobacter jejuni and Campylobacter coli isolated from children and environmental sources in urban and suburban areas. BMC Microbiol., 17(1): 80. [Crossref]