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Investigating the Presence of Salmonella spp. in the Feces of Red Deer (Cervus elaphus) in Istanbul

Year 2022, Volume: 7 Issue: 2, 110 - 114, 30.06.2022
https://doi.org/10.35229/jaes.1061914

Abstract

Wildlife is an important source of many infectious agents for domestic animals and humans. Increasing interactions between humans, domestic animals, and wildlife may cause the infection of contagious agents between the species. Domestic animals can be easily infected with Salmonella serovars as a result of its asymptomatic presence in the intestinal flora of wild animals and its spreading around. The presence of Salmonella species in the feces of red deer, which is an important member of wildlife in Turkey, was investigated in the present study. A total of 240 fecal samples were collected in sterile dry plastic containers from free-ranging deer at the Deer Breeding Farm in Istanbul Belgrad Forest, at least once a month for a year. The samples collected were examined through conventional culture and molecular methods (PCR). Salmonella spp. was not isolated from the samples examined.

Supporting Institution

Scientific Research Projects Coordination Unit of Istanbul University-Cerrahpasa

Project Number

TDK-2019-33776

Thanks

This study was funded by Scientific Research Projects Coordination Unit of Istanbul University-Cerrahpasa. Project number: TDK-2019-33776. Essential permission for collecting deer feces samples were obtained from the General Directorate of Nature Conservation and National Parks.

References

  • Albufera, U., Bhugaloo-Vial, P., Issack, M. I., & Jaufeerally-Fakim, Y. (2009). Molecular characterization of Salmonella isolates by REP-PCR and RAPD analysis. Infection, genetics and evolution, 9(3), 322-327.
  • Ayanegui-Alcerreca, M. A., Wilson, P. R., Mackintosh, C. G., Collins-Emerson, J. M., Heuer, C., Midwinter, A. C., & Castillo-Alcala, F. (2007). Leptospirosis in farmed deer in New Zealand: a review. New Zealand veterinary journal, 55(3), 102-108.
  • Botti, V., Navillod, F. V., Domenis, L., Orusa, R., Pepe, E., Robetto, S., & Guidetti, C. (2013). Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Vet Ital, 49(2), 195-202.
  • Carrillo-Del Valle, M. D., J. A. De la Garza-García, E. Díaz-Aparicio, A. G. Valdivia-Flores, L. F. Cisneros-Guzmán, C. Rosario, Á. H. Manjarrez-Hernández, A. Navarro, J. Xicohtencatl-Cortes, P. Maravilla, and R. Hernández-Castro. (2016). Characterization of Escherichia coli strains from red deer (Cervus elaphus) faeces in a Mexican protected natural area. Eur. J. Wildl. Res. 62:415–421.
  • Carroll, D., Wang, J., Fanning, S., & McMahon, B. J. (2015). Antimicrobial resistance in wildlife: implications for public health. Zoonoses and public health, 62(7), 534-542.
  • Crawford, R. W., Rosales-Reyes, R., de la Luz Ramírez-Aguilar, M., Chapa-Azuela, O., Alpuche-Aranda, C., & Gunn, J. S. (2010). Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proceedings of the National Academy of Sciences, 107(9), 4353-4358.
  • Çakın, M, Başaran Kahraman, B, Diren Sığırcı, B, Bağcıgil, A. (2020). Distribution of Salmonella serovars and characterization of isolates in cattle feces and environmental samples. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 67 (3), 215-220.
  • Dos Santos, E. J. E., Azevedo, R. P., Lopes, A. T. S., Rocha, J. M., Albuquerque, G. R., Wenceslau, A. A., ... & Maciel, B. M. (2020). Salmonella spp. in Wild Free-Living Birds from Atlantic Forest Fragments in Southern Bahia, Brazil. BioMed research international, 2020.
  • Farias, L.F.P., Oliveira, C.J.B., Medardus, J.J., Molla, B.Z., Wolfe, B.A. and Gebreyes, W.A. (2015), Phenotypic and Genotypic Characterization of Salmonella enterica in Captive Wildlife and Exotic Animal Species in Ohio, USA. Zoonoses Public Health, 62: 438-444.
  • French, E., Rodriguez-Palacios, A., & LeJeune, J. T. (2010). Enteric bacterial pathogens with zoonotic potential isolated from farm-raised deer. Foodborne pathogens and disease, 7(9), 1031-1037.
  • Gorski L, Parker CT, Liang A, Cooley MB, Jay-Russell MT, Gordus AG, Atwill ER, Mandrell RE. (2011) Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl Environ Microbiol. Apr;77(8):2734-48.
  • Henderson T. G., Hemmingsen P. (1983) Faecal survey of deer for Yersinia pseudotuberculosis and Salmonella sp., New Zealand Veterinary Journal, Pages 225-226 | Published online: 23 Feb 2011.
  • Hilbert F, Smulders FJM, Chopra-Dewasthaly R, Paulsen P. Salmonella in the wildlife-human interface. Food Res Int 2012;45:603-8. Integrated Taxonomic Information System – Report (2012) https://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=180694 (Date of access: November 5, 2021).
  • Iovine, R. D. O., Dejuste, C., Miranda, F., Filoni, C., Bueno, M. G., & Carvalho, V. M. D. (2015). Isolation of Escherichia coli and Salmonella spp. from free-ranging wild animals. Brazilian Journal of Microbiology, 46(4), 1257-1263.
  • Jijón S, Wetzel A, LeJeune J. Salmonella enterica isolated from wildlife at two Ohio rehabilitation centers (2007). J Zoo Wildl Med. Sep;38(3):409-13.
  • Lillehaug, A., Bergsjø, B., Schau, J., Bruheim, T., Vikøren, T., & Handeland, K. (2005). Campylobacter spp., Salmonella spp., verocytotoxic Escherichia coli, and antibiotic resistance in indicator organisms in wild cervids. Acta Veterinaria Scandinavica, 46(1), 23.
  • Mackintosh C, Haigh JC, Griffin F. (2002) Bacterial diseases of farmed deer and bison. Revue Scientifique et Technique (International Office of Epizootics). Aug;21(2):249-263.
  • Oğurlu, İ. (1988). İşletme ormanlarında yaban hayatı habitatlarının düzenlenmesi. Journal of the Faculty of Forestry Istanbul University, 38(2), 120-135.
  • Onbüyük, M. A., & Keskin, O. (2020) Yabani Kanatlılarda Salmonella Spp. İzolasyonu ve Serotiplendirilmesi. Dicle Üniversitesi Veteriner Fakültesi Dergisi, 13(2), 125-129.
  • Paulsen, P., Smulders, F. J. M., & Hilbert, F. (2012). Salmonella in meat from hunted game: A Central European perspective. Food Research International, 45(2), 609-616.
  • Popoff, M. Y., & Le Minor, L. E. (2015). Salmonella. Bergey's Manual of Systematics of Archaea and Bacteria, 1-1.
  • Rahn, K., De Grandis, S. A., Clarke, R. C., McEwen, S. A., Galan, J. E., Ginocchio, C., ... & Gyles, C. L. (1992). Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Molecular and cellular probes, 6(4), 271-279.
  • Renter David G., Gnad David P., Sargeant Jan M., Hygnstrom Scott E. (2006) Prevalence and Serovars of Salmonella in the Feces of Free-Ranging White-Tailed Deer (Odocoileus virginianus) in Nebraska, Journal of Wildlife Diseases, 42(3), 2006, pp. 699–703.
  • Rubini, S., Ravaioli, C., Previato, S., D’Incau, M., Tassinari, M., Guidi, E., ... & Bergamini, M. (2016). Prevalence of Salmonella strains in wild animals from a highly populated area of north-eastern Italy. Annali dell'Istituto superiore di sanita, 52(2), 277-280.
  • Sanchez, S., Hofacre, C. L., Lee, M. D., Maurer, J. J., & Doyle, M. P. (2002). Animal sources of salmonellosis in humans. Journal of the American Veterinary Medical Association, 221(4), 492-497.
  • Sato Y., Kobayashi C., Ichikawa K., Kuwamoto Y., Matsuura S., Koyama T.(1999) An Occurrence of Salmonella Typhimurium Infection in Sika Deer (Cervus nippon), Journal of Veterinary Medical Science, 2000, Volume 62, Issue 3, Pages 313-315.
  • Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis. (2011) 17(1):7-15.
  • Sieber, V., Robert, N., Schybli, M., Sager, H., Miserez, R., Engels, M., & Ryser-Degiorgis, M. P. (2010). Causes of mortality and diseases in farmed deer in Switzerland. Veterinary medicine international.
  • Simpson, K.M.J., Hill-Cawthorne, G.A., Ward, M.P. et al.(2018) Diversity of Salmonella serotypes from humans, food, domestic animals and wildlife in New South Wales, Australia. BMC Infect Dis 18, 623.
  • Skov MN, Madsen JJ, Rahbek C, Lodal J, Jespersen JB, Jørgensen JC, Dietz HH, Chriél M, Baggesen DL.(2008) Transmission of Salmonella between wildlife and meat-production animals in Denmark. J Appl Microbiol. Nov;105(5):1558-68.
  • WHO (2010): Laboratory protocol: Isolation of Salmonella spp. from food and animal faeces. Available at: http://antimicrobialresistance.dk/CustomerData/Files/Folders/6-pdf-protocols/63_18-05-isolation-of-salm-220610.pdf (Date of access: November 10, 2021).

İstanbul’da Bulunan Kızıl Geyiklerin (Cervus elaphus) Dışkılarında Salmonella spp. Varlığının Araştırılması

Year 2022, Volume: 7 Issue: 2, 110 - 114, 30.06.2022
https://doi.org/10.35229/jaes.1061914

Abstract

Yaban hayatı, hem evcil hayvanlar hem de insanlar için birçok infesiyöz etkenin önemli bir kaynağıdır. İnsanlar, evcil hayvanlar ve yaban hayatı arasındaki artan etkileşimler, infeksiyöz etkenlerin türler arası bulaşmasına neden olabilmektedir. Salmonella serovarlarının yaban hayvanlarının barsak florasında asemptomatik olarak bulunması ve çevreye yayılması sonucu kolaylıkla evcil hayvanlara bulaşabilmektedir. Bu çalışmada Türkiye’de yaban hayatının önemli bir üyesi olan kızıl geyik dışkılarında Salmonella türlerinin varlığı araştırıldı. İstanbul Belgrad Ormanı’ndaki Geyik Üretim Çiftliği’nde serbest halde yaşayan geyiklerden bir yıl boyunca her ay en az bir kez olmak üzere steril kuru plastik kaplara toplamda 240 dışkı örneği toplandı. Toplanan örnekler konvansiyonel kültür yöntemleri ve moleküler yöntemler (PCR) ile incelendi. İncelenen örneklerden Salmonella spp. izole edilmedi.

Project Number

TDK-2019-33776

References

  • Albufera, U., Bhugaloo-Vial, P., Issack, M. I., & Jaufeerally-Fakim, Y. (2009). Molecular characterization of Salmonella isolates by REP-PCR and RAPD analysis. Infection, genetics and evolution, 9(3), 322-327.
  • Ayanegui-Alcerreca, M. A., Wilson, P. R., Mackintosh, C. G., Collins-Emerson, J. M., Heuer, C., Midwinter, A. C., & Castillo-Alcala, F. (2007). Leptospirosis in farmed deer in New Zealand: a review. New Zealand veterinary journal, 55(3), 102-108.
  • Botti, V., Navillod, F. V., Domenis, L., Orusa, R., Pepe, E., Robetto, S., & Guidetti, C. (2013). Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Vet Ital, 49(2), 195-202.
  • Carrillo-Del Valle, M. D., J. A. De la Garza-García, E. Díaz-Aparicio, A. G. Valdivia-Flores, L. F. Cisneros-Guzmán, C. Rosario, Á. H. Manjarrez-Hernández, A. Navarro, J. Xicohtencatl-Cortes, P. Maravilla, and R. Hernández-Castro. (2016). Characterization of Escherichia coli strains from red deer (Cervus elaphus) faeces in a Mexican protected natural area. Eur. J. Wildl. Res. 62:415–421.
  • Carroll, D., Wang, J., Fanning, S., & McMahon, B. J. (2015). Antimicrobial resistance in wildlife: implications for public health. Zoonoses and public health, 62(7), 534-542.
  • Crawford, R. W., Rosales-Reyes, R., de la Luz Ramírez-Aguilar, M., Chapa-Azuela, O., Alpuche-Aranda, C., & Gunn, J. S. (2010). Gallstones play a significant role in Salmonella spp. gallbladder colonization and carriage. Proceedings of the National Academy of Sciences, 107(9), 4353-4358.
  • Çakın, M, Başaran Kahraman, B, Diren Sığırcı, B, Bağcıgil, A. (2020). Distribution of Salmonella serovars and characterization of isolates in cattle feces and environmental samples. Ankara Üniversitesi Veteriner Fakültesi Dergisi, 67 (3), 215-220.
  • Dos Santos, E. J. E., Azevedo, R. P., Lopes, A. T. S., Rocha, J. M., Albuquerque, G. R., Wenceslau, A. A., ... & Maciel, B. M. (2020). Salmonella spp. in Wild Free-Living Birds from Atlantic Forest Fragments in Southern Bahia, Brazil. BioMed research international, 2020.
  • Farias, L.F.P., Oliveira, C.J.B., Medardus, J.J., Molla, B.Z., Wolfe, B.A. and Gebreyes, W.A. (2015), Phenotypic and Genotypic Characterization of Salmonella enterica in Captive Wildlife and Exotic Animal Species in Ohio, USA. Zoonoses Public Health, 62: 438-444.
  • French, E., Rodriguez-Palacios, A., & LeJeune, J. T. (2010). Enteric bacterial pathogens with zoonotic potential isolated from farm-raised deer. Foodborne pathogens and disease, 7(9), 1031-1037.
  • Gorski L, Parker CT, Liang A, Cooley MB, Jay-Russell MT, Gordus AG, Atwill ER, Mandrell RE. (2011) Prevalence, distribution, and diversity of Salmonella enterica in a major produce region of California. Appl Environ Microbiol. Apr;77(8):2734-48.
  • Henderson T. G., Hemmingsen P. (1983) Faecal survey of deer for Yersinia pseudotuberculosis and Salmonella sp., New Zealand Veterinary Journal, Pages 225-226 | Published online: 23 Feb 2011.
  • Hilbert F, Smulders FJM, Chopra-Dewasthaly R, Paulsen P. Salmonella in the wildlife-human interface. Food Res Int 2012;45:603-8. Integrated Taxonomic Information System – Report (2012) https://www.itis.gov/servlet/SingleRpt/SingleRpt?search_topic=TSN&search_value=180694 (Date of access: November 5, 2021).
  • Iovine, R. D. O., Dejuste, C., Miranda, F., Filoni, C., Bueno, M. G., & Carvalho, V. M. D. (2015). Isolation of Escherichia coli and Salmonella spp. from free-ranging wild animals. Brazilian Journal of Microbiology, 46(4), 1257-1263.
  • Jijón S, Wetzel A, LeJeune J. Salmonella enterica isolated from wildlife at two Ohio rehabilitation centers (2007). J Zoo Wildl Med. Sep;38(3):409-13.
  • Lillehaug, A., Bergsjø, B., Schau, J., Bruheim, T., Vikøren, T., & Handeland, K. (2005). Campylobacter spp., Salmonella spp., verocytotoxic Escherichia coli, and antibiotic resistance in indicator organisms in wild cervids. Acta Veterinaria Scandinavica, 46(1), 23.
  • Mackintosh C, Haigh JC, Griffin F. (2002) Bacterial diseases of farmed deer and bison. Revue Scientifique et Technique (International Office of Epizootics). Aug;21(2):249-263.
  • Oğurlu, İ. (1988). İşletme ormanlarında yaban hayatı habitatlarının düzenlenmesi. Journal of the Faculty of Forestry Istanbul University, 38(2), 120-135.
  • Onbüyük, M. A., & Keskin, O. (2020) Yabani Kanatlılarda Salmonella Spp. İzolasyonu ve Serotiplendirilmesi. Dicle Üniversitesi Veteriner Fakültesi Dergisi, 13(2), 125-129.
  • Paulsen, P., Smulders, F. J. M., & Hilbert, F. (2012). Salmonella in meat from hunted game: A Central European perspective. Food Research International, 45(2), 609-616.
  • Popoff, M. Y., & Le Minor, L. E. (2015). Salmonella. Bergey's Manual of Systematics of Archaea and Bacteria, 1-1.
  • Rahn, K., De Grandis, S. A., Clarke, R. C., McEwen, S. A., Galan, J. E., Ginocchio, C., ... & Gyles, C. L. (1992). Amplification of an invA gene sequence of Salmonella typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Molecular and cellular probes, 6(4), 271-279.
  • Renter David G., Gnad David P., Sargeant Jan M., Hygnstrom Scott E. (2006) Prevalence and Serovars of Salmonella in the Feces of Free-Ranging White-Tailed Deer (Odocoileus virginianus) in Nebraska, Journal of Wildlife Diseases, 42(3), 2006, pp. 699–703.
  • Rubini, S., Ravaioli, C., Previato, S., D’Incau, M., Tassinari, M., Guidi, E., ... & Bergamini, M. (2016). Prevalence of Salmonella strains in wild animals from a highly populated area of north-eastern Italy. Annali dell'Istituto superiore di sanita, 52(2), 277-280.
  • Sanchez, S., Hofacre, C. L., Lee, M. D., Maurer, J. J., & Doyle, M. P. (2002). Animal sources of salmonellosis in humans. Journal of the American Veterinary Medical Association, 221(4), 492-497.
  • Sato Y., Kobayashi C., Ichikawa K., Kuwamoto Y., Matsuura S., Koyama T.(1999) An Occurrence of Salmonella Typhimurium Infection in Sika Deer (Cervus nippon), Journal of Veterinary Medical Science, 2000, Volume 62, Issue 3, Pages 313-315.
  • Scallan E, Hoekstra RM, Angulo FJ, et al. Foodborne illness acquired in the United States--major pathogens. Emerg Infect Dis. (2011) 17(1):7-15.
  • Sieber, V., Robert, N., Schybli, M., Sager, H., Miserez, R., Engels, M., & Ryser-Degiorgis, M. P. (2010). Causes of mortality and diseases in farmed deer in Switzerland. Veterinary medicine international.
  • Simpson, K.M.J., Hill-Cawthorne, G.A., Ward, M.P. et al.(2018) Diversity of Salmonella serotypes from humans, food, domestic animals and wildlife in New South Wales, Australia. BMC Infect Dis 18, 623.
  • Skov MN, Madsen JJ, Rahbek C, Lodal J, Jespersen JB, Jørgensen JC, Dietz HH, Chriél M, Baggesen DL.(2008) Transmission of Salmonella between wildlife and meat-production animals in Denmark. J Appl Microbiol. Nov;105(5):1558-68.
  • WHO (2010): Laboratory protocol: Isolation of Salmonella spp. from food and animal faeces. Available at: http://antimicrobialresistance.dk/CustomerData/Files/Folders/6-pdf-protocols/63_18-05-isolation-of-salm-220610.pdf (Date of access: November 10, 2021).
There are 31 citations in total.

Details

Primary Language English
Journal Section Articles
Authors

Cansu Engin 0000-0001-5840-9675

Mehmet Can Öztürk 0000-0003-4856-3796

Yalçın Abul 0000-0001-8783-9420

Ilgın Kekeç 0000-0002-0821-8376

Arzu Funda Bağcıgil 0000-0002-8838-7291

Project Number TDK-2019-33776
Early Pub Date June 16, 2022
Publication Date June 30, 2022
Submission Date January 23, 2022
Acceptance Date March 8, 2022
Published in Issue Year 2022 Volume: 7 Issue: 2

Cite

APA Engin, C., Öztürk, M. C., Abul, Y., Kekeç, I., et al. (2022). Investigating the Presence of Salmonella spp. in the Feces of Red Deer (Cervus elaphus) in Istanbul. Journal of Anatolian Environmental and Animal Sciences, 7(2), 110-114. https://doi.org/10.35229/jaes.1061914


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