Clostridium (Clostridioides) difficile is a Gram-positive anaerobic rod-shaped bacterium and the main cause of nosocomial diarrhoea in humans. In recent years, the transmission of C. difficile from environmental reservoirs (e.g. food) to humans has become a major focus of research. The aim of this study was to investigate the prevalence and corresponding toxin genes of C. difficile in faecal samples and meat of quails. Thirty samples of packed quail meat in Mashhad, Iran and 500 faecal samples (pooled to n = 5) were collected on quail farms in the Northeastern Khorasan region for further investigation. Of 100 pooled quail faecal samples 10% showed cultural growth of C. difficile. In meat samples two out of 30 specimens (7%) showed cultural growth. In six of ten isolates from faecal samples toxin genes (tcdB and tcdA) were present, while four isolates harboured no toxin genes. However, in meat isolates no toxin genes were present. Mutations in the tcdC gene were not detected, indicating that ‘hypervirulent’ strains such as RT027 and RT078 were not present. The data suggest that quail and quail products might hold a potential for the spread of C. difficile.
Abdel-Glil, M. Y., Thomas, P., Schmoock, G., Abou-El-Azm, K., Wieler, L. H., Neubauer, H. and Seyboldt, C. (2018): Presence of Clostridium difficile in poultry and poultry meat in Egypt. Anaerobe 51, 21–25.
al Saif, N. and Brazier, J. S. (1996): The distribution of Clostridium difficile in the environment of South Wales. J. Med. Microbiol. 45, 133–137.
Antikainen, J., Pasanen, T., Mero, S., Tarkka, E., Kirveskari, J., Kotila, S., Mentula, S., Kononen, E., Virolainen-Julkunen, A. R., Vaara, M. and Tissari, P. (2009): Detection of virulence genes of Clostridium difficile by multiplex PCR. APMIS 117, 607–613.
Azimirad, M., Krutova, M., Nyc, O., Hasani, Z., Afrisham, L., Alebouyeh, M. and Zali, M. R. (2017): Molecular typing of Clostridium difficile isolates cultured from patient stool samples and gastroenterological medical devices in a single Iranian hospital. Anaerobe 47, 125–128.
Baverud, V. (2002): Clostridium difficile infections in animals with special reference to the horse. A review. Vet. Q. 24, 203–219.
Belanger, S. D., Boissinot, M., Clairoux, N., Picard, F. J. and Bergeron, M. G. (2003): Rapid detection of Clostridium difficile in feces by real-time PCR. J. Clin. Microbiol. 41, 730–734.
Borriello, S. P., Honour, P., Turner, T. and Barclay, F. (1983): Household pets as a potential reservoir for Clostridium difficile infection. J. Clin. Pathol. 36, 84–87.
Crobach, M. J., Planche, T., Eckert, C., Barbut, F., Terveer, E. M., Dekkers, O. M., Wilcox, M. H. and Kuijper, E. J. (2016): European Society of Clinical Microbiology and Infectious Diseases: update of the diagnostic guidance document for Clostridium difficile infection. Clin. Microbiol. Infect. 22, Suppl. 4, S63–81.
Curry, S. R., Marsh, J. W., Muto, C. A., O’Leary, M. M., Pasculle, A. W. and Harrison, L. H. (2007): tcdC genotypes associated with severe TcdC truncation in an epidemic clone and other strains of Clostridium difficile. J. Clin. Microbiol. 45, 215–221.
Dupuy, B., Govind, R., Antunes, A. and Matamouros, S. (2008): Clostridium difficile toxin synthesis is negatively regulated by TcdC. J. Med. Microbiol. 57, 685–689.
Gerding, D. N., Johnson, S., Rupnik, M. and Aktories, K. (2014): Clostridium difficile binary toxin CDT: mechanism, epidemiology, and potential clinical importance. Gut Microbes 5, 15–27.
Hussain, I., Borah, P., Sharma, R. K., Rajkhowa, S., Rupnik, M., Saikia, D. P., Hasin, D., Hussain, I., Deka, N. K., Barkalita, L. M., Nishikawa, Y. and Ramamurthy, T. (2016): Molecular characteristics of Clostridium difficile isolates from human and animals in the North Eastern region of India. Mol. Cell. Probes 30, 306–311.
Indra, A., Lassnig, H., Baliko, N., Much, P., Fiedler, A., Huhulescu, S. and Allerberger, F. (2009): Clostridium difficile: a new zoonotic agent? Wien. Klin. Wochenschr. 121, 91–95.
Jalali, M., Khorvash, F., Warriner, K. and Weese, J. S. (2012): Clostridium difficile infection in an Iranian hospital. BMC Res. Notes 5, 159.
Knetsch, C. W., Connor, T. R., Mutreja, A., van Dorp, S. M., Sanders, I. M., Browne, H. P., Harris, D., Lipman, L., Keessen, E. C., Corver, J., Kuijper, E. J. and Lawley, T. D. (2014):. Whole genome sequencing reveals potential spread of Clostridium difficile between humans and farm animals in the Netherlands, 2002 to 2011. Euro Surveill. 19, 20954.
Kouhsari, E., Douraghi, M., Fakhre Yaseri, H., Talebi, M., Ahmadi, A., Sholeh, M. and Amirmozafari, N. (2019): Molecular typing of Clostridioides difficile isolates from clinical and non-clinical samples in Iran. APMIS 127, 222–227.
Lawson, P. A., Citron, D. M., Tyrrell, K. L. and Finegold, S. M. (2016): Reclassification of Clostridium difficile as Clostridioides difficile (Hall and O’Toole 1935) Prevot 1938. Anaerobe 40, 95–99.
Lefebvre, S. L., Arroyo, L. G. and Weese, J. S. (2006): Epidemic Clostridium difficile strain in hospital visitation dog. Emerg. Infect. Dis. 12, 1036–1037.
Levett, P. N. (1986): Clostridium difficile in habitats other than the human gastro-intestinal tract. J. Infect. 12, 253–263.
Nasar, A., Rahman, A., Hoque, N., Kumar Talukder, A. and Das, Z. C. (2016): A survey of Japanese quail (Coturnix coturnix japonica) farming in selected areas of Bangladesh. Vet. World 9, 940–947.
Persson, S., Jensen, J. N. and Olsen, K. E. (2011): Multiplex PCR method for detection of Clostridium difficile tcdA, tcdB, cdtA, and cdtB and internal in-frame deletion of tcdC. J. Clin. Microbiol. 49, 4299–4300.
Persson, S., Torpdahl, M. and Olsen, K. E. (2008): New multiplex PCR method for the detection of Clostridium difficile toxin A (tcdA) and toxin B (tcdB) and the binary toxin (cdtA/cdtB) genes applied to a Danish strain collection. Clin. Microbiol. Infect. 14, 1057–1064.
Rupnik, M., Wilcox, M. H. and Gerding, D. N. (2009): Clostridium difficile infection: new developments in epidemiology and pathogenesis. Nat. Rev. Microbiol. 7, 526–536.
Saka, J. O., Oyegbami, A., Okere, I. A., Omole, A. J. and Fayenuwo, J. O. (2018): Production systems of Japanese quail (Coturnix coturnix japonica) in the urban communities of southwestern Nigeria. Trop. Anim. Health Prod. 50, 1295–1303.
Samie, A., Obi, C. L., Franasiak, J., Archbald-Pannone, L., Bessong, P. O., Alcantara-Warren, C. and Guerrant, R. L. (2008): PCR detection of Clostridium difficile triose phosphate isomerase (tpi), toxin A (tcdA), toxin B (tcdB), binary toxin (cdtA, cdtB), and tcdC genes in Vhembe District, South Africa. Am. J. Trop. Med. Hyg. 78, 577–585.
Shoaei, P., Shojaei, H., Khorvash, F., Hosseini, S. M., Ataei, B., Tavakoli, H., Jalali, M. and Weese, J. S. (2019): Molecular epidemiology of Clostridium difficile infection in Iranian hospitals. Antimicrob. Resist. Infect. Control 8, 12.
Songer, J. G. (2004): The emergence of Clostridium difficile as a pathogen of food animals. Anim. Health Res. Rev. 5, 321–326.
Songer, J. G. and Anderson, M. A. (2006): Clostridium difficile: an important pathogen of food animals. Anaerobe 12, 1–4.
Stare, B. G., Delmee, M. and Rupnik, M. (2007): Variant forms of the binary toxin CDT locus and tcdC gene in Clostridium difficile strains. J. Med. Microbiol. 56, 329–335.
Varshney, J. B., Very, K. J., Williams, J. L., Hegarty, J. P., Stewart, D. B., Lumadue, J., Venkitanarayanan, K. and Jayarao, B. M. (2014): Characterization of Clostridium difficile isolates from human fecal samples and retail meat from Pennsylvania. Foodborne Pathog. Dis. 11, 822–829.
Weese, J. S., Reid-Smith, R. J., Avery, B. P. and Rousseau, J. (2010): Detection and characterization of Clostridium difficile in retail chicken. Lett. Appl. Microbiol. 50, 362–365.
Wolff, D., Bruning, T. and Gerritzen, A. (2009): Rapid detection of the Clostridium difficile ribotype 027 tcdC gene frame shift mutation at position 117 by real-time PCR and melt curve analysis. Eur. J. Clin. Microbiol. Infect. Dis. 28, 959–962.