Molecular characterization of quinolones resistant Salmonella typhi isolates from patients infected with Typhoid fever in Al-Najaf province, Iraq
Main Article Content
Keywords
Typhoid fever, PMQR, qnrB, MLST
Abstract
Background: The global spread of typhoid fever is still a major public health concern. Typhoid fever is a potentially fatal infection often treated with quinolones, especially fluoroquinolones. Resistance to quinolones antibiotics in Salmonella typhi has made it harder to treat and has led to more mortalities. In this study, we detected of the qnr genes (plasmid-mediated quinolone resistance PMQR) in S.typhi isolated from patients in two main hospitals in AL-Najaf province, Iraq and determined the clonal relatedness between S.typhi isolates carried qnr genes.
Materials and Methods: Antimicrobial susceptibility tests were performed using the disc diffusion method to investigate the ability of S. typhi to the resistance of 10 antibiotics. Qnr genes (qnrA,qnrB,qnrS) were detected by PCR amplification, and clonal relatedness between S.typhi isolates harbor qnr genes was analyzed following multilocus sequence typing (MLST).
Results: Out of 246 blood samples collected from patients with suspected typhoid fever, 32 (13%) cases of S. typhi were identified using culture methods and confirmed using an automated Vitek-2 system. The highest antibiotic resistance rates were for ampicillin (24/32; 75%) and levofloxacin (19/32; 59.3%). All isolated (100%) were susceptible to ceftriaxone, cefixime, imipenem, meropenem, and azithromycin. Among PMQR genes determinants, qnrA, qnrB, and qnrS were positive in (1/32; 3%), (4/32; 12.5%) and (3/32; 9.3%) of the isolates, respectively. ST19, ST34, and ST36 were identified in (5/8; 62.5%), (2/8; 25%), and 1 (1/8; 12.5%) in S. typhi isolates positive for qnr genes,respectively.
Conclusion: The first study from Iraq demonstrated the presence of qnr genes in S. typhi clinical isolates. In comparison to qnrS and qnrA, the qnrB gene was more common. The first study used multilocus sequence typing (MLST) to identify the sequence types of S. typhi isolates from hospitals in Al-Najaf. The Majority of ST19 sequence type of S. typhi was found.
References
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26. Stepan RM, Sherwood JS, Petermann SR, Logue CM. Molecular and comparative analysis of Salmonella entericaSenftenberg from humans and animals using PFGE, MLST and NARMS. BMC Microbiol. 2011;11(1):1–9.
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28. Hardjo Lugito NP. Antimicrobial resistance of Salmonella enterica serovars Typhi and Paratyphi isolates from a general hospital in Karawaci, Tangerang, Indonesia: A five-year review. Int J Microbiol. 2017;2017.
29. Aljanaby AAJ, Medhat AR. Research article prevalence of some antimicrobials resistance associated-genes in Salmonella typhi isolated from patients infected with typhoid fever. J Biol Sci. 2017;17(4):171–84.
30. AL-Fatlawy HNK, AL-Hadrawi HAN. Molecular Profiling of Class I Integron Gene in MDR Salmonella Typhi Isolates. J Pure Appl Microbiol. 2020;14:1825–33.
31. Rahman BA, Wasfy MO, Maksoud MA, Hanna N, Dueger E, House B. Multi-drug resistance and reduced susceptibility to ciprofloxacin among Salmonella enterica serovar Typhi isolates from the Middle East and Central Asia. New microbes new Infect. 2014;2(4):88–92.
32. He J, Sun F, Sun D, Wang Z, Jin S, Pan Z, et al. Multidrug resistance and prevalence of quinolone resistance genes of Salmonella enterica serotypes 4,[5], 12: i:-in China. Int J Food Microbiol. 2020;330:108692.
33. Dong N, Li Y, Zhao J, Ma H, Wang J, Liang B, et al. The phenotypic and molecular characteristics of antimicrobial resistance of Salmonella enterica subsp. enterica serovar Typhimurium in Henan Province, China. BMC Infect Dis. 2020;20(1):1–11.
34. Njum AA, Hassan RN, Alwan JA. Identification of Antibiotic-Resistant Genes in Salmonella Typhi Isolated From Typhoid Patient in Samawa City. Iraqi J Sci. 2019;60(5):980–4.
35. Malehmir S, Ranjbar R, Harzandi N. The molecular study of antibiotic resistance to quinolones in Salmonella enterica strains isolated in Tehran, Iran. Open Microbiol J. 2017;11:189.
36. Salman HA, Abdulmohsen AM, Falih MN, Romi ZM. serovar Typhi isolated from Iraqi subjects. 2021;14:1922–8.
37. Bhetwal A, Maharjan A, Khanal PR, Parajuli NP. Enteric Fever Caused by Salmonella enterica Serovars with Reduced Susceptibility of Fluoroquinolones at a Community Based Teaching Hospital of Nepal. Int J Microbiol. 2017;2017.
38. Ali A, Ali HA, Shah FH, Zahid A, Aslam H, Javed B. Pattern of antimicrobial drug resistance of salmonella typhi and paratyphi a in a teaching hospital in Islamabad. J Pak Med Assoc. 2017;67(3):375–9.
39. Qamar FN, Azmatullah A, Kazi AM, Khan E, Zaidi AKM. A three-year review of antimicrobial resistance of Salmonella enterica serovars Typhi and Paratyphi A in Pakistan. J Infect Dev Ctries. 2014;8(8):981–6.
40. Tadesse G, Tessema TS, Beyene G, Aseffa A. Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: A systematic review and meta-analysis. PLoS One. 2018;13(2):e0192575.
41. Kim H Bin, Park CH, Kim CJ, Kim E-C, Jacoby GA, Hooper DC. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother. 2009;53(2):639–45.
42. Geetha VK, Yugendran T, Srinivasan R, Harish BN. Plasmid-mediated quinolone resistance in typhoidal Salmonellae: a preliminary report from South India. Indian J Med Microbiol. 2014;32(1):31–4.
43. Pribul BR, Festivo ML, Rodrigues MS, Costa RG, Rodrigues EC dos P, De Souza MMS, et al. Characteristics of quinolone resistance in Salmonella spp. isolates from the food chain in Brazil. Front Microbiol. 2017;8:299.
44. Rad M, Kooshan M, Mesgarani H. Quinolone resistance among Salmonella enterica and Escherichia coli of animal origin. Comp Clin Path. 2012;21(2):161–5.
45. Britto CD, Wong VK, Dougan G, Pollard AJ. A systematic review of antimicrobial resistance in Salmonella enterica serovar Typhi, the etiological agent of typhoid. PLoS Negl Trop Dis. 2018;12(10):e0006779.
46. Ranjbar R, Elhaghi P, Shokoohizadeh L. Multilocus sequence typing of the clinical isolates of Salmonella enterica serovar Typhimurium in Tehran Hospitals. Iran J Med Sci. 2017;42(5):443.
47. Sun J, Ke B, Huang Y, He D, Li X, Liang Z, et al. The molecular epidemiological characteristics and genetic diversity of Salmonella Typhimurium in Guangdong, China, 2007–2011. PLoS One. 2014;9(11):e113145.
48. Ke B, Sun J, He D, Li X, Liang Z, Ke C. Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007–2012 in Guangdong, China. BMC Infect Dis. 2014;14(1):1–10.
49. Lee S, Park N, Yun S, Hur E, Song J, Lee H, et al. Presence of plasmid-mediated quinolone resistance (PMQR) genes in non-typhoidal Salmonella strains with reduced susceptibility to fluoroquinolones isolated from human salmonellosis in Gyeonggi-do, South Korea from 2016 to 2019. Gut Pathog. 2021;13(1):1–7.
50. Gymoese P, Sørensen G, Litrup E, Olsen JE, Nielsen EM, Torpdahl M. Investigation of outbreaks of Salmonella enterica serovar Typhimurium and its monophasic variants using whole-genome sequencing, Denmark. Emerg Infect Dis. 2017;23(10):1631.
2. Tatavarthy A, Luna VA, Amuso PT. How multidrug resistance in typhoid fever affects treatment options. Ann N Y Acad Sci. 2014;1323(1):76–90.
3. Xie L, Ming L, Ding M, Deng L, Liu M, Cong Y. Paratyphoid Fever A: Infection and Prevention. Front Microbiol. 2022;13.
4. Adesiji YO, Deekshit VK, Karunasagar I. Antimicrobial‐resistant genes associated with Salmonella spp. isolated from human, poultry, and seafood sources. Food Sci Nutr. 2014;2(4):436–42.
5. Dutta S, Das S, Mitra U, Jain P, Roy I, Ganguly SS, et al. Antimicrobial resistance, virulence profiles and molecular subtypes of Salmonella enterica serovars Typhi and Paratyphi A blood isolates from Kolkata, India during 2009-2013. PLoS One. 2014;9(8):e101347.
6. Wong VK, Baker S, Pickard DJ, Parkhill J, Page AJ, Feasey NA, et al. Phylogeographical analysis of the dominant multidrug-resistant H58 clade of Salmonella Typhi identifies inter-and intracontinental transmission events. Nat Genet. 2015;47(6):632–9.
7. Das S, Samajpati S, Ray U, Roy I, Dutta S. Antimicrobial resistance and molecular subtypes of Salmonella enterica serovar Typhi isolates from Kolkata, India over a 15 years period 1998– 2012. Int J Med Microbiol. 2017;307(1):28–36.
8. Harish BN, Menezes GA, Sarangapani K, Parija SC. A case report and review of the literature: Ciprofloxacin resistant Salmonella enterica serovar Typhi in India. J Infect Dev Ctries. 2008;2(04):324–7.
9. Cuypers WL, Jacobs J, Wong V, Klemm EJ, Deborggraeve S, Van Puyvelde S. Fluoroquinolone resistance in Salmonella: insights by whole-genome sequencing. Microbgenomics. 2018;4(7).
10. Nüesch-Inderbinen M, Abgottspon H, Sägesser G, Cernela N, Stephan R. Antimicrobial susceptibility of travel-related Salmonella enterica serovar Typhi isolates detected in Switzerland (2002–2013) and molecular characterization of quinolone resistant isolates. BMC Infect Dis. 2015;15(1):1–5.
11. Malla S, Kansakar P, Serichantalergs O, Rahman M, Basnet S. Epidemiology of typhoid and paratyphoid fever in Kathmandu: two years study and trends of antimicrobial resistance. JNMA J Nepal Med Assoc. 2005;44(157):18–22.
12. Cattoir V, Weill F-X, Poirel L, Fabre L, Soussy C-J, Nordmann P. Prevalence of qnr genes in Salmonella in France. J Antimicrob Chemother.2007;59(4):751–4.
13. Ruiz J. Transferable mechanisms of quinolone resistance from 1998 onward. Clin Microbiol Rev. 2019;32(4):e00007-19.
14. Aldred KJ, Kerns RJ, Osheroff N. Mechanism of quinolone action and resistance. Biochemistry. 2014;53(10):1565–74.
15. Karp BE, Campbell D, Chen JC, Folster JP, Friedman CR. Plasmid‐mediated quinolone resistance in human non‐typhoidal Salmonella infections: An emerging public health problem in the United States. Zoonoses Public Health. 2018;65(7):838–49.
16. Tran JH, Jacoby GA, Hooper DC. Interaction of the plasmid-encoded quinolone resistance protein Qnr with Escherichia coli DNA gyrase.Antimicrob Agents Chemother. 2005;49(1):118– 25.
17. Seo KW, Lee YJ. Characterization of plasmid mediated quinolone resistance determinants in ciprofloxacin resistant-Escherichia coli from chicken meat produced by integrated broiler operations in Korea. Int J Food Microbiol. 2019;307:108274.
18. Tran JH, Jacoby GA, Hooper DC. Interaction of the plasmid-encoded quinolone resistance protein QnrA with Escherichia coli topoisomerase IV. Antimicrob Agents Chemother. 2005;49(7):3050–2.
19. Hooper DC, Jacoby GA. Mechanisms of drug resistance: quinolone resistance. Ann N Y Acad Sci. 2015;1354(1):12–31.
20. Ranjbar R, Karami A, Farshad S, Giammanco GM, Mammina C. Typing methods used in the molecular epidemiology of microbial pathogens: a how-to guide. New Microbiol. 2014;37(1):1–15.
21. Ranjbar R, Naghoni A, Farshad S, Lashini H, Najafi A, Sadeghifard N, et al. Use of TaqMan® real-time PCR for rapid detection of Salmonella enterica serovar Typhi. Acta Microbiol Immunol Hung. 2014;61(2):121–30.
22. Liu Y-Y, Chen C-C, Chiou C-S. Construction of a pan-genome allele database of Salmonella enterica serovar enteritidis for molecular subtyping and disease cluster identification. Front Microbiol. 2016;7:2010.
23. Tiba-Casas MR, Sacchi CT, Gonçalves CR, Almeida EA, Soares FB, de Jesus Bertani AM, et al. Molecular analysis of clonally related Salmonella Typhi recovered from epidemiologically unrelated cases of typhoid fever, Brazil. Int J Infect Dis. 2019;81:191–5.
24. Ashton PM, Nair S, Peters TM, Bale JA, Powell DG, Painset A, et al. Identification of Salmonella for public health surveillance using whole genome sequencing. PeerJ. 2016;4:e1752.
25. Zhang Z, Yang J, Xu X, Zhou X, Shi C, Zhao X, et al. Co-existence of mphA, oqxAB and blaCTXM-65 on the IncHI2 Plasmid in highly drugresistant Salmonella enterica serovar Indiana ST17 isolated from retail foods and humans in China. Food Control. 2020;118:107269.
26. Stepan RM, Sherwood JS, Petermann SR, Logue CM. Molecular and comparative analysis of Salmonella entericaSenftenberg from humans and animals using PFGE, MLST and NARMS. BMC Microbiol. 2011;11(1):1–9.
27. Leekitcharoenphon P, Lukjancenko O, Friis C, Aarestrup FM, Ussery DW. Genomic variation in Salmonella enterica core genes for epidemiological typing. BMC Genomics. 2012;13(1):1–12.
28. Hardjo Lugito NP. Antimicrobial resistance of Salmonella enterica serovars Typhi and Paratyphi isolates from a general hospital in Karawaci, Tangerang, Indonesia: A five-year review. Int J Microbiol. 2017;2017.
29. Aljanaby AAJ, Medhat AR. Research article prevalence of some antimicrobials resistance associated-genes in Salmonella typhi isolated from patients infected with typhoid fever. J Biol Sci. 2017;17(4):171–84.
30. AL-Fatlawy HNK, AL-Hadrawi HAN. Molecular Profiling of Class I Integron Gene in MDR Salmonella Typhi Isolates. J Pure Appl Microbiol. 2020;14:1825–33.
31. Rahman BA, Wasfy MO, Maksoud MA, Hanna N, Dueger E, House B. Multi-drug resistance and reduced susceptibility to ciprofloxacin among Salmonella enterica serovar Typhi isolates from the Middle East and Central Asia. New microbes new Infect. 2014;2(4):88–92.
32. He J, Sun F, Sun D, Wang Z, Jin S, Pan Z, et al. Multidrug resistance and prevalence of quinolone resistance genes of Salmonella enterica serotypes 4,[5], 12: i:-in China. Int J Food Microbiol. 2020;330:108692.
33. Dong N, Li Y, Zhao J, Ma H, Wang J, Liang B, et al. The phenotypic and molecular characteristics of antimicrobial resistance of Salmonella enterica subsp. enterica serovar Typhimurium in Henan Province, China. BMC Infect Dis. 2020;20(1):1–11.
34. Njum AA, Hassan RN, Alwan JA. Identification of Antibiotic-Resistant Genes in Salmonella Typhi Isolated From Typhoid Patient in Samawa City. Iraqi J Sci. 2019;60(5):980–4.
35. Malehmir S, Ranjbar R, Harzandi N. The molecular study of antibiotic resistance to quinolones in Salmonella enterica strains isolated in Tehran, Iran. Open Microbiol J. 2017;11:189.
36. Salman HA, Abdulmohsen AM, Falih MN, Romi ZM. serovar Typhi isolated from Iraqi subjects. 2021;14:1922–8.
37. Bhetwal A, Maharjan A, Khanal PR, Parajuli NP. Enteric Fever Caused by Salmonella enterica Serovars with Reduced Susceptibility of Fluoroquinolones at a Community Based Teaching Hospital of Nepal. Int J Microbiol. 2017;2017.
38. Ali A, Ali HA, Shah FH, Zahid A, Aslam H, Javed B. Pattern of antimicrobial drug resistance of salmonella typhi and paratyphi a in a teaching hospital in Islamabad. J Pak Med Assoc. 2017;67(3):375–9.
39. Qamar FN, Azmatullah A, Kazi AM, Khan E, Zaidi AKM. A three-year review of antimicrobial resistance of Salmonella enterica serovars Typhi and Paratyphi A in Pakistan. J Infect Dev Ctries. 2014;8(8):981–6.
40. Tadesse G, Tessema TS, Beyene G, Aseffa A. Molecular epidemiology of fluoroquinolone resistant Salmonella in Africa: A systematic review and meta-analysis. PLoS One. 2018;13(2):e0192575.
41. Kim H Bin, Park CH, Kim CJ, Kim E-C, Jacoby GA, Hooper DC. Prevalence of plasmid-mediated quinolone resistance determinants over a 9-year period. Antimicrob Agents Chemother. 2009;53(2):639–45.
42. Geetha VK, Yugendran T, Srinivasan R, Harish BN. Plasmid-mediated quinolone resistance in typhoidal Salmonellae: a preliminary report from South India. Indian J Med Microbiol. 2014;32(1):31–4.
43. Pribul BR, Festivo ML, Rodrigues MS, Costa RG, Rodrigues EC dos P, De Souza MMS, et al. Characteristics of quinolone resistance in Salmonella spp. isolates from the food chain in Brazil. Front Microbiol. 2017;8:299.
44. Rad M, Kooshan M, Mesgarani H. Quinolone resistance among Salmonella enterica and Escherichia coli of animal origin. Comp Clin Path. 2012;21(2):161–5.
45. Britto CD, Wong VK, Dougan G, Pollard AJ. A systematic review of antimicrobial resistance in Salmonella enterica serovar Typhi, the etiological agent of typhoid. PLoS Negl Trop Dis. 2018;12(10):e0006779.
46. Ranjbar R, Elhaghi P, Shokoohizadeh L. Multilocus sequence typing of the clinical isolates of Salmonella enterica serovar Typhimurium in Tehran Hospitals. Iran J Med Sci. 2017;42(5):443.
47. Sun J, Ke B, Huang Y, He D, Li X, Liang Z, et al. The molecular epidemiological characteristics and genetic diversity of Salmonella Typhimurium in Guangdong, China, 2007–2011. PLoS One. 2014;9(11):e113145.
48. Ke B, Sun J, He D, Li X, Liang Z, Ke C. Serovar distribution, antimicrobial resistance profiles, and PFGE typing of Salmonella enterica strains isolated from 2007–2012 in Guangdong, China. BMC Infect Dis. 2014;14(1):1–10.
49. Lee S, Park N, Yun S, Hur E, Song J, Lee H, et al. Presence of plasmid-mediated quinolone resistance (PMQR) genes in non-typhoidal Salmonella strains with reduced susceptibility to fluoroquinolones isolated from human salmonellosis in Gyeonggi-do, South Korea from 2016 to 2019. Gut Pathog. 2021;13(1):1–7.
50. Gymoese P, Sørensen G, Litrup E, Olsen JE, Nielsen EM, Torpdahl M. Investigation of outbreaks of Salmonella enterica serovar Typhimurium and its monophasic variants using whole-genome sequencing, Denmark. Emerg Infect Dis. 2017;23(10):1631.
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Mar 13, 2023
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Hani Hasan Jubair, Noor Abdul Ridha Al-Buhamrah, & Sabreen Ghanem Al-Fatlawi. (2023). Molecular characterization of quinolones resistant Salmonella typhi isolates from patients infected with Typhoid fever in Al-Najaf province, Iraq. Journal of Population Therapeutics and Clinical Pharmacology, 30(3), 11-19. https://doi.org/10.47750/jptcp.2023.30.03.002
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How to Cite
Hani Hasan Jubair, Noor Abdul Ridha Al-Buhamrah, & Sabreen Ghanem Al-Fatlawi. (2023). Molecular characterization of quinolones resistant Salmonella typhi isolates from patients infected with Typhoid fever in Al-Najaf province, Iraq. Journal of Population Therapeutics and Clinical Pharmacology, 30(3), 11-19. https://doi.org/10.47750/jptcp.2023.30.03.002