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Kırmızı yanaklı su kaplumbağalarında (Trachemys scripta elegans) Salmonella spp. varlığı ve antibakteriyel duyarlılıkları

Year 2018, Volume: 35 Issue: 4, 373 - 380, 15.12.2018

Selmin Özer , Merve Konucu Hülya Altıntaş Belkıs Levent , Revasiye Güleşen Mahmut Ülger

https://doi.org/10.12714/egejfas.2018.35.4.02
Cited By: 1

Abstract



Son yıllarda kırmızı yanaklı su
kaplumbağaları (Trachemys scripta elegans, Wied-Neuwied, 1839) ülkemizde
evcil hayvan olarak ilgi görmektedir. Sürüngen hayvanların normal bağırsak
mikrobiyotasında Salmonella türlerini barındırdıkları ise bilinen bir durumdur.
Ülkemizde evcil hayvan olarak satışı yapılan kırmızı yanaklı su kaplumbağaları
ile ilgili yapılmış herhangi bir mikrobiyolojik araştırmaya rastlanamamıştır.
Bu çalışmada, evcil hayvan işletmelerinde satışa sunulan kırmızı yanaklı su
kaplumbağalarında, insanlar için patojen olan Salmonella spp. varlığı ve
antibakteriyel ilaç duyarlılıkları araştırılmıştır.



Araştırma kapsamında, Mersin’de 10 ayrı
işletmeden 10’ar adet kaplumbağanın kloaka sürüntü örneği ve kaplumbağaların
içinde barındığı sudan 50 mL alınarak toplam 110 adet çalışılmıştır. Salmonella
izolasyonu ve identifikasyonu klasik teknikler, API20E ticari sistemi,
aglütinasyon yöntemine dayalı serolojik testler ve arbitrarily primed polimeraz
zincir reaksiyonu (AP-PZR) uygulanarak gerçekleştirilmiştir. İzolatların
antibakteriyel duyarlılık testi Kirby-Bauer disk difüzyon yöntemi ile
yapılmıştır.



Araştırma neticesinde beş adet
Salmonella spp. izole edilmiş, izolatlar 100 adet kırmızı yanaklı kaplumbağa
kloaka sürüntü örneğinin dördünde (% 4) ve 10 adet su örneğinin birinde (%  10) saptanmıştır. İzolatların tümünün
Salmonella enterica subsp. enterica serovar pomona [28; y; 1,7 (z60)] ve AP-PZR
sonuçlarına göre de izolatların aynı genotipik yapıya sahip oldukları
belirlenmiştir.



Antibakteriyel ilaç duyarlılık test
sonuçlarına göre izolatların tamamının ampisilin, enrofloksasin, gentamisin,
neomisin, siprofloksasin, streptomisin, tetrasiklin ve
sülfametoksazol-trimetoprime duyarlı; doksisilin’e orta derecede duyarlı;
amoksisilin, eritromisin, klindamisin, linkomisin, novobiosin, penisilin ve
vankomisin’e dirençli oldukları anlaşılmıştır.



Yapılmış olan literatür taramalarına
göre Salmonella enterica subsp. enterica serovar pomona ülkemizde ilk defa
saptanmıştır.



Sonuç olarak, Mersin’de satışı yapılan
kırmızı yanaklı su kaplumbağalarında ve paludaryum suyu örneğinde Salmonella
spp. saptanmış olup, özellikle çocuk, hamile, yaşlı ve bağışıklık sistemi
yetersizliği olan bireylerin bu hayvanlarla ve suyla temaslarında hijyen
kurallarına uymaları; insan sağlığının korunması amacıyla pet hayvanlardan
kaynaklanabilecek bulaş tehlikesinin daha ayrıntılı araştırılarak, gerekli
tedbirlerin alınması önem arz etmektedir. 



Keywords

Kırmızı yanaklı su kaplumbağası (Trachemys scripta elegans) Salmonella spp. AP-PZR antibakteriyel ilaç duyarlılığı

References

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  • Burger, J. (2009). Red-eared slider turtles (Trachemys scripta elegans). Retrieved from http://depts.washington.edu/oldenlab/wordpress/wp-content/uploads/2013/03/Trachemys-scripta-elegans_Burger.pdf (12.12.2017).
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  • Clara, M., Santiago, V. & Francisco, M.-J. (2016). Tiny turtles purchased at pet stores are a potential high risk for Salmonella human infection in the Valencian Region, Eastern Spain. Vector-Borne Zoonotic Diseases, 16(7), 455-460. DOI: 10.1089/vbz.2016.1950
  • Çiçek, K. & Ayaz, D. (2015). Does the red-eared slider (Trachemys scripta elegans) breed in Turkey? Hyla, 1, 4-10.
  • de Jong, B., Andersson, Y. & Ekdahl, K. (2005). Effect of Regulation and Education on Reptile-associated Salmonellosis. Emerging Infectious Diseases, 11(3), 398-403. DOI:  10.3201/eid1103.040694
  • Durmaz, R. & Ayan, M. (2001). Acinetobacter baumannii izolatlarinin moleküler epidemiyolojisinde Arbitrarily Primed “PZR ve Pulsed-Field Gel” Elektroforezi. In Durmaz R (Ed.), Uygulamali Moleküler Mikrobiyoloji (pp 219–228). Istanbul: Nobel Tip Kitabevleri.
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  • European Centre for Disease Prevention and Control (ECDC). (2017). Salmonellosis. Surveillance Atlas of Infectiuos Diseases. Retrived from http://atlas.ecdc.europa.eu/public/index.aspx (11.02.2018).
  • Gaertner, J.P., Hahn, D., Rose, F.L. & Forstner, M.R.J. (2008). Detection of Salmonellae in different turtle species within a headwater spring ecosystem. Journal of Wildlife Disseases, 44(2), 519–526. DOI: 10.7589/0090-3558-44.2.519. 
  • Gong, S., Wang, F., Shi, H., Zhou, P., Ge, Y., Hua, L. & Lui, W. (2014). Highly pathogenic Salmonella Pomona was first isolated from the exotic red-eared slider (Trachemys scripta elegans) in the wild in China: Implications for public health. Science of the Total Environment, 468, 28–30. DOI: 10.1016/j.scitotenv.2013.08.025
  • Hahn, D., Gaertner, J., Forstner, M.R.J. & Rose, F.L. (2007). High-resolution analysis of salmonellae from turtles within a headwater spring ecosystem. FEMS Microbiology Ecology, 60, 148–155. DOI:10.1111/j.1574-6941.2007.00275.x
  • Hidalgo-Vila, J., Díaz-Paniagua, C., Pérez-Santigosa, C., De Frutos-Escobar, C. & Herrero-Herrero, A. (2008). Salmonella in free-living exotic and native turtles and in pet exotic turtles from SW Spain. Research of Veterinary Science, 85, 449–452. DOI:10.1016/j.rvsc.2008.01.011
  • Kuroki, T., Ito, K., Ishihara, T., Furukawa, I., Kaneko, A., Suzuki, Y., Seto, J. & Kamiyama, T. (2015). Turtle-Associated salmonella infections in Kanagawa, Japan. Japanese Journal of Infectious Diseases, 68, 333–337. DOI: 10.7883/yoken.JJID.2014.490
  • List of Prokaryotic Names with Standing in Nomenclature (LPSN). (2017). Genus Salmonella. List of Prokaryotic Names. Retrived from http://www.bacterio.net/salmonella.html (10.02.2018).
  • Meervenne, E.V., Botteldoorn, N., Lokietek, S., Vatlet, M., Cupa, A., Naranjo, M., Dierick, K. & Bertrand, S. (2009). Turtle-associated Salmonella septicaemia and meningitis in a 2-month-old baby. Journal of Medical Microbiology, 58, 1379–1381. DOI: 10.1099/jmm.0.012146-0
  • Mughini-Gras, L., Heck, M. & van Pelt, W. (2016). Increase in reptile-associated human salmonellosis and shift toward adulthood in the age groups at risk, the Netherlands, 1985 to 2014. Eurosurveillance, 21(34), pii=30324. DOI: 10.2807/1560-7917
  • Nowakiewicz, A., Ziołkowska, G., Zieba, P., Stepniewska, K. & Tokarzewski, S. (2012). Russian tortoises (Agrionemys horsfieldi) as a potential reservoir for Salmonella spp. Research of Veterinary Science, 92, 187–190. DOI: 10.1016/j.rvsc.2011.03.019
  • Özcan, M., Kılıç, A., Kan, N. İ. & Sarıeyyüpoğlu, M. (2006). Tatlı su kaplumbağası (Mauremys caspica caspica Gmelin, 1774)’nda karaciğer, dalak, böbrek ve bağırsakların aerob bakteriler yönünden incelenmesi. Doğu Anadolu Bölgesi Araştırmaları, 23-26.
  • Özcan, M. & Sarıeyyüpoğlu, M. (2009). Investigation of Salmonella in fresh water turtle (Mauremys caspica caspica, Gmelin, 1774) from sewage discharged region into Keban Dam Lake, Elazığ. Kafkas Universitesi Veteriner Fakültesi Dergisi, 15(5), 759-763. DOI: 10.9775/kvfd.2009.104-A
  • Popoff, M.Y. (2001). Antigenic formulas of the Salmonella serovars. WHO Collaborating Center for Reference and Research on Salmonella. Paris: Institut Pasteur, France.
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  • Sánchez-Jiménez, M.M., Rincón-Ruiz, P.A., Duque, S., Giraldo, M.A., Ramírez-Monroy, D.M., Jaramillo, G. & Cardona-Castro, N. (2011). Salmonella enterica in semi-aquatic turtles in Colombia. Journal of Infection of Developing Countries, 5(5), 361-364. DOI: 10.3855/jidc.1126
  • Shane, S.M., Gilbert, R. & Harrington, K.S. (1990). Salmonella colonization in commercial pet turtles (Pseudemys scripta elegans). Epidemiology and Infection, 105, 307-316.
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Occurence and antibacterial susceptibility of Salmonella spp. on red-eared slider turtles (Trachemys scripta elegans)

Year 2018, Volume: 35 Issue: 4, 373 - 380, 15.12.2018

Selmin Özer , Merve Konucu Hülya Altıntaş Belkıs Levent , Revasiye Güleşen Mahmut Ülger

https://doi.org/10.12714/egejfas.2018.35.4.02
Cited By: 1

Abstract



In recent years, red-eared slider turtles (Trachemys scripta elegans, Wied-Neuwied, 1839) are popular among domestic pet animals, in Turkey. It is well known that intestinal microbiota of reptiles embody the types of human pathogenic Salmonella. In our country, there is no research about this issue. In this study the presence of Salmonella on red-eared slider turtles saled in pet shops in Mersin was determined. Also antibacterial susceptibilities of the isolates have been detected.



For this purpose, a total of 100 cloacal swab samples of 100 turtles and 10 water samples, provided from ten pet shops, were studied. Isolation and identification of Salmonella have been carried out by conventional techniques, API20E trade system, agglutination tests for serological diagnosis, and arbitrarily primed PCR (AP-PCR). Antibacterial susceptibility test was performed by Kirby-Bauer disk diffusion method.



As a result of this study, five Salmonella spp. have been isolated, four (4 %) from turtles, and one (10 %) from water. All the strains have been identified as Salmonella enterica subsp. enterica serovar pomona [28; y; 1.7 (z60)]. According to the results of AP-PCR the genotypic structure of the isolates were identical.



The antibacterial susceptibility results of the five isolates were also identical. All isolates were sensitive to ampicillin, enrofloxacin, gentamicin, neomycin, ciprofloxacin, streptomycin, tetracycline, and sulfamethoxazole-trimethoprim; moderately sensitive to doxycycline; and resistant to amoxicillin, erythromycin, clindamycin, lincomycin, novobiocin, penicillin, and vancomycin.



To best of our knowledge, this is the first detection of Salmonella enterica subsp. enterica serovar Pomona in our country. Findings of this study indicates that hygiene precautions are nessessary in contact with red eared water turtles and their paludarium water. Further investigations are necessary for protection of human health from the risk of microbiological contaminations by pet animals. 



Keywords

Red eared slider turtle (Trachemys scripta elegans) Salmonella spp. AP-PCR antibacterial susceptibility

References

  • Anğ, Ö., Özek, Ö., Çetin, E.T. & Töreci, K. (1973). Salmonella serotypes isolated from tortoises and frogs in İstanbul. Journal of Hygiene Cambridge, 71, 85-88.
  • Anğ, Ö., Töreci, K. & Anğ-Küçüker, M. (1993). Salmonellae and salmonellosis in Turkey. In F. Cabello, C. Hormaecehe, P. Mastroeni & L. Bonina (Eds.), Biology of Salmonella (pp. 25-33). New York: Plenum Press. DOI: 10.1007/978-1-4615-2854-8_4
  • Bertrand, S., Rimhanen-Finne, R., Weill, F.X., Rabsch, W., Thornton, L., Perevoscikovs, J., van Pelt, W. & Heck, M. (2008). Salmonella infection associated with reptiles: the current situation in Europe. Eurosurveillance, 13(4–6).
  • Bošnjak, I., Zdravković, N., Čolović, S., Ranđelović, S., Galić, N., Radojičić, M., Šekler, M., Aleksić-Kovačević, S. &, Krnjaić, D. (2016). Neglected zoonosis – The Prevalence of Salmonella spp. in pet reptiles in Serbia. Vojnosanitetski Pregled, 73(10), 980–982. DOI: 10.2298/VSP160809222B
  • Burger, J. (2009). Red-eared slider turtles (Trachemys scripta elegans). Retrieved from http://depts.washington.edu/oldenlab/wordpress/wp-content/uploads/2013/03/Trachemys-scripta-elegans_Burger.pdf (12.12.2017).
  • Center for Disease Control and Prevention (CDC). (1995). Reptile-Associated Salmonellosis-Selected States, 1994-1995. Morbidity and Mortality Weekly Report, 44(17), 347-350.
  • Center for Disease Control and Prevention (CDC). (2003). Reptile-Associated Salmonellosis-Selected States, 1998-2002. Morbidity and Mortality Weekly Report, 52(49), 1206-1209.
  • Center for Disease Control and Prevention (CDC). (2005). Salmonellosis Associated with Pet Turtles-Wisconsin and Wyoming, 2004. Morbidity and Mortality Weekly Report, 54(09), 223-226.
  • Center for Disease Control and Prevention (CDC). (2008). Multistate Outbreak of Human Salmonella Infections Associated with Exposure to Turtles-United States, 2007-2008. Morbidity and Mortality Weekly Report, 57(03): 69-72.
  • Center for Disease Control and Prevention (CDC). (2018). Reports of Selected Salmonella Outbreak Investigations. Salmonella infections linked to pet/small turtles 2012-2017. Retrived from http://www.cdc.gov/salmonella/outbreaks.html (04.01.2018).
  • Center for Food Security and Public Health (CFSPH). (2013). Reptile-Associated Salmonellosis. Retrived from http://www.cfsph.iastate.edu/ (04.01.2018).
  • Clinical and Laboratory Standards Institute (CLSI). (2012). Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard—Eleventh Edition. CLSI document M02-A11. Wayne, PA, 2012.
  • Chen, C.Y., Chen, W.C., Chin, S.C., Lai, Y.H., Tung, K.C., Chiou, C.S., Hsu, Y.M. & Chang, C.C. (2010). Prevalence and antimicrobial susceptibility of Salmonellae. Journal of Veterinary Diagnostic Investigation, 22, 44-50. DOI: 10.1177/104063871002200107
  • Clara, M., Santiago, V. & Francisco, M.-J. (2016). Tiny turtles purchased at pet stores are a potential high risk for Salmonella human infection in the Valencian Region, Eastern Spain. Vector-Borne Zoonotic Diseases, 16(7), 455-460. DOI: 10.1089/vbz.2016.1950
  • Çiçek, K. & Ayaz, D. (2015). Does the red-eared slider (Trachemys scripta elegans) breed in Turkey? Hyla, 1, 4-10.
  • de Jong, B., Andersson, Y. & Ekdahl, K. (2005). Effect of Regulation and Education on Reptile-associated Salmonellosis. Emerging Infectious Diseases, 11(3), 398-403. DOI:  10.3201/eid1103.040694
  • Durmaz, R. & Ayan, M. (2001). Acinetobacter baumannii izolatlarinin moleküler epidemiyolojisinde Arbitrarily Primed “PZR ve Pulsed-Field Gel” Elektroforezi. In Durmaz R (Ed.), Uygulamali Moleküler Mikrobiyoloji (pp 219–228). Istanbul: Nobel Tip Kitabevleri.
  • Erdem, B., Hasçelik, G., Gedikoğlu, S., Gür, D., Ercis, S., Sümerkan, B., Aysev, A.D., Tuncer, İ., Tuğrul, M., Tatman Otkun, M., Tuncer, A., Akgün, Y., Acar, N., Köksal, İ., Gültekin, M., Söyletir, G. & Elhan, A. (2004). Salmonella enterica serotipleri ve Salmonella enfeksiyonları: Türkiye’de on ili kapsayan çok merkezli bir çalışma. Mikrobiyoloji Bülteni, 38, 173-186.
  • European Centre for Disease Prevention and Control (ECDC). (2017). Salmonellosis. Surveillance Atlas of Infectiuos Diseases. Retrived from http://atlas.ecdc.europa.eu/public/index.aspx (11.02.2018).
  • Gaertner, J.P., Hahn, D., Rose, F.L. & Forstner, M.R.J. (2008). Detection of Salmonellae in different turtle species within a headwater spring ecosystem. Journal of Wildlife Disseases, 44(2), 519–526. DOI: 10.7589/0090-3558-44.2.519. 
  • Gong, S., Wang, F., Shi, H., Zhou, P., Ge, Y., Hua, L. & Lui, W. (2014). Highly pathogenic Salmonella Pomona was first isolated from the exotic red-eared slider (Trachemys scripta elegans) in the wild in China: Implications for public health. Science of the Total Environment, 468, 28–30. DOI: 10.1016/j.scitotenv.2013.08.025
  • Hahn, D., Gaertner, J., Forstner, M.R.J. & Rose, F.L. (2007). High-resolution analysis of salmonellae from turtles within a headwater spring ecosystem. FEMS Microbiology Ecology, 60, 148–155. DOI:10.1111/j.1574-6941.2007.00275.x
  • Hidalgo-Vila, J., Díaz-Paniagua, C., Pérez-Santigosa, C., De Frutos-Escobar, C. & Herrero-Herrero, A. (2008). Salmonella in free-living exotic and native turtles and in pet exotic turtles from SW Spain. Research of Veterinary Science, 85, 449–452. DOI:10.1016/j.rvsc.2008.01.011
  • Kuroki, T., Ito, K., Ishihara, T., Furukawa, I., Kaneko, A., Suzuki, Y., Seto, J. & Kamiyama, T. (2015). Turtle-Associated salmonella infections in Kanagawa, Japan. Japanese Journal of Infectious Diseases, 68, 333–337. DOI: 10.7883/yoken.JJID.2014.490
  • List of Prokaryotic Names with Standing in Nomenclature (LPSN). (2017). Genus Salmonella. List of Prokaryotic Names. Retrived from http://www.bacterio.net/salmonella.html (10.02.2018).
  • Meervenne, E.V., Botteldoorn, N., Lokietek, S., Vatlet, M., Cupa, A., Naranjo, M., Dierick, K. & Bertrand, S. (2009). Turtle-associated Salmonella septicaemia and meningitis in a 2-month-old baby. Journal of Medical Microbiology, 58, 1379–1381. DOI: 10.1099/jmm.0.012146-0
  • Mughini-Gras, L., Heck, M. & van Pelt, W. (2016). Increase in reptile-associated human salmonellosis and shift toward adulthood in the age groups at risk, the Netherlands, 1985 to 2014. Eurosurveillance, 21(34), pii=30324. DOI: 10.2807/1560-7917
  • Nowakiewicz, A., Ziołkowska, G., Zieba, P., Stepniewska, K. & Tokarzewski, S. (2012). Russian tortoises (Agrionemys horsfieldi) as a potential reservoir for Salmonella spp. Research of Veterinary Science, 92, 187–190. DOI: 10.1016/j.rvsc.2011.03.019
  • Özcan, M., Kılıç, A., Kan, N. İ. & Sarıeyyüpoğlu, M. (2006). Tatlı su kaplumbağası (Mauremys caspica caspica Gmelin, 1774)’nda karaciğer, dalak, böbrek ve bağırsakların aerob bakteriler yönünden incelenmesi. Doğu Anadolu Bölgesi Araştırmaları, 23-26.
  • Özcan, M. & Sarıeyyüpoğlu, M. (2009). Investigation of Salmonella in fresh water turtle (Mauremys caspica caspica, Gmelin, 1774) from sewage discharged region into Keban Dam Lake, Elazığ. Kafkas Universitesi Veteriner Fakültesi Dergisi, 15(5), 759-763. DOI: 10.9775/kvfd.2009.104-A
  • Popoff, M.Y. (2001). Antigenic formulas of the Salmonella serovars. WHO Collaborating Center for Reference and Research on Salmonella. Paris: Institut Pasteur, France.
  • Sajduda, A., Brzostek, A. & Popławska, M. (2004). Molecular characterization of rifampin and isoniazid resistant Mycobacterium tuberculosis strains isolated in Poland. Journal of Clinical Microbiology, 42, 2425-2431.
  • Sánchez-Jiménez, M.M., Rincón-Ruiz, P.A., Duque, S., Giraldo, M.A., Ramírez-Monroy, D.M., Jaramillo, G. & Cardona-Castro, N. (2011). Salmonella enterica in semi-aquatic turtles in Colombia. Journal of Infection of Developing Countries, 5(5), 361-364. DOI: 10.3855/jidc.1126
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There are 41 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Selmin Özer 0000-0001-6283-5976

Merve Konucu 0000-0003-2493-1523

Hülya Altıntaş 0000-0001-8686-7980

Belkıs Levent 0000-0002-2866-0823

Revasiye Güleşen 0000-0002-3975-3646

Mahmut Ülger 0000-0001-6649-4195

Publication Date December 15, 2018
Submission Date April 6, 2018
Published in Issue Year 2018Volume: 35 Issue: 4

Cite

APA Özer, S., Konucu, M., Altıntaş, H., Levent, B., et al. (2018). Kırmızı yanaklı su kaplumbağalarında (Trachemys scripta elegans) Salmonella spp. varlığı ve antibakteriyel duyarlılıkları. Ege Journal of Fisheries and Aquatic Sciences, 35(4), 373-380. https://doi.org/10.12714/egejfas.2018.35.4.02

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