Class1-3 integrons and antimicrobial resistance profile in Salmonella spp. isolated from broiler chicken in Western Iran

Salmonella broiler integrons 1-3 antimicrobial resistance Western Iran

Salmonella spp. are major etiologies of food-borne infections that are disseminated primarily through poultry to human. Nowadays, the high rate of antimicrobial resistance and the emergence of multi-drug resistant (MDR) strains, worse the threat imposed to the public health. Integrons are attributed as important contributors to MDR isolates. The present research aimed to identify the frequency of integrons 1-3 and the antimicrobial resistance patterns in Salmonella spp. isolated from broiler chicken in Western Iran. A total of 500 fecal samples were screened for Salmonella phenotypically. The isolates were confirmed genotypically and the frequency of integrons 1-3 was evaluated molecularly among the isolates. Besides, the antimicrobial resistance of the isolates was determined through the agar disk diffusion method. In general, 67 (13.4%) isolates of Salmonella spp. were recovered phenotypically, all of which were confirmed molecularly. The incidence of class 1, 2, and 3 integrons was 40.29% (27 isolates), 28.35% (19 isolates), and 11.94% (eight isolates), respectively. Coexistence of integrons was also detected in 26.86% of the isolates including class 1+2 (13 isolates, 40.62%), class 1+3 (2 isolates, 6.25%), and class 1+2+3 (3 isolates, 9.37%). No statistical association was detected between the frequencies of Salmonella spp. or Salmonella-bearing integron isolates with age, season, and location. The most frequent antimicrobial resistance was exhibited to ampicillin, nalidixic acid, trimethoprim-sulphamethoxazole, and tetracycline; while ciprofloxacin, gentamicin, and ceftazidime were the most effective drugs. 35.82% of the isolates were MDR, all of which harbored at least one class of integrons. Statistical assessment represented an association between the prevalence of integrons and tetracycline, chloramphenicol, streptomycin, and ceftazidime resistance rates. An alarming rate of integrons and MDR frequency among poultry-originated Salmonella spp. in the studied region demands the constant stewardship and prudent prescription and use of antibiotics to prevent human infections and preserve the effectiveness of those antibiotics in treating human salmonellosis.

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Abdel Aziz SA, Abdel-Latefa GK, Shanyb SAS, Roubyc SR (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.
Abdel-Maksoud M, Abdel-Khalek R, El-Gendy A, Gamal RF, Abdelhady HM, House BL (2015) Genetic characterization of multidrug-resistant Salmonella enterica serotypes isolated from poultry in Cairo, Egypt. Afr J Lab Med 4:158.
Al–Abadi IKM, Al-Mayah AAS (2012) Isolation and identification of Salmonella spp. from chicken and chicken environment in Basrah province. Iraqi Poult Sci J 6:88-99.
Ansari-Lari M, Shekarforoush S, Mehrshad S, Safari H (2014) Prevalence and risk factors for Salmonella spp. colonization in broiler flocks in Shiraz, southern Iran. Vet Res Forum 5:61-64.
Antunes P, Machado J, Sousa JC, Peixe L (2004) Dissemination amongst humans and food products of animal origin of a Salmonella Typhimurium clone expressing an integron-borne OXA-30 beta lactamase. J Antimicrob Chemother 54:429-34.
Asgharpour F, Rajabnia R, Shahandashti EF, Marashi MA, Khalilian M, Moulana Z (2014) Investigation of class I integron in Salmonella Infantis and its association with drug resistance. Jundishapur J Microbiol 7:e10019.
Asgharpour F, Marashi SMA, Moulana Z (2018) Molecular detection of class 1, 2 and 3 integrons and some antimicrobial resistance genes in Salmonella Infantis isolates. Iran J Microbiol 10:104-110.
Barraud O, Casellas M, Dagot C, Ploy MC (2013) An antibiotic-resistant class 3 integron in an Enterobacter cloacae isolate from hospital effluent. Clin Microbiol Infect 19:E306-308.
Barrow PA (2000) The paratyphoid Salmonellae. Rev Sci Tech Off Int Epiz 19:351-375.
Briggs CE, Fratamico PM, (1999) Molecular characterization of an antibiotic resistance gene cluster of Salmonella Typhimurium DT104. Antimicrob Agents Chemother 43:846-849.
Cambray G, Guerout AM, Mazel D (2010) Integrons. Annu Rev Genet 44:141-166.
Clemente L, Correia I, Themudo P, Neto I, Canica M, Bernardo F (2014) Antimicrobial susceptibility of Salmonella enterica isolates from healthy breeder and broiler flocks in Portugal. Vet J 200:276-281.
Carli KT, Eyigor A, Caner V (2001) Prevalence of Salmonella serovars in chickens in Turkey. J Food Prot 64:1832-1835.
Carattoli A (2001) Importance of integrons in the diffusion of resistance. Vet Res 32:243-259.
CLSI (2012) Methods for Dilution Antimicrobial Susceptibility Tests for Bacteria That Grow Aerobically; Approved Standard—Ninth Edition. Wayne, PA: Clinical and Laboratory Standards Institute.
Correa FE, Dantas FG, Grisolia AB, Crispim Bdo A, Oliveira KM (2014) Identification of class 1 and 2 integrons from clinical and environmental Salmonella isolates. J Infect Dev Ctries 8:1518-1524.
Dessie HK, Bae DH, Lee YJ (2013) Characterization of integrons and their cassettes in Escherichia coli and Salmonella isolates from poultry in Korea. Poult Sci 92:3036-3043.
Djeffal S, Bakour S, Mamache B, Elgroud R, Agabou A, Chabou S, Hireche S, Bouaziz O, Rahal K, Rolain JM (2017) Prevalence and clonal relationship of ESBL-producing Salmonella strains from humans and poultry in northeastern Algeria. BMC Vet Res 13:132.
Doosti Irani M, 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.
Doulatyabi S, Peighambari SM, Morshed R (2016) Survey of Salmonella infections in broiler farms around Sanandaj. J Ilam Uni Med Sci 25:70-78.
Eshraghi S, Dalall S, Mehdi M, Fardsanei F, Zahraii Salehi T, Nikmanesh B, Aminharati F, Abdosamadi Z, Akbari A (2010) Salmonella enteritidis and antibiotic resistance patterns: a study on 1950 children with diarrhea. Tehran Uni Med J 67:876-82.
Farahani NN, Jazi FM, Nikmanesh B, Asadolahi P, Kalani BS, Amirmozafari N (2018) Prevalence and antibiotic susceptibility patterns of Salmonella and Shigella species isolated from pediatric diarrhea in Tehran. Arch Pediatr Infect Dis 6:e57328.
Gong J, Xu M, Zhu C, Miao J, Liu X, Xu B, Zang J, Yu Y, Jia X (2013) Antimicrobial resistance, presence of integrons and biofilm formation of Salmonella pullorum isolates from eastern China (1962-2010). Avian Pathol 42:290-294.
Gaze WH, Abdouslam N, Hawkey PM, Wellington EM (2005) Incidence of class 1 integrons in a quaternary ammonium compound-polluted environment. Antimicrob Agents Chemother 49:1802-1807.
Goldstein C, Lee MD, Sanchez S, Hudson C, Phillips B, Register B, Grady M, Liebert C, Summers AO, White DJ, Maurer J (2001). Incidence of class 1 and 2 integrases in clinical and commensal bacteria from livestock, companion animals, and exotics. Antimicrob Agents Chemother 45:723-726.
Haeri A, Ahmadi E (2019) Fecal colonization of extended-spectrum beta lactamase-producing Salmonella spp. in broilers in Lorestan province of Iran. Int J Enteric Pathog 7:80-87.
Halawa M, Moawad A, Eldesouky I, Ramadan H (2016) Detection of antimicrobial phenotypes, β-lactamase encoding genes and class I integrons in Salmonella serovars isolated from broilers. Int J Poult Sci 15:1-7.
Hansson K, Sundstrom L, Pelletier A, Roy PH (2002) IntI2 integron integrase in Tn7. J Bacteriol 184:1712-1721.
Hugas M, Beloeil PA (2014) Controlling Salmonella along the food chain in the European Union – progress over the last ten years. Euro Surveill 19:19.
Idrees M, Mussarat U, Badshah Y, Qadir M, Bokhari H (2011) Prevalence of antimicrobial resistance and integrons in Escherichia coli from Punjab, Pakistan. Braz J Microbiol 42: 462-466.
Koeleman JG, Stoof J, Van Der Bijl MW, Vandenbroucke-Grauls CM, Savelkoul PH (2001). Identification of epidemic strains of Acinetobacter baumannii by integrase gene PCR. J Clin Microbiol 39:8-13.
Labbate M, Case RJ, Stokes HW (2009) The integron gene cassette system: an active player in bacterial adaptation. Methods Mol Biol 532:103-125.
Lamas A, Fernandez-No IC, Miranda JM, V´azquez B, Cepeda A, Franco1 CM (2016) Prevalence, molecular characterization and antimicrobial resistance of Salmonella serovars isolated from northwestern Spanish broiler flocks (2011–2015). Poult Sci 95:2097-2105.
Lu Y, Zhao H, Sun J, Liu Y, Zhou X, Beier RC, Wu G, Hou X (2014) Characterization of multidrug-resistant Salmonella enterica serovars Indiana and Enteritidis from chickens in eastern China. PLOS One 9:e96050.
Macedo-Viñas M, Cordeiro NF, Bado I, Herrera-Leon S, Vola M, Robino L, Gonzalez-Sanz R, Mateos S, Schelotto F, Algorta G, Ayala JA, Echeita A, Vignoli R (2009) Surveillance of antibiotic resistance evolution and detection of class 1 and 2 integrons in human isolates of multi-resistant Salmonella Typhimurium obtained in Uruguay between 1976 and 2000. Int J Infect Dis 13:342-348.
Mahero M, Byarugaba DK, Doetkott DK, Olet S, Khaitsa ML (2013) Antimicrobial resistance and presence of class 1 integrons in Salmonella serovars isolated from clinical cases of animals and humans in North Dakota and Uganda. Clin Microbial 2:128.
Malek MM, Amer FA, Allam AA, El-Sokkary RH, Gheith T, Arafa MA (2015) Occurrence of classes I and II integrons in Enterobacteriaceae collected from Zagazig University hospitals. Front Microbiol 6:601.
Mannion C, Fanning J, McLernon J, Lendrum L, Gutierrez M, Duggan S, Egan J (2012) The role of transport, lairage and slaughter process in the dissemination of Salmonella spp. in pigs in Ireland. Food Res Int 45:871-879.
Matthew M, Sykes RB (1977) Properties of the b-lactamase specified by the Pseudomonas plasmid RPL11. J Bacteriol 132:341-345.
Mazel D (2006) Integrons: agents of bacterial evolution. Nat Rev Microbiol 4:608-620.
Mirzaie S, Hassanzadeh M, Ashrafi I (2010) Identification and characterization of Salmonella isolates from captured house sparrows. Turkish J Vet Animal Sci 34:181-186.
Molla B, Miko A, Pries K (2007) Class 1 integron 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.
Morshed R, Peighambari SM (2010) Salmonella infections in poultry flocks in the vicinity of Tehran. Iran J Vet Med 4:273-276.
OIE (2019) Biosecurity procedures on poultry production. Terrestrial Animal Health Code - 28/06/2019: Office International des Epizooties (Paris), Chapter 6.5. 2019.
Okamoto AS, Andreatti Filho RL, Rocha TS, Menconi A, Marietto-Gonçalves GA (2009) Detection and transfer of antimicrobial resistance gene integron in Salmonella Enteritidis Derived from Avian Material. Brazil J Poultry Sci 11:195-201.
Parry CM, Threlfall EJ (2008) Antimicrobial resistance in typhoidal and nontyphoidal Salmonellae. Curr Opin Infect Dis 21:531-538.
Peighambari SM, Qorbaniun E, Morshed R, Haghbin Nazarpak H (2019) A survey on Salmonella infection in broiler farms around Mashhad city: determination of serogroups and antimicrobial resistance pattern of the Salmonella isolates. Iran Vet J 15: 34-43.
Peters ED, L-van MA, Box AT (2001) Novel gene cassettes and integrons. Antimicrob Agents Chemother 45:2961–2964.
Pui CF, Wong WC, Chai LC, Tunung R, Jeyaletchumi P, Noor Hidayah MS, Ubong A, Farinazleen MG, Cheah YK, Son R (2011) Salmonella: A foodborne pathogen. Int Food J Res. 18:465-473.
Rahmani M, Peighambari SM, Svendsen CA, Cavaco LM, Agerso Y, Hendriksen RS (2013) 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.
Rahn K, De Grandis SA, Clarke RC, McEwen SA, Galin JE, Ginocchio C, R. Curtiss 111 R, Gyles CL (1992) Amplification of an invA gene sequence of Salmonella Typhimurium by polymerase chain reaction as a specific method of detection of Salmonella. Mol Cell Probes 6:271-279.
Ramirez MS, Tolmasky ME (2010) Aminoglycoside modifying enzymes. Drug Resist 13:151-171.
Ranjbar R, Giammanco GM, Farshad S, Owlia P, Aleo A, Mammina C (2011) Serotypes, antibiotic resistance, and class 1 integrons in Salmonella isolates from pediatric cases of enteritis in Tehran, Iran. Foodborne Pathog Dis 8:547-553.
Recchia GD, Hall RM (1995) Gene cassettes: a new class of mobile element. Microbiol 141:3015-3027.
Roberts MC, Schwarz S, Aarts HJ (2012) Erratum: Acquired antibiotic resistance genes: an overview. Front Microbiol 3:384.
Sandvang D, Aarestrup FM, Jensen LB (1997) Characterization of integrons and antibiotic resistance genes in Danish multiresistant Salmonella enterica Typhimurium DT104. FEMS Microbiol Lett 157:177-181.
Shabana SM, Helmy SM, Abd El-Halem A, Hegazy M (2019) Characterization of class 1 integrons and some antimicrobial resistance genes in Salmonella species isolated from poultry in Egypt. Slov Vet Res 56:725-734.
Shan X, Huang M (2010) Multidrug resistance of bacteria and integron gene cassette system. Med Recapitulate 16:354-356.
Shaw KJ, Rather PN, Hare RS, Miller G H (1993) Molecular genetics of aminoglycoside resistance genes and familial relationships of the aminoglycoside-modifying enzymes. Microbiol Rev 57:138–163.
Seifi S, Khoshbakht R, Raeisi M (2016) Salmonellosis and related risk factors in broiler flocks in Mazandaran province, Northern Iran. Int J Enteric Pathog 4:e34031.
Su LH, Chiu CH, Chu CS, Ou JT (2004) Antimicrobial resistance in nontyphoid Salmonella serotypes: A global challenge. Clin Infect Dis 39:546-551.
Tennstedt T, Szczepanowski R, Braun S, Pühler A, Schlüter A (2003) Occurrence of integron-associated resistance gene cassettes located on antibiotic resistance plasmids isolated from a wastewater treatment plant. FEMS Microbiol Ecol 45:239-252.
Tribuddharat C, Fennewald M (1999) Integron mediated rifampin resistance in Pseudomonas aeruginosa, Antimicrob Agents Chemother 43:960-962.
Trongjit S, Angkititrakul S, Tuttle RE, Poungseree J, Padungtod P, Chuanchuen R (2017) Prevalence and antimicrobial resistance in Salmonella enterica isolated from broiler chickens, pigs and meat products in Thailand–Cambodia border provinces. Microbiol Immunol 61:23–33.
van Hoek AHAM, Mevius D, Guerra B, Mullany P, Roberts AP, Aarts HJM (2011) Acquired antibiotic resistance genes: an overview. Front Microbiol 2:203.
Wannaprasat W, Padungtod P, Chuanchuen R (2011) Class 1 integrons and virulence genes in Salmonella enterica isolates from pork and humans. Int J Antimicrob Agents 37: 457-461.
Wilke MS, Lovering AL, Strynadka NC. Beta-lactam antibiotic resistance: a current structural perspective (2005) Curr Opin Microbiol 8:525-533.
Yan H, Li L, Alam MJ, Shinoda S, Miyoshi S, Shi L (2010) Prevalence and antimicrobial resistance of Salmonella in retail foods in northern China. Int J Food Microbiol 143:230-234.
Zhao X, Yang J, Zhang B, Sun S, Chang W (2017) Characterization of integrons and resistance genes in Salmonella isolates from farm animals in Shandong province, China. Front Microbiol 8:1300.