Salmonella Infantis

Yıl 2023, Cilt: 94 Sayı: 1, 73 - 83, 15.01.2023

Cemil Kürekci , Seyda Şahin

https://doi.org/10.33188/vetheder.1130376

Öz

Salmonella enterica subsp. enterica serovar Infantis (S. Infantis) izolatlarının tespiti ve küresel yayılımı Türkiye’de dahil olmak üzere bir çok ülkede kanatlı ve kanatlı et örneklerinde artan oranda rapor edilmektedir. Ayrıca, S. Infantis Avrupa Birliği ülkelerinde ve Türkiye’de insanda salmonelloza neden olan en yaygın serotiplerden birisidir, bu nedenle de insan sağlığı açısından risk teşkil etmektedir. Bu durum genellikle çeşitli antimikrobiyal direnç ve virulens genleri ile ilişkilendirilen pESI (∼280 kb) olarak adlandırılan büyük bir megaplazmidin varlığı ile açıklanmaktadır. S. Infantis izolatlarında çoklu ilaç direnci belirlenmiş olup bu da insanlarda vakaların tedavisi sorusunu gündeme getirmektedir. Dolayısıyla, bu derlemede yeni ortaya çıkan problem epidemiyolojik ve genomik açıdan değerlendirildi. Sonuç olarak, insan olgularındaki S. Infantis’in gerçek prevalansının tam olarak açıklığa kavuşturulması gerektiği söylenebilir. Türkiye’de S. Infantis’in insanlara bulaşma yolunu araştıran herhangi bir çalışma olmamasına rağmen, asıl bulaşma kaynağının tavuk eti tüketimi olduğuna inanılmaktadır. Bu yüzden, insan ve hayvan kökenli izolatlarda tüm genom analizi yapılması ile S. Infantis epidemiyolojisinin anlaşılmasına katkı sağlayacaktır. Sonuçta, S. Infantis’in kanatlı hayvanların bağırsaklarında taşınmasını kontrol etmek için yeni politikalar başlatılabilir.

Anahtar Kelimeler

broyler, halk sağlığı, S. Infantis, pESI plazmid, virulens geni

Salmonella Infantis

Öz

The detection and global dissemination of Salmonella enterica subsp. enterica serovar Infantis (S. Infantis) isolates from poultry and poultry meat samples from various countries including Turkey have been increasingly reported. Additionally, S. infantis has been one of the most prevalent serovar causing human salmonellosis in European Union countries and in Turkey, is therefore a significant burden on human health. This was explained by the presence of a large megaplasmid termed as pESI (∼280 kb) that was often associated with various antimicrobial resistance traits as well as virulence genes. Worryingly, multi drug resistance in S. Infantis isolates have documented, raising the question of treating of cases in humans. Therefore, this review article concentrates on the epidemiological and genomics aspects of this emerging threat. As a result, it can be said that the true prevalence of S. Infantis in human cases must be fully understood. Although there are no studies exploring the transmission routes of S. Infantis to humans in Turkey, the consumption of chicken is believed to be the main exposure route. Therefore, analysis of the whole genome in isolates from human patients and animals will certainly provide insight for understanding S. Infantis epidemiology. Finally, new policies might be initiated to control the intestinal carriage of poultry.

Anahtar Kelimeler

broiler, public health, S. Infantis, pESI plasmid, virulence gene

Kaynakça

• Neuert S, Nair S, Day MR, Doumith M, Ashton PM, Mellor KC. et al. Prediction of phenotypic antimicrobial resistance profiles from whole genome sequences of non-typhoidal Salmonella enterica. Front Microbiol 2018;9:592.
• Eng SK, Pusparajah P, Ab Mutalib NS, Ser HL, Chan KG, Lee LH. Salmonella: a review on pathogenesis, epidemiology and antibiotic resistance. Front Life Sci 2015;8(3):284-293.
• Stanaway JD, Parisi A, Sarkar K, Blacker BF, Reiner RC, HaySI, et al. The global burden of non-typhoidal salmonella invasive disease: a systematic analysis for the Global Burden of Disease Study 2017. Lancet Infect Dis 2019;19(12);1312-1324.
• Li H, Wang H, D’Aoust JY, Maurer J. Salmonella species. In: Doyle MP. Buchanan RL. Editors. Food Microbiology: Fundamentals and Frontiers, ASM Press; 2012. p. 223-261.
• Flowers RS, D’Aoust JY, Andrews WH, Bailey JS. Salmonella. In Vanderzant C. Splittstoesser DF. Editors. Compendium of Methods for the Microbiological Examination of Foods. Washington: American Public Health Association; 1992. p. 371-422.
• International Standard Organization (ISO) Microbiology of the food chain-Horizontal method for the detection, enumeration and serotyping of Salmonella- Part 1: Detection of Salmonella spp. ISO 6579-1:2017. [cited 2022 April 4]; Available from: URL https://www.iso.org/standard/56712.html
• Wattiau P, Boland C, Bertrand S. Methodologies for Salmonella enterica subsp. enterica subtyping: gold standards and alternatives. Appl Environ Microbiol 2011;77(22):7877-7885.
• Issenhuth-Jeanjean S, Roggentin P, Mikoleit M, Guibourdenche M, De Pinna E, Nair S, et al. Supplement 2008–2010 (no. 48) to the white–Kauffmann–Le minor scheme. Res Microbiol 2014;165(7):526-530.
• Chen R, Cheng RA, Wiedmann M, Orsi RH. Development of a genomics-based approach to identify putative hypervirulent nontyphoidal Salmonella isolates: Salmonella enterica Serovar Saintpaul as a model. Msphere 2022;7(1):e00730-21.
• Guibourdenche M, Roggentin P, Mikoleit M, Fields PI, Bockemühl J, Grimont PA, et al. Supplement 2003–2007 (No. 47) to the white-Kauffmann-Le minor scheme. Res Microbiol 2010;161(1):26-29.
• Ando Y, Ono K, Tsuji R, Masutani T, Fujiwara Y, Kurazono T, et al. Investigation on contamination level of Salmonella spp. in chicken meat and analysis of Salmonella Infantis by PFGE method, Jpn J Food Microbiol 200;20:123-127.
• Gal-Mor O, Valinsky L, Weinberger M, Guy S, Jaffe J, Schorr YI, et al. Multidrug-resistant Salmonella enterica serovar Infantis, Israel. Emerg Infect Dis 2010;16(11):1754.
• Szmolka A, Szabó M, Kiss J, Pászti J, Adrián E, Olasz F, et al. Molecular epidemiology of the endemic multiresistance plasmid pSI54/04 of Salmonella Infantis in broiler and human population in Hungary. Food Microbiol 2018;71:25-31.
• Ulusal Salmonella Kontrol Programı (USKP), [online]. 2018. [cited 2021 July 16] Ulusal Salmonella kontrol programı sonuç raporu. Available from: URL: https://www.tarimorman.gov.tr/GKGM/Duyuru/323/Ulusal-Salmonella-Kontrol-Programi
• Aviv G, Cornelius A, Davidovich M, Cohen H, Suwandi A, Galeev A, Gal-Mor O. Differences in the expression of SPI-1 genes pathogenicity and epidemiology between the emerging Salmonella enterica serovar Infantis and the model Salmonella enterica serovar Typhimurium. J Infect Dis 2019;220(6); 1071-1081.
• EFSA and ECDC (European Food Safety Authority and European Centre for Disease Prevention and Control). The European Union One Health 2019 Zoonoses Report. EFSA J 2021;19(2):6406, pp.286.
• Centers for Disease Control and Prevention [online]. 2016 [cited 2022 April 4]; Available from: URL https://www.cdc.gov/nationalsurveillance/pdfs/2016-Salmonella-report-508.pdf.
• Nurmi E, Rantala M. New aspects of Salmonella Infection in broiler production. Nature 1973;241:210-211.
• Wegener HC, Baggesen DL. Investigation of an outbreak of human salmonellosis caused by Salmonella enterica ssp. enterica serovar Infantis by use of pulsed field gel electrophoresis. Int J Food Microbiol 1996;32(1-2):125-131.
• Nógrády N, Király M, Davies R, Nagy B. Multidrug resistant clones of Salmonella Infantis of broiler origin in Europe. Int J Food Microbiol 2012;157(1):108-112.
• Antunes P, Mourão J, Campos J, Peixe L. Salmonellosis: The role of poultry meat. Clin Microbiol Infect 2016;22(2):110-121.
• Alba P, Leekitcharoenphon P, Carfora V, Amoruso R, Cordaro G, Di Matteo P, Engage-Eurl-Ar Network Study Group. Molecular epidemiology of Salmonella Infantis in Europe: insights into the success of the bacterial host and its parasitic pESI-like megaplasmid. Microb Genom 2020;6(5): e000365.
• Carli KT, Eyigor A, Caner V. Prevalence of Salmonella serovars in chickens in Turkey. J Food Protect 2001; 64(11):1832-1835.
• Abbasoglu D, Akcelik M. Phenotypic and genetic characterization of multidrug-resistant Salmonella Infantis strains isolated from broiler chicken meats in Turkey. Biologia 2011;66(3):406-410.
• Şahan Ö, Aral EM, Aden MMA, Aksoy A, Yılmaz Ö, Jahed R, et al. Türkiye’deki broyler tavuk işletmelerinden izole edilen Salmonella serovarlarının antimikrobiyel direnç durumu. Ankara Üniv Vet Fak Derg 2016;3(1):1-6.
• Acar S, Bulut E, Durul B, Uner I, Kur M, Avsaroglu MD, Soyer Y. Phenotyping and genetic characterization of Salmonella enterica isolates from Turkey revealing arise of different features specific to geography. Int J Food Microbiol 2017;241:98-107.
• Acar S, Bulut E, Stasiewicz MJ, Soyer Y. Genome analysis of antimicrobial resistance, virulence, and plasmid presence in Turkish Salmonella serovar Infantis isolates. Int J Food Microbiol 2019;307: 108275.
• Arkali, A, Çetinkaya B. Molecular identification and antibiotic resistance profiling of Salmonella species isolated from chickens in eastern Turkey. BMC Vet Res 2020;16(1):1-8.
• Kürekci C, Sahin S, Iwan E, Kwit R, Bomba A, Wasyl D. Whole-genome sequence analysis of Salmonella Infantis isolated from raw chicken meat samples and insights into pESI-like megaplasmid. Int J Food Microbiol 2021;337:108956.
• Shahada F, Chuma T, Tobata T, Okamoto K, Sueyoshi M, Takase K. Molecular epidemiology of antimicrobial resistance among Salmonella enterica serovar Infantis from poultry in Kagoshima, Japan. Int J Antimicrob Agents 2006;28(4):302-307.
• Hauser E, Tietze E, Helmuth R, Junker E, Prager R, Schroeter A, et al. Clonal dissemination of Salmonella enterica serovar Infantis in Germany. Foodborne Pathog Dis 2012;9(4):352-360.
• Kasimoglu Dogru A, Ayaz ND, Gencay YE. Serotype identification and antimicrobial resistance profiles of Salmonella spp. isolated from chicken carcasses. Trop Anim Health Prod 2010;42(5):893-897.
• Franco A, Leekitcharoenphon P, Feltrin F, Alba P, Cordaro, G, Iurescia, M, et al. Emergence of a clonal lineage of multidrug-resistant ESBL-producing Salmonella Infantis transmitted from broilers and broiler meat to humans in Italy between 2011 and 2014. PloS One 2015;10(12):e0144802.
• Hindermann, D, Gopinath G, Chase H, Negrete F, Althaus D, Zurfluh K, et al. Salmonella enterica serovar Infantis from food and human infections, Switzerland, 2010-2015: poultry-related multidrug resistant clones and an emerging ESBL producing clonal lineage. Front Microbiol 2017;8:1322.
• Pate M, Mičunovič J, Golob M, Vestby LK, Ocepek M. Salmonella Infantis in broiler flocks in Slovenia: the prevalence of multidrug resistant strains with high genetic homogeneity and low biofilm-forming ability. Biomed Res Int 2019;1-13.
• Newton K, Gosling B, Rabie A, Davies R. Field investigations of multidrug-resistant Salmonella Infantis epidemic strain incursions into broiler flocks in England and Wales. Avian Pathol 2020;49(6):631-641.
• Bogomazova AN, Gordeeva VD, Krylova EV, Soltynskaya IV, Davydova EE, Ivanova OE, et al. Mega-plasmid found worldwide confers multiple antimicrobial resistance in Salmonella Infantis of broiler origin in Russia. Int J Food Microbiol 2020;319:108497.
• Ammar AM, Abdeen EE, Abo‐Shama UH, Fekry E, Kotb Elmahallawy E. Molecular characterization of virulence and antibiotic resistance genes among Salmonella serovars isolated from broilers in Egypt. Lett Appl Microbiol 2019;68(2):188-195.
• Ranjbar R, Rahmati H, Shokoohizadeh L. Detection of common clones of Salmonella enterica serotype Infantis from human sources in Tehran hospitals. Gastroenterol Hepatol Bed Bench 2018;11(1):54.
• Pardo-Este C, Lorca D, Castro-Severyn J, Krüger G, Alvarez-Thon L, Zepeda P, et al. Genetic characterization of Salmonella Infantis with multiple drug resistance profiles ısolated from a poultry-farm in Chile. Microorganisms 2021;9(11):2370.
• Aviv G, Tsyba K, Steck N, Salmon‐Divon M, Cornelius A, Rahav G, Gal‐Mor O. A unique megaplasmid contributes to stress tolerance and pathogenicity of an emergent Salmonella enterica serovar Infantis strain. Environ Microbiol 2014;16(4):977-994.
• Tate H, Folster JP, Hsu CH, Chen J, Hoffmann M, Li C, et al. Comparative analysis of extended-spectrum-β-lactamase CTX-M-65-producing Salmonella enterica serovar Infantis isolates from humans, food animals, and retail chickens in the United States. Antimicrob Agents Chemother 2017; 61(7):e00488-17.
• Yokoyama E, Ando N, Ohta T, Kanada A, Shiwa Y, Ishige, T, et al. A novel subpopulation of Salmonella enterica serovar Infantis strains isolated from broiler chicken organs other than the gastrointestinal tract. Vet Microbiol 2015;175(2-4):312-318.
• Egorova A, Mikhaylova Y, Saenko S, Tyumentseva M, Tyumentsev A, Karbyshev K, et al. Comparative Whole-Genome Analysis of Russian Foodborne Multidrug-Resistant Salmonella Infantis Isolates. Microorganisms 2022;10(1):89.
• García-Soto S, Abdel-Glil MY, Tomaso H, Linde J, Methner U. Emergence of multidrug-resistant Salmonella enterica subspecies enterica serovar infantis of multilocus sequence type 2283 in German broiler farms. Front Microbiol 2020;11:1741.
• Mughini-Gras L, van Hoek AH, Cuperus T, Dam-Deisz C, van Overbeek W, van den Beld M, et al. Prevalence, risk factors and genetic traits of Salmonella Infantis in Dutch broiler flocks. Vet Microbiol 2021;258:109120.
• Dos Santos AMP, Panzenhagen P, Ferrari RG, Rodrigues GL, Conte-Junior CA. The pESI mega-plasmid conferring virulence and multiple-drug resistance is detected in Salmonella Infantis genome from Brazil. Infect Genet Evol 2021;95:104934.
• Lee WW, Mattock J, Greig DR, Langridge GC, Baker D, Bloomfield S, et al. Characterization of a pESI-like plasmid and analysis of multidrug-resistant Salmonella enterica Infantis isolates in England and Wales. Microb Genom 2021;7(10): 000658.
• Argudín, MA, Hoefer A, Butaye P. Heavy metal resistance in bacteria from animals. Res Vet Sci 2019; 122:132-147.
• Villa L, García-Fernández A, Fortini D, Carattoli A. Replicon sequence typing of IncF plasmids carrying virulence and resistance determinants. J Antimicrob Chemother 2010;65(12):2518-2529.
• Sakano C, Kuroda M, Sekizuka T, Ishioka T, Morita Y, Ryo, A. et al. Genetic analysis of non-hydrogen sulfide-producing Salmonella enterica serovar Typhimurium and S. enterica serovar Infantis isolates in Japan. J Clin Microbiol 2013;51(1):328-330.
• Almeida F, Pitondo-Silva A, Oliveira MA, Falcão JP. Molecular epidemiology and virulence markers of Salmonella Infantis isolated over 25 years in São Paulo State, Brazil. Infect Genet Evol 2013;19:145-151.
• Mejía L, Medina JL, Bayas R, Salazar CS, Villavicencio F, Zapata S, et al. Genomic epidemiology of Salmonella Infantis in Ecuador: from poultry farms to human infections. Front Vet Sci 2020;7:547891.
• Durul B, Acar S, Bulut E, Kyere EO, Soyer Y. Subtyping of Salmonella food isolates suggests the geographic clustering of serotype Telaviv. Foodborne Pathog Dis 2015;12(12):958-965.
• Sarıçam S, Müştak HK. Kanatlı kökenli Salmonella Infantis suşlarının multilokus dizi tiplendirmesi ile filogenetik analizi. Ankara Üniv Vet Fak Derg 2018;65(4):407-411.
• Cesur A, Ulutaş SÖ, Soyer Y. Isolation and molecular characterization of Salmonella enterica and Escherichia coli from poultry samples. Turk J Vet Anim Sci 2019;43(3):408-422.
• Karacan Sever N, Akan M. Molecular analysis of virulence genes of Salmonella Infantis isolated from chickens and turkeys. Microb Pathog 2019;126:199-204.
• Lapierre L, Cornejo J, Zavala S, Galarce N, Sánchez F, Benavides MB, et al. Phenotypic and genotypic characterization of virulence factors and susceptibility to antibiotics in Salmonella Infantis strains isolated from chicken meat: First findings in Chile. Animals 2020;10(6):1049.
• Sırıken B. Salmonella patojenite adaları. Mikrobiyol Bul 2013;47(1):181-188.
• Namli S, Soyer Y. Investigation of class 1 integrons and virulence genes in the emergent Salmonella serovar Infantis in Turkey. Int Microbiol 2021;1-7.
• Nolle N, Felsl A, Heermann R, Fuchs TM. Genetic characterization of the galactitol utilization pathway of Salmonella enterica serovar Typhimurium. J Bacteriol 2017;199(4):e00595-16.
• Figueiredo R, Card R, Nunes C, Abuoun M, Bagnall MC, Nunez, J, et al. Virulence characterization of Salmonella enterica by a new microarray: Detection and evaluation of the cytolethal distending toxin gene activity in the unusual host S. Typhimurium. PLoS One 2015;10(8):e0135010.
• Ehuwa O, Jaiswal AK, Jaiswal S. Salmonella, food safety and food handling practices. Foods 2021; 10(5):907.
• Akan M. Kanatlılarda salmonella infeksiyonları ve kontrolünde temel prensipler. Mektup Ankara 2008;6:3-4.
• Van Oort R. Salmonella control: A global perspective. Poultry World 2021;1:18.
• Scharff RL. Food attribution and economic cost estimates for meat-and poultry-related illnesses. J Food Protect 2020;83(6):959-967.
• Türk Gıda Kodeksi (TGK) Mikrobiyolojik Kriterler Yönetmeliği, Sayı: 28145, Tarih: 29 Aralık 2011, Resmî Gazete, Başbakanlık Basımevi, Ankara.
• European Union [online]. Commission Regulation (EU) No 1086/2011 of 27 October 2011 amending Annex II to Regulation (EC) No 2160/2003 of the European Parliament and of the Council and Annex I to Commission Regulation (EC) No 2073/2005 as regards Salmonella in fresh poultry meat. 2022 April 4 [cited 2022 April 4]; Available from: URL https://eur-lex.europa.eu/legal-content/EN/TXT/?uri=CELEX%3A32011R1086
• Türk Gıda Kodeksi (TGK) Mikrobiyolojik Kriterler Yönetmeliğinde Değişiklik Yapılmasına Dair Yönetmelik, Sayı: 30560, Tarih: 9 Ekim 2018, Resmî Gazete, Başbakanlık Basımevi, Ankara.
• Barrow PA. Salmonella infections: immune and non-immune protection with vaccines. Avian Pathol 2007;36(1):1-13.
• Acevedo-Villanueva KY, Akerele GO, Al Hakeem WG, Renu S, Shanmugasundaram R, Selvaraj RK. A Novel approach against Salmonella: A review of polymeric nanoparticle vaccines for broilers and layers. Vaccines 2021;9(9):1041.
• Jones MK, Da Costa M, Hofacre CL, Baxter VA, Cookson K, Schaeffer J, et al. Evaluation of a modified live Salmonella typhimurium vaccination efficacy against Salmonella enterica serovar Infantis in broiler chickens at processing age. J Appl Poult Res 2021;30(2):100156.
• Loretz M, Stephan R, Zweifel C. Antimicrobial activity of decontamination treatments for poultry carcasses: a literature survey. Food Control 2010;21(6):791-804.