İnci Başak KAYA, ÖZLEM ŞAHAN YAPICIER, MEHMET AKAN, KADİR SERDAR DİKER

Class 1 Integrons and the Antibiotic Resistance Profile of Salmonella Infantis Strains from Broiler Chickens

Salmonella infeksiyonları kanatlı hayvanlarda görülen ve ekonomik kayıplara neden olan en önemli hastalıklardan biridir. Etkenin zoonotik karakteri ve gıda kaynaklı infeksiyonlara neden olması da halk sağlığı açısından önem göstermektedir. Son yıllarda artan antibiyotik dirençliliği Salmonella infeksiyonlarının kontrolünü güçleştirmektedir. Türkiye'de non-tifoidal Salmonella serotiplerinden Salmonella Infantis'in oranı artış göstermektedir. Bu artış ile birlikte, diğer Salmonella serotiplerinde yaygın olarak görülen antimikrobiyal dirençliliğin Salmonella Infantis suşlarında da bilinmesi önem taşımaktadır. Bu çalışmada, sağlıklı broyler tavukların dışkılarından izole edilen Salmonella Infantis suşlarında antibiyotik dirençliliği ve plasmidler, transpozonlar gibi antibiyotik dirençliliğinin taşınmasında rol oynayan sınıf 1 integronların sıklığının araştırılması amaçlandı. Bu amaçla ISO 6579-2002 ve Kauffmann-White serotiplendirme şemasına göre identifiye edilen 150 adet Salmonella Infantis suşu kullanıldı. Suşların antibiyotik dirençleri CLSI 2011 standart protokolüne göre disk difüzyon yöntemi ile belirlendi ve PZR ile sınıf 1 integronlar araştırıldı. Elde edilen sonuçlara göre yüksek oranda çoklu antibiyotik dirençliliği (%89.3), yüksek oranda (%100) sefotaksim, siprofloksasin, gentamisin, seftazidime karşı duyarlılık ve incelenen suşların tamamında sınıf 1 integron varlığı tespit edildi. Sonuç olarak, Salmonella Infantis suşlarının hepsinde sınıf 1 integronların varlığı, bu suşların potansiyel direnç alıcı haline gelmesi bakımından önem taşıdığını göstermektedir

Broyler Tavuklardan Elde Edilen Salmonella Infantis Suşlarının Antibiyotik Direnç Profilleri ve Sınıf 1 İntegron Varlığı

Salmonella infections are one of the most important diseases and cause economic problems in poultry. The zoonotic feature of the agent and leading to food-borne infections are also important in public health issues. Increasing antibiotic resistance causes difficulties of controlling Salmonella infections, in recent years. Among non-typhoidal Salmonella serotypes the rate of Salmonella Infantis are increasing in Turkey. With this increase, it is important to know the antimicrobial resistance patterns of Salmonella Infantis strains as seen in other Salmonella serotypes. In this study, we aimed to investigate Salmonella Infantis strains which were isolated from feces of healthy broiler chickens for the presence of antibiotic resistance and frequency of Class 1 integrons that is responsible for the transfer of antibiotic resistance as plasmids, transposons. For this purpose a total of 150 S. Infantis strains which were isolated and identified according to the ISO 6579-2002 and Kauffmann-White serotyping scheme were used. Antimicrobial resistance of the strains was determined by the disc diffusion method following to the recommendations of CLSI 2011 standard protocol and also Class 1 integrons were investigated by PCR. According to the results, high rate of multi-drug antibiotic resistance (89.3%), high rate of sensitivity (100%) to cefotaxime, ciprofloxacin, gentamicin, ceftazidime were observed and also Class 1 integrons were determined in all isolates. In conclusion, the presence of Class 1 integron is all strains of Salmonella Infantis showed the potential importance of these strains as recipient for antibiotic resistance

PDF

___

1. Asgharpour F, Rajabnia R, Shahandashti EF, Marashi MA, Khalilian M, Moulana Z: Investigation of Class I integron in Salmonella Infantis and its association with drug resistance. Jundishapur J Microbiol, 7, 1-5, 2013. DOI: 10.5812/jjm.10019
2. Lutful Kabir SM: Avian colibacillosis and salmonellosis: A clooser look at epidemiology, pathogenesis, diagnosis, control and public health concerns. Int J Environ Res Public Health, 7, 89-104, 2010. DOI: 10.3390/ ijerph7010089
3. Majitanova L, Majitan T, Majitan V: Detection of the Class 1 integrons and SGI1 among Salmonella enterica serovar Typhimurium DT104, U302, DT120, DT193 and nontypable human isolates. Jpn J Infect Dis, 63, 292- 295, 2010.
4. European Food Safety Authority: The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2014. EFSA Journal, 14 (2): 4380, 2016.
5. Şahan Ö, Aral EM, Aden MMA, Aksoy A, Yılmaz Ö, Jahed R, Akan M: Türkiye’de broyler tavuk işletmelerinden izole edilen Salmonella serovarlarının antimikrobiyel direnç durumu. Ankara Üniv Vet Fak Derg, 63, 1-6, 2016.
6. Dionisi AM, Lucarelli C, Benedetti I, Owczarek S, Luzzi I: Molecular characterisatiobn of multidrug-resistant Salmonella enterica serotype Infantis from humans, animals and the environment in Italy. Int J Antimicrob Agents, 38, 384-389, 2011. DOI: 10.1016/j.ijantimicag.2011.07.001
7. Miller T, Prager R, Rabsch W, Fehlhaber K, Voss M: Epidemiological relationship between Salmonella Infantis isolates of human and broiler origin. Lohman Information, 45 (2): 27-31, 2010.
8. Firoozeh F, Zahraei-Salehi T, Shahcheraghi F: Molecular clonality and detection of Class 1 Integron in multidrug-resistant Salmonella enterica Isolates from animal and human in Iran. Microb Drug Resist, 20, 517-524, 2014. DOI: 10.1089/mdr.2013.0198
9. Lopes GV, Michael GB, Cardoso M, Schwarz S: Antimicrobial resistance and Class 1 integron-associated gene casettes in Salmonella enterica serovar Typhimurium isolated from pigs at slaughter and abottoir environment. Vet Microbiol, 194, 84-92, 2016. DOI: 10.1016/j. vetmic.2016.04.020
10. Tseng CS, Yen YC, Chang CC, Hsu YM: Polymorphism of gene cassette promoter variants of Class 1 integron harbored in S. Choleraesuis and Typhimurium isolated from Taiwan. BioMedicine, 4 (3): 29-34, 2014. doi: 10.7603/s40681-014-0020-3
11. Wu K, Wang F, Sun J, Wang Q, Chen Q, Yu S, Rui Y: Class 1 integron gene casettes in multidrug-resistant Gram-negative bacteria in southern China. Int J Antimicrob Agents, 40, 264-267, 2012. DOI: 10.1016/j. ijantimicag. 2012.05.017
12. Lopes GV, Michael GB, Cardoso M, Schwarz S: Identification and characterization of Salmonella enterica subsp. Enterica serovar Derby isolates carrying a new aadA26 gene cassette in a Class 1 integron obtained at pig slaughterhouses. Fems Microbiol Lett, 356, 71-78, 2014. DOI: 10.1111/1574-6968.12473
13. Wannaprasat W, Padungtod P, Chuanchuen R: Class 1 integrons and virulence genes in Salmonella enterica isolates from pork and humans. Int J Antimicrob Agents, 37, 457-461, 2010. DOI: 10.1016/j. ijantimicag.2010.12.001
14. Guerra B, Junker E, Miko A, Helmuth R, Mendoza MC: Characterization and localization of drug resistance determinants in multidrug-resistant, integron-carrying Salmonella enterica serotype Typhimurium strains. Microb Drug Resist, 10, 83-91, 2004. DOI: 10.1089/1076629041310136
15. Bilgili A: Kanatlılarda antibakteriyel ilaç kullanım seçenekleri ve sakıncaları. Ankara Üniv Vet Fak Derg, 41, 243-253, 1994.
16. Carraminana JJ, Rota C, Agustin I, Herrera A: High prevalence of multiple resistance to antibiotics in Salmonella serovars isolated from a poultry slaughterhouse in Spain. Vet Microbiol, 104, 133-139, 2004. DOI: 10.1016/j.vetmic.2004.08.010
17. Molbak K: Human health consequences of antimicrobial drugresistant Salmonella and other foodborne pathogens. Food Saf, 41, 1613- 1620, 2005. DOI: 10.1086/497599
18. Tessari ENC, Kanashiro AMI, Stoppe GFS, Luciano LR, Castro AGM, Cardoso ALSP: Important aspects of Salmonella in the poultry industry and in Public. In, Mahmoud BSM (Ed): Salmonella-A Dangerous Foodborne Pathogen. 181-206, InTech, Rijeka, Croatia, 2012.
19. Anonim: Yem Katkıları ve Premikslerin Üretimi, İthalatı, İhracatı, Satışı ve Kullanımı Hakkında Tebliğde Değişiklik Yapılmasına Dair Tebliğ. Tarım ve Köyişleri Bakanlığından. 21 Ocak 2006. Sayı: 26056 Tebliğ No: 2006/1 Resmi Gazete, 2006.
20. Nogrady N, Toth A, Kostyak A, Paszti J, Nagy B: Emergence of multidrug resistance clones of Salmonella Infantis in broiler chickens and humans in Hungary. J Antimicrob Chemother, 60, 645-648, 2007. DOI: 10.1093/jac/dkm249
21. Kudaka J, Itokazu K, Taira K, Iwai A, Kondo M, Susa T, Iwanaga M: Characterization of Salmonella isolated in Okinawa, Japan. Jpn J Infect Dis, 59, 15-19, 2006.
22. Morshed R, Peighambari SM: Drug resistance, plasmid profile and random amplified polymorphic DNA analysis of Iranian isolates of Salmonella Enteritidis. New Microbiol, 33, 47-56, 2010.
23. Rahmani M, Peighambari SM, Svendsen CA, Cavaco LM, Agerso Y, Hendriksen RS: Molecular clonality and antimicrobial resistance in Salmonella enterica serovars Enteritidis and Infantis from broilers in three Northern regions of Iran. BMC Vet Res, 9, 66, 2013. DOI: 10.1186/1746- 6148-9-66
24. Kim KY, Park JH, Kwak HS, Woo GJ: Characterization of the quinolone resistance mechanism in foodborne Salmonella isolates with high nalidixic acid resistance. Int J Food Microbiol, 146, 52-456, 2011. DOI: 10.1016/j.ijfoodmicro.2011.01.037
25. Burke L, Hopkins KL, Meunier D, de Pinna E, Fitzgerald-Hughes D, Humphreys H, Woodford N: Resistance to third-generation cephalosporins in human non-typhoidal Salmonella enterica isolates from England and Wales, 2010-12. J Antimicrob Chemother, 69, 977-981, 2014. DOI: 10.1093/ jac/dkt469
26. Izumiya H, Mori K, Higashide M, Tamura K, Takai N, Hirose K, Terajima J, Watanabe H: Identication of CTX-M-14 β-lactamase in a Salmonella enterica serovar Enteritidis isolate from Japan. Antimicrob Agents Chemother, 49, 2568-2570, 2005. DOI: 10.1128/AAC.49.6.2568- 2570.2005
27. Liakopoulos A, Geurts Y, Dierikx CM, Brouwer MSM, Kant A, Wit B, Heymans R, van Pelt W, Mevius DJ: Extended-spectrum cephalosporin resistant Salmonella enterica serovar Heidelberg strains, the Netherlands. Emerg Infect Dis, 22, 1257-1261, 2016. DOI: 10.3201/eid2207.151377
28. Kameyama M, Chuma T, Yokoi T, Yabata J, Tominaga K, Miyasako D, Iwata H, Okamoto K: Emergence of Salmonella enterica serovar Infantis harboring IncI1 Plasmid with blaCTX-M-14 in a broiler farm in Japan. J Vet Med Sci, 74, 1213-1216, 2012. DOI: 10.1292/jvms.11-0488
29. Poirel L, Carrer A, Pitout JD, Nordmann P: Integron mobilization unit as a source of mobility of antibiotic resistance genes. Antimicrob Agents Chemother, 53, 2492-2498, 2009. DOI: 10.1128/AAC.00033-09
30. Roy CP, Ingold A, Vanegas N, Martinez E, Merlino J, Merkier AK: Dissemination of multiple drug resistance genes by Class 1 integrons in Klebsiella pneumoniae isolates from four countries: a comparative study. Antimicrob Agents Chemother, 55, 3140-3149, 2011. DOI: 10.1128/ AAC.01529-10
31. Naghoni A, Ranjbar R, Tabaraie B, Farshad S, Owlia P, Safiri Z: High prevalence of integron-mediated resistance in clinical isolates of Salmonella enterica. Jpn J Infect Dis, 63, 417-21, 2010.
32. Khan AA, Ponce E, Nawaz MS, Cheng CM, Khan JA, West CS: Identification and characterization of Class 1 integron resistance gene cassettes among Salmonella strains isolated from imported sea-food. Appl Environ Microbiol, 75, 1192-1196, 2009. DOI: 10.1128/AEM.02054-08
33. Molla B, Miko A, Pries K, Hildebrandt G, Kleer J, Schroeter A: Class 1 integrons and resistance gene cassettes among multidrug resistant Salmonella serovars isolated from slaughter animals and foods of animal origin in Ethiopia. Acta Trop, 103, 142-149, 2007. DOI: 10.1016/j. actatropica.2007.05.018
34. Zhao S, Fedorka-Cray PJ, Friedman S, McDermott PF, Walker RD, Qaiyumi S: Characterization of Salmonella Typhimurium of animal origin obtained from the National Antimicrobial Resistance Monitoring System. Foodborne Pathog Dis, 2, 169-681, 2005. DOI: 10.1089/fpd.2005.2.169
35. Miko A, Pries K, Schroeter A, Helmuth R: Molecular mechanisms of resistance in multidrug-resistant serovars of Salmonella enterica isolated from foods in Germany. J Antimicrob Chemother. 56, 1025-1033, 2005. DOI: 10.1093/jac/dki365
36. Vo AT, van Duijkeren E, Gaastra W, Fluit AC: Antimicrobial resistance, class 1 integrons, and genomic island 1 in Salmonella isolates from Vietnam. PLoS One, 5, e9440, 2010. DOI: 10.1371/journal.pone.0009440
37. Abbasoğlu D, Akçelik M: Phenotypic and genetic characterization of multidrug-resistant Salmonella Infantis strains isolated from broiler chicken meats in Turkey. Biol J, 66, 406-410, 2011. DOI: 10.2478/s11756- 011-0051-0