High prevalence of clonally related multiple resistant Salmonella Infantis carrying class 1 integrons in broiler farms


Salmonella Infantis

How to Cite

Askari Badouei, M., Vaezi, H., Nemati, A., Ghorbanyoon, E., Firoozeh, F., Jajarmi, M., & Peighambari, S. M. (2021). High prevalence of clonally related multiple resistant Salmonella Infantis carrying class 1 integrons in broiler farms . Veterinaria Italiana, 57(3). https://doi.org/10.12834/VetIt.2269.13773.1


The poultry industry in Iran is the main supplier of protein in the food chain. In the present study, we showed the importance of the possible dissemination of clonally related multiple drug resistant (MDR) Salmonella Infantis in broiler farms in Iran. In total, 156 fecal samples belonging to 23 poultry farms in Razavi Khorasan province, northeast of Iran, were examined for the presence of Salmonella serovars. Molecular serotypes and serogroups, class 1 and 2 integron types, colistin resistance genes ( mcr1 and mcr2) and antimicrobial susceptibility patterns were determined on the recovered Salmonella isolates. Based on PCR analysis, 30 recovered Salmonella isolates were identified asS. Infantis (23 isolates; 76.6%),S. Enteritidis (six isolates; 20%), and one isolate (3.3%) was not serotyped by the applied method. Class 1 integrons were detected in 22 isolates (95.6%) and class 2 integrons were not detected in any of the isolates. Although colistin resistance was prevalent in disc diffusion test, mcr-1 and mcr-2 genes were not detected. All class 1 integrons carried the cassette aadA1 gene. All Salmonella isolates were resistant to colistin and amoxicillin/clavulanic acid and MDR patterns were observed in most (96.6%) isolates. This study revealed a high prevalence rate of S. Infantis and the presence of class 1 integrons in broiler farms. The presence of the same integron cassettes in the sequenced isolates suggests that strains are clonally related. Stringent monitoring programs are required to prevent the spreading of MDR Salmonella serovars into food chain via poultry products.




Akbarian R., Peighambari S.M., Morshed R. & Yazdani A. 2010. Survey of Salmonella infection in Iranian poultry flocks. Int J Vet Res, 4, 273–276.

Almeida F., Seribelli A.A., Medeiros M.I.C., Rodrigues D.D.P., de MelloVarani A., Luo Y., Allard M.W. & Falcão J.P. 2018. Phylogenetic and antimicrobial resistance gene analysis of Salmonella Typhimurium strains isolated in Brazil by whole genome sequencing. PLoS One, 13, e0201882.

Antunes P., Mourão J., Campos J. & Peixe L. 2016. Salmonellosis: the role of poultry meat. Clin Microbiol Infect, 22, 110–121.

Asadpour Y., Mohammadi M., Pourbakhsh S.A. & Rasa M. 2014. Isolation, serotyping and antibiotic resistance of Salmonella isolated from chicken carcasses in Guilan province. Iran Vet J, 9, 5–13.

Aziz S.A.A., Abdel-Latef G.K., Shany S.A.S. & Rouby S.R. 2018. Molecular detection of integron and antimicrobial resistance genes in multidrug resistant Salmonella isolated from poultry, calves and human in Beni-Suef governorate, Egypt. Beni-Suef Univ J basic Appl Sci, 7, 535–542.

Badouei M.A., Jajarmi M. & Mirsalehian A. 2015. Virulence profiling and genetic relatedness of Shiga toxin-producing Escherichia coli isolated from humans and ruminants. Comp Immunol Microbiol Infect Dis, 38, 15–20.

Barbieri N.L., Nielsen D.W., Wannemuehler Y., Cavender T., Hussein A., Yan S.G., Nolan L.K. & Logue C.M. 2017. mcr-1 identified in avian pathogenic Escherichia coli (APEC). PLoS One, 12, e0172997.

Borowiak M., Fischer J., Baumann B., Hammerl J.A., Szabo I. & Malorny B. 2018. Complete genome sequence of a VIM-1-producing Salmonella enterica subsp. enterica serovar Infantis isolate derived from minced pork meat. Genome Announc, 6, e00327-18.

Carramiñana J.J., Rota C., Agustin I. & Herrera A. 2004. High prevalence of multiple resistance to antibiotics in Salmonella serovars isolated from a poultry slaughterhouse in Spain. Vet Microbiol, 104, 133–139.

Chung Y.H., Kim S.Y. & Chang Y.H. 2003. Prevalence and antibiotic susceptibility of Salmonella isolated from foods in Korea from 1993 to 2001. J Food Prot, 66, 1154–1157.

Clinical and Laboratory Standards Institute (CLSI). 2018. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals (CLSI supplement VET08), 4th ed. PA, Clinical and Laboratory Standards Institute, Wayne.

Donado-Godoy P., Gardner I., Byrne B.A., Leon M., Perez-Gutierrez E., Ovalle M.V., Tafur M.A. & Miller W. 2012. Prevalence, risk factors, and antimicrobial resistance profiles of Salmonella from commercial broiler farms in two important poultry-producing regions of Colombia. J Food Prot, 75, 874–883.

El-Prince E., Hussein M.F. & El-Rahman A.M.A. 2019. Incidence of Salmonella species in table eggs and some egg-based products. J Adv Vet Res , 9, 1–7.

Ezatpanah E., Moradi Bidhendi S., Khaki P., Ghaderi R., Seyedan J.E. & Moghtadaee F.S. 2013. Detection, determination of serotypes and antibiotic resistance patterns of Salmonella strains isolated from Arak city poultry. Iran Vet J, 9, 88–96.

Fallah S.H., Asgharpour F., Naderian Z. & Moulana Z. 2013. Isolation and determination of antibiotic resistance patterns in nontyphoid Salmonella spp. isolated from chicken. Int J Enteric Pathog, 1, 17–21.

Firoozeh F., Mahluji Z., Khorshidi A. & Zibaei M. 2019. Molecular characterization of class 1, 2 and 3 integrons in clinical multi-drug resistant Klebsiella pneumoniae isolates. Antimicrob Resist Infect Control, 8, 59.

Firouzabadi A., Saadati D., Najimi M. & Jajarmi M. 2020. Prevalence and related factors of Salmonella spp. and Salmonella Typhimurium contamination among broiler farms in Kerman province, Iran. Prev Vet Med ,175, 104838.

Firoozeh F., Shahcheraghi F., Zahraei Salehi T., Karimi V. & Aslani M.M. 2011. Antimicrobial resistance profile and presence of class I integrongs among Salmonella enterica serovars isolated from human clinical specimens in Tehran, Iran. Iran J Microbiol, 3, 112.

Firoozeh F., Zahraei-Salehi T. & Shahcheraghi F. 2014. 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.

Gillings M., Boucher Y., Labbate M., Holmes A., Krishnan S., Holley M. & Stokes H.W. 2008. The evolution of class 1 integrons and the rise of antibiotic resistance. J Bacteriol, 190, 5095–5100.

Gupta R., Chauhan S.L., Kumar S., Jindal N., Mahajan N.K. & Joshi V.G. 2019. Carriage of Class 1 integrons and molecular characterization of intI1 gene in multidrug-resistant Salmonella spp. isolates from broilers. Vet World, 12, 609.

Hossain S., De Silva B.C.J., Dahanayake P.S., Shin G.-W. & Heo G.J. 2019. Molecular characterization of virulence, antimicrobial resistance genes, and class one integron gene cassettes in salmonella enterica subsp. enterica isolated from pet turtles in Seoul, Korea. J Exot Pet Med, 28, 209–217.

Irani M.D., Faghani M. & Doosti A. 2018. Study of class 1 to 3 integrons in salmonella and antimicrobial resistance pattern isolated from broiler chicks. Electron J Biol,14, 81–86.

Jajere S.M. 2019. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and antimicrobial resistance including multidrug resistance. Vet World, 12, 504.

Jorgensen J.H., Hindler J.F., Reller L.B. & Weinstein M.P. 2007. New consensus guidelines from the Clinical and Laboratory Standards Institute for antimicrobial susceptibility testing of infrequently isolated or fastidious bacteria. Clin Infect Dis, 44, 280–286.

Kardos G., Farkas T. & Antal M. 2007. Novel PCR assay for identification of Salmonella enterica serovar Infantis. Lett Appl Microbiol, 45, 421–425.

Kaushik M., Kumar S. & Kapoor R.K. 2018. Integrons in Enterobacteriaceae: diversity, distribution and epidemiology. Int J Antimicrob Agents, 51, 167–176.

Mainali C., McFall M., King R. & Irwin R. 2014. Evaluation of antimicrobial resistance profiles of Salmonella isolates from broiler chickens at slaughter in Alberta, Canada. J Food Prot, 77, 485–492.

Markey B., Leonard F. & Archambault M. 2013. Clinical Veterinary Microbiology. E-Book, Elsevier Health Sciences.

Marshall B.M. & Levy S.B. 2011. Food animals and antimicrobials: impacts on human health. Clin Microbiol Rev, 24, 718–733.

Mehdi Y., Létourneau-Montminy M.P. & Gaucher M.L. 2018. Use of antibiotics in broiler production: Global impacts and alternatives. Anim Nutr, 4, 170–178.

Merino L.A., Ronconi M.C. & Navia M.M. 2003. Analysis of the clonal relationship among clinical isolates of Salmonella enterica serovar Infantis by different typing methods. Rev Inst Med Trop Sao Paulo, 45, 119–123.

Nirmala T.V., Reddy A.D. & Karuna Sree E. 2018. Salmonellosis in poultry: a case report. Int J Curr Microbiol Appl Sci, 7, 2347–2349.

Peighambari S.M., Taheri H., Solgi H. & Shahcheraghi F. 2018. Pulse-Field Gel Electrophoresis (PFGE) of Salmonella Serovar Infantis Isolates From Poultry. Iran J Vet Med, 12, 197–198.

Rahmani M., Peighambari S.M. & Svendsen C.A. 2013. Molecular clonality and antimicrobial resistance in Salmonella entericaserovars Enteritidis and Infantis from broilers in three Northern regions of Iran. BMC Vet Res, 9, 66.

Reller L.B., Weinstein M., Jorgensen J.H. & Ferraro M.J. 2009. Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin Infect Dis, 49, 1749–1755.

Shabana S., Helmy S. & Hegazy A.E.-H. 2019. Characterization of class 1 integrons and some anti-microbial resistance genes in Salmonella species isolated from poultry in Egypt. Slov Vet Res, 56, 725-734.

Threlfall E.J. 2002. Antimicrobial drug resistance in Salmonella: problems and perspectives in food-and water-borne infections. FEMS Microbiol Rev, 26, 141–148.

VT Nair D., Venkitanarayanan K. & Kollanoor Johny A. 2018. Antibiotic-resistant Salmonella in the food supply and the potential role of antibiotic alternatives for control. Foods, 7,167.

Wajid M., Saleemi M.K., Sarwar Y. & Ali A. 2019. Detection and characterization of multidrug‐resistant Salmonella enterica serovar Infantis as an emerging threat in poultry farms of Faisalabad, Pakistan. J Appl Microbiol, 127, 248–261.

Zahraei Salehi T., Badouei M.A. & Madadgar O. 2013. Shepherd dogs as a common source for Salmonella enterica serovar Reading in Garmsar, Iran. Turkish J Vet Anim Sci , 37, 102–105.

Zhao X., Ye C., Chang W. & Sun S. 2017. Serotype distribution, antimicrobial resistance, and class 1 integrons profiles of Salmonella from animals in slaughterhouses in Shandong province, China. Front Microbiol, 8, 1049.

Zhu C., Yue M. & Rankin S. 2015. One-step identification of five prominent chicken Salmonella serovars and biotypes. J Clin Microbiol, 53, 3881–3883.