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Infectious Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5265
ISSN (Online): 2212-3989

Research Article

Antimicrobial Resistance and Presence of Class 1 Integrons Among Different Serotypes of Salmonella spp. Recovered From Children with Diarrhea in Tehran, Iran

Author(s): Seyedeh Hanieh Eshaghi Zadeh, Hossein Fahimi, Fatemeh Fardsanei and Mohammad Mehdi Soltan Dallal*

Volume 20, Issue 2, 2020

Page: [160 - 166] Pages: 7

DOI: 10.2174/1871526519666190130171020

Price: $65

Abstract

Background: Salmonellosis is a major food-borne disease worldwide. The increasing prevalence of antimicrobial resistance among food-borne pathogens such as Salmonella spp. is concerning.

Objective: The main objective of this study is to identify class 1 integron genes and to determine antibiotic resistance patterns among Salmonella isolates from children with diarrhea.

Methods: A total of 30 Salmonella isolates were recovered from children with diarrhea. The isolates were characterized for antimicrobial susceptibility and screened for the presence of class 1 integron genes (i.e. intI1, sulI1, and qacEΔ1).

Results: The most prevalent serotype was Enteritidis 36.7%, followed by Paratyphi C (30%), and Typhimurium (16.7%). The highest rates of antibiotic resistance were obtained for nalidixic acid (53.3%), followed by streptomycin (40%), and tetracycline (36.7%). Regarding class 1 integrons, 36.7%, 26.7%, and 33.3% of the isolates carried intI1, SulI, and qacEΔ1, respectively, most of which (81.8%) were multidrug-resistant (MDR). Statistical analysis revealed that the presence of class 1 integron was significantly associated with resistance to streptomycin and tetracycline (p = 0.042). However, there was no association between class 1 integron and other antibiotics used in this study (p > 0.05).

Conclusion: The high frequency of integron class 1 gene in MDR Salmonella strains indicates that these mobile genetic elements are versatile among different Salmonella serotypes, and associated with reduced susceptibility to many antimicrobials.

Keywords: Salmonella, serotype, class 1 integrons, multidrug-resistant, children, diarrhea, antimicrobials resistance.

Graphical Abstract

[1]
Majowicz, S.E.; Musto, J.; Scallan, E.; Angulo, F.J.; Kirk, M.; O’Brien, S.J.; Jones, T.F.; Fazil, A.; Hoekstra, R.M. The global burden of nontyphoidal Salmonella gastroenteritis. Clin. Infect. Dis., 2010, 50(6), 882-889.
[http://dx.doi.org/10.1086/650733] [PMID: 20158401]
[2]
Fardsanei, F.; Soltan Dallal, M.M.; Douraghi, M.; Zahraei Salehi, T.; Mahmoodi, M.; Memariani, H.; Nikkhahi, F. Genetic diversity and virulence genes of Salmonella enterica subspecies enterica serotype Enteritidis isolated from meats and eggs. Microb. Pathog., 2017, 107, 451-456.
[http://dx.doi.org/10.1016/j.micpath.2017.04.026] [PMID: 28433796]
[3]
Eng, S-K.; Pusparajah, P.; Ab Mutalib, N-S.; Ser, H-L.; Chan, K-G.; Lee, L-H. Salmonella: A review on pathogenesis, epidemiology and antibiotic resistance. Front. Life Sci., 2015, 8, 284-293.
[http://dx.doi.org/10.1080/21553769.2015.1051243]
[4]
Campioni, F.; Moratto Bergamini, A.M.; Falcão, J.P. Genetic diversity, virulence genes and antimicrobial resistance of Salmonella Enteritidis isolated from food and humans over a 24-year period in Brazil. Food Microbiol., 2012, 32(2), 254-264.
[http://dx.doi.org/10.1016/j.fm.2012.06.008] [PMID: 22986188]
[5]
Gal-Mor, O.; Boyle, E.C.; Grassl, G.A. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol., 2014, 5, 391.
[http://dx.doi.org/10.3389/fmicb.2014.00391] [PMID: 25136336]
[6]
Soltan Dallal, M.M.; Sharifi Yazdi, M.K.; Mirzaei, N.; Kalantar, E. Prevalence of Salmonella spp. in packed and unpacked red meat and chicken in South of Tehran. Jundishapur J. Microbiol., 2014, 7(4)e9254
[http://dx.doi.org/10.5812/jjm.9254] [PMID: 25147699]
[7]
Firoozeh, F.; Zahraei-Salehi, T.; Shahcheraghi, F.; Karimi, V.; Aslani, M.M. Characterization of class I integrons among Salmonella enterica serovar Enteritidis isolated from humans and poultry. FEMS Immunol. Med. Microbiol., 2012, 64(2), 237-243.
[http://dx.doi.org/10.1111/j.1574-695X.2011.00883.x] [PMID: 22066813]
[8]
Asif, M.; Rahman, H.; Qasim, M.; Khan, T.A.; Ullah, W.; Jie, Y. Molecular detection and antimicrobial resistance profile of zoonotic Salmonella enteritidis isolated from broiler chickens in Kohat, Pakistan. J. Chin. Med. Assoc., 2017, 80(5), 303-306.
[http://dx.doi.org/10.1016/j.jcma.2016.11.007] [PMID: 28286058]
[9]
Deng, Y.; Bao, X.; Ji, L.; Chen, L.; Liu, J.; Miao, J.; Chen, D.; Bian, H.; Li, Y.; Yu, G. Resistance integrons: class 1, 2 and 3 integrons. Ann. Clin. Microbiol. Antimicrob., 2015, 14, 45.
[http://dx.doi.org/10.1186/s12941-015-0100-6] [PMID: 26487554]
[10]
Mazel, D. Integrons: agents of bacterial evolution. Nat. Rev. Microbiol., 2006, 4(8), 608-620.
[http://dx.doi.org/10.1038/nrmicro1462] [PMID: 16845431]
[11]
Majtán, V.; Majtánová, L.; Kovác, L. Analysis of integrons in human isolates of Salmonella enterica serovar typhimurium isolated in the Slovak Republic. FEMS Microbiol. Lett., 2004, 239(1), 25-31.
[http://dx.doi.org/10.1016/j.femsle.2004.08.013] [PMID: 15451097]
[12]
Wiesner, M.; Zaidi, M.B.; Calva, E.; Fernández-Mora, M.; Calva, J.J.; Silva, C. Association of virulence plasmid and antibiotic resistance determinants with chromosomal multilocus genotypes in Mexican Salmonella enterica serovar Typhimurium strains. BMC Microbiol., 2009, 9, 131.
[http://dx.doi.org/10.1186/1471-2180-9-131] [PMID: 19573249]
[13]
Fardsanei, F.; Nikkhahi, F.; Bakhshi, B.; Salehi, T.Z.; Tamai, I.A.; Soltan Dallal, M.M. Molecular characterization of Salmonella enterica serotype Enteritidis isolates from food and human samples by serotyping, antimicrobial resistance, plasmid profiling, (GTG)5-PCR and ERIC-PCR. New Microbes New Infect., 2016, 14, 24-30.
[http://dx.doi.org/10.1016/j.nmni.2016.07.016] [PMID: 27656286]
[14]
Performance standards for antimicrobial susceptibility testing, CLSI supplement M100S, 26th ed; Clinical and Laboratory Standards Institute: Wayne, PA, 2016.
[15]
Magiorakos, A.P.; Srinivasan, A.; Carey, R.B.; Carmeli, Y.; Falagas, M.E.; Giske, C.G.; Harbarth, S.; Hindler, J.F.; Kahlmeter, G.; Olsson-Liljequist, B.; Paterson, D.L.; Rice, L.B.; Stelling, J.; Struelens, M.J.; Vatopoulos, A.; Weber, J.T.; Monnet, D.L. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin. Microbiol. Infect., 2012, 18(3), 268-281.
[http://dx.doi.org/10.1111/j.1469-0691.2011.03570.x] [PMID: 21793988]
[16]
Ashtiani, M.T.; Monajemzadeh, M.; Kashi, L. Trends in antimicrobial resistance of fecal Shigella and Salmonella isolates in Tehran, Iran. Indian J. Pathol. Microbiol., 2009, 52(1), 52-55.
[http://dx.doi.org/10.4103/0377-4929.44964] [PMID: 19136781]
[17]
Farahani, NN; Jazi, FM; Nikmanesh, B; Asadolahi, P; Kalani, BS; Amirmozafari, N Prevalence and antibiotic susceptibility patterns of Salmonella and Shigella species isolated from pediatric diarrhea in Tehran. Arch Pediatr Infect Dis,, 2018, e57328.
[18]
Mahmoudi, S.; Pourakbari, B.; Moradzadeh, M.; Eshaghi, H.; Ramezani, A.; Haghi Ashtiani, M.T.; Keshavarz Valian, S.; Mamishi, S. Prevalence and antimicrobial susceptibility of Salmonella and Shigella spp. among children with gastroenteritis in an Iranian referral hospital. Microb. Pathog., 2017, 109, 45-48.
[http://dx.doi.org/10.1016/j.micpath.2017.05.023] [PMID: 28526638]
[19]
Li, Y.; Xie, X.; Xu, X.; Wang, X.; Chang, H.; Wang, C.; Wang, A.; He, Y.; Yu, H.; Wang, X.; Zeng, M. Nontyphoidal salmonella infection in children with acute gastroenteritis: prevalence, serotypes, and antimicrobial resistance in Shanghai, China. Foodborne Pathog. Dis., 2014, 11(3), 200-206.
[http://dx.doi.org/10.1089/fpd.2013.1629] [PMID: 24313784]
[20]
Sousa, M.A.B.; Mendes, E.N.; Penna, F.J.; Péret-Filho, L.A.; Magalhães, P.P. Acute diarrhea associated with Salmonella enterica in Belo Horizonte-MG: prevalence and characterization of isolates. J. Bras. Patol. Med. Lab., 2013, 49, 34-38.
[http://dx.doi.org/10.1590/S1676-24442013000100005]
[21]
Qu, M.; Lv, B.; Zhang, X.; Yan, H.; Huang, Y.; Qian, H.; Pang, B.; Jia, L.; Kan, B.; Wang, Q. Prevalence and antibiotic resistance of bacterial pathogens isolated from childhood diarrhea in Beijing, China (2010-2014). Gut Pathog., 2016, 8, 31.
[http://dx.doi.org/10.1186/s13099-016-0116-2] [PMID: 27303446]
[22]
Langendorf, C.; Le Hello, S.; Moumouni, A.; Gouali, M.; Mamaty, A.A.; Grais, R.F.; Weill, F.X.; Page, A.L. Enteric bacterial pathogens in children with diarrhea in Niger: diversity and antimicrobial resistance. PLoS One, 2015, 10(3)e0120275
[http://dx.doi.org/10.1371/journal.pone.0120275] [PMID: 25799400]
[23]
Campos, M.J.; Palomo, G.; Hormeño, L.; Herrera-León, S.; Domínguez, L.; Vadillo, S.; Píriz, S.; Quesada, A. Prevalence of quinolone resistance determinants in non-typhoidal Salmonella isolates from human origin in Extremadura, Spain. Diagn. Microbiol. Infect. Dis., 2014, 79(1), 64-69.
[http://dx.doi.org/10.1016/j.diagmicrobio.2014.01.010] [PMID: 24581744]
[24]
Fardsanei, F.; Soltan Dallal, M.M.; Douraghi, M.; Memariani, H.; Bakhshi, B.; Zahraei Salehi, T.; Nikkhahi, F. Antimicrobial resistance, virulence genes and genetic relatedness of Salmonella enterica serotype Enteritidis isolates recovered from human gastroenteritis in Tehran, Iran. J. Glob. Antimicrob. Resist., 2018, 12, 220-226.
[http://dx.doi.org/10.1016/j.jgar.2017.10.005] [PMID: 29045813]
[25]
Alizadeh-Hesar, M.; Bakhshi, B.; Najar-peerayeh, S. Molecular diagnosis of Salmonella enterica and Shigella spp. in stool sample of children with diarrhea in Tehran. Int J Enteric Pathog,, 2014, 2e17002.
[http://dx.doi.org/10.17795/ijep17002]
[26]
Arndt, M.B.; Mosites, E.M.; Tian, M.; Forouzanfar, M.H.; Mokhdad, A.H.; Meller, M.; Ochiai, R.L.; Walson, J.L. Estimating the burden of paratyphoid a in Asia and Africa. PLoS Negl. Trop. Dis., 2014, 8(6)e2925
[http://dx.doi.org/10.1371/journal.pntd.0002925] [PMID: 24901439]
[27]
Judd, M.C.; Mintz, E.D. Typhoid & paratyphoid fever. Centers for Disease Control and Prevention (CDC)., 2017.https://wwwnc.cdc.gov/travel/yellowbook/2018/infectious-diseases-related-to-travel/typhoid-paratyphoid-fever
[28]
Baghbani-arani, F.; Tajbakhsh, M.; Soltaniyeh, A.H.; Rajaei, B.; Siadat, S.D.; Aghasadeghi, M. Molecular typing of Salmonella paratyphi B and Salmonella paratyphi C isolates from clinical samples in Iran. J Fasa Univ Med Sci, 2012, 2, 19-25.
[29]
Irajian, G.; Ranjbar, R.; Moghadas, A.J. Detection of extended spectrum beta lactamase producing Salmonella spp. and multidrug resistance pattern. Iran. J. Pathol., 2009, 4, 128-132.
[30]
Uppal, B.; Perween, N.; Aggarwal, P.; Kumar, S.K. A comparative study of bacterial and parasitic intestinal infections in India. J. Clin. Diagn. Res., 2015, 9(3), DC01-DC04.
[http://dx.doi.org/10.7860/JCDR/2015/11965.5619] [PMID: 25954615]
[31]
Ranjbar, R.; Giammanco, G.M.; Farshad, S.; Owlia, P.; Aleo, A.; Mammina, C. Serotypes, antibiotic resistance, and class 1 integrons in Salmonella isolates from pediatric cases of enteritis in Tehran, Iran. Foodborne Pathog. Dis., 2011, 8(4), 547-553.
[http://dx.doi.org/10.1089/fpd.2010.0736] [PMID: 21204690]
[32]
Capuano, F.; Mancusi, A.; Capparelli, R.; Esposito, S.; Proroga, Y.T. Characterization of drug resistance and virulotypes of Salmonella strains isolated from food and humans. Foodborne Pathog. Dis., 2013, 10(11), 963-968.
[http://dx.doi.org/10.1089/fpd.2013.1511] [PMID: 24102078]
[33]
Fernández, J.; Guerra, B.; Rodicio, M.R. Resistance to carbapenems in non-typhoidal Salmonella enterica serovars from humans, animals and food. Vet. Sci., 2018, 5(2), 40.
[http://dx.doi.org/10.3390/vetsci5020040] [PMID: 29642473]
[34]
Firoozeh, F.; Shahcheraghi, F.; Zahraei Salehi, T.; Karimi, V.; Aslani, M.M. Antimicrobial resistance profile and presence of class I integrongs among Salmonella enterica serovars isolated from human clinical specimens in Tehran, Iran. Iran. J. Microbiol., 2011, 3(3), 112-117.
[PMID: 22347592]
[35]
Ranjbar, R.; Naghoni, A. Class 1 integron-mediated antibiotic resistance in Salmonella enterica strains isolated in Tehran, Iran. Iran. J. Med. Microbiol., 2014, 7, 16-23.
[36]
Asgharpour, F.; Rajabnia, R. Ferdosi, S.E.; Marashi, M.A.; Khalilian,M.; Moulana, Z.Investigation of class I integron in Salmonella infantis and its association with drug resistance. Jundishapur J. Microbiol., 2014, 7(5)e10019
[http://dx.doi.org/10.5812/jjm.10019] [PMID: 25147710]
[37]
Ribeiro, V.B.; Lincopan, N.; Landgraf, M.; Franco, B.D.G.M.; Destro, M.T. Characterization of class 1 integrons and antibiotic resistance genes in multidrug-resistant Salmonella enterica isolates from foodstuff and related sources. Braz. J. Microbiol., 2011, 42(2), 685-692.
[http://dx.doi.org/10.1590/S1517-83822011000200033] [PMID: 24031680]
[38]
Patchanee, P.; Zewde, B.M.; Tadesse, D.A.; Hoet, A.; Gebreyes, W.A. Characterization of multidrug-resistant Salmonella enterica serovar Heidelberg isolated from humans and animals. Foodborne Pathog. Dis., 2008, 5(6), 839-851.
[http://dx.doi.org/10.1089/fpd.2008.0149] [PMID: 18991546]
[39]
Dessie, H.K.; Bae, D.H.; Lee, Y.J. Characterization of integrons and their cassettes in Escherichia coli and Salmonella isolates from poultry in Korea. Poult. Sci., 2013, 92(11), 3036-3043.
[http://dx.doi.org/10.3382/ps.2013-03312] [PMID: 24135609]
[40]
Lopes, G.V.; Michael, G.B.; Cardoso, M.; Schwarz, S. Antimicrobial resistance and class 1 integron-associated gene cassettes in Salmonella enterica serovar Typhimurium isolated from pigs at slaughter and abattoir environment. Vet. Microbiol., 2016, 194, 84-92.
[http://dx.doi.org/10.1016/j.vetmic.2016.04.020] [PMID: 27142182]

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