Non-typhoidal Salmonella blood stream infection in Kuwait: Clinical and microbiological characteristics
Affiliations
Affiliations
- Department of Microbiology, Faculty of Medicine, Kuwait University, Jabriya, Kuwait.
- Microbiological Diagnostic Unit, Public Health Laboratory, Peter Doherty Institute for Infection and Immunity, The University of Melbourne, Victoria, Australia.
- Microbiology Unit, Department of Laboratories, Al Farwaniya Hospital, Sabah Al-Nasser, Kuwait.
- National Institute of Infectious Diseases, Tokyo, Japan.
- Department of Microbiology, Al Amiri Hospital, Sharq, Kuwait.
- Microbiology Unit, Muabarak Al Kabeer Hospital, Jabriya, Kuwait, and.
- Department of Medicine, University of Fribourg, Switzerland.
Abstract
Non-typhoidal Salmonella (NTS) bacteremia is a significant cause of morbidity and mortality worldwide. It is considered to be an emerging and neglected tropical disease in Africa. We studied this in two tertiary hospitals-Al Farwaniya and Al Amiri-in Kuwait, a subtropical country, from April 2013-May 2016. NTS bacteremia was present in 30 of 53,860 (0.75%) and 31 of 290,36 (1.33%) blood cultures in the two hospitals respectively. In Al Farwaniya hospital, one-third of the patients were from some tropical developing countries of Asia. About 66% of all patients (40/61) had diarrhea, and of these, 65% had the corresponding blood serovar isolated from stool culture. A few patients had Salmonella cultured from urine. Patients were either young or old. Most of the patients had co-morbidities affecting the immune system. Two patients each died in both hospitals. The number of different serovars cultured in each hospital was 13, and most infections were due to S. Enteritidis (all sequence type [ST]) 11) and S. Typhimurium (all ST19) except in a subgroup of expatriate patients from tropical developing countries in Al Farwaniya hospital. About a quarter of the isolates were multidrug-resistant. Most patients were treated with a cephalosporin with or without other antibiotics. S. Enteritidis and S. Typhimurium isolates were typed by pulsed field-gel electrophoresis (PFGE) and a selected number of isolates were whole-genome sequenced. Up to four different clades were present by PFGE in either species. Whole-genome sequenced isolates showed antibiotic-resistance genes that showed phenotypic correlation, and in some cases, phenotypes showed absence of specific genes. Whole-genome sequenced isolates showed presence of genes that contributed to blood-stream infection. Phylogeny by core genome analysis showed a close relationship with S. Typhimurium and S. Enteritidis from other parts of the world. The uniqueness of our study included the finding of a low prevalence of infection, mortality and multidrug-resistance, a relatively high prevalence of gastrointestinal infection in patients, and the characterization of selected isolates of S. Typhimurium and S. Enteritidis serovars by whole-genome sequencing that shed light on phylogeny, virulence and resistance. Similarities with studies from developing countries especially Africa included infection in patients with co-morbidities affecting the immune system, predominance of S. Typhimurium and S. Enteritidis serovars and presence of drug-resistance in isolates.
Conflict of interest statement
No authors have competing interests.
Similar articles
Shahunja KM, Leung DT, Ahmed T, Bardhan PK, Ahmed D, Qadri F, Ryan ET, Chisti MJ.PLoS Negl Trop Dis. 2015 Sep 11;9(9):e0004066. doi: 10.1371/journal.pntd.0004066. eCollection 2015.PMID: 26361076 Free PMC article.
Hendriksen RS, Hyytia-Trees E, Pulsrikarn C, Pornruangwong S, Chaichana P, Svendsen CA, Ahmed R, Mikoleit M.BMC Microbiol. 2012 Jun 6;12:92. doi: 10.1186/1471-2180-12-92.PMID: 22672324 Free PMC article.
Falay D, Kuijpers LM, Phoba MF, De Boeck H, Lunguya O, Vakaniaki E, Bertrand S, Mattheus W, Ceyssens PJ, Vanhoof R, Devlieger H, Van Geet C, Verheyen E, Ngbonda D, Jacobs J.BMC Infect Dis. 2016 Jun 10;16:271. doi: 10.1186/s12879-016-1604-1.PMID: 27286886 Free PMC article.
Tapia MD, Tennant SM, Bornstein K, Onwuchekwa U, Tamboura B, Maiga A, Sylla MB, Sissoko S, Kourouma N, Toure A, Malle D, Livio S, Sow SO, Levine MM.Clin Infect Dis. 2015 Nov 1;61 Suppl 4(Suppl 4):S332-8. doi: 10.1093/cid/civ729.PMID: 26449949 Free PMC article. Review.
Oneko M, Kariuki S, Muturi-Kioi V, Otieno K, Otieno VO, Williamson JM, Folster J, Parsons MB, Slutsker L, Mahon BE, Hamel MJ.Clin Infect Dis. 2015 Nov 1;61 Suppl 4:S310-6. doi: 10.1093/cid/civ674.PMID: 26449946 Review.
Cited by
Gao F, Huang Z, Xiong Z, Zheng H, Deng Q, Zhong H, Zhu S, Long Y, Wang J.Front Pediatr. 2023 Mar 15;11:1077158. doi: 10.3389/fped.2023.1077158. eCollection 2023.PMID: 37009297 Free PMC article.
Ji HJ, Jang AY, Song JY, Ahn KB, Han SH, Bang SJ, Jung HK, Hur J, Seo HS.Front Immunol. 2022 Jul 11;13:931052. doi: 10.3389/fimmu.2022.931052. eCollection 2022.PMID: 35898510 Free PMC article.
Zhao J, Lu X, Tie A, Ngegba E, Wang L, Sun L, Liang Y, Abdulai MK, Bah S, Wang G, Dong X, Harding D, Kan B.Emerg Microbes Infect. 2022 Dec;11(1):1416-1424. doi: 10.1080/22221751.2022.2076612.PMID: 35537043 Free PMC article.
Marchello CS, Birkhold M, Crump JA; Vacc-iNTS consortium collaborators.Lancet Infect Dis. 2022 May;22(5):692-705. doi: 10.1016/S1473-3099(21)00615-0. Epub 2022 Feb 1.PMID: 35114140 Free PMC article.
Emerging Status of Multidrug-Resistant Bacteria and Fungi in the Arabian Peninsula.
Borgio JF, Rasdan AS, Sonbol B, Alhamid G, Almandil NB, AbdulAzeez S.Biology (Basel). 2021 Nov 6;10(11):1144. doi: 10.3390/biology10111144.PMID: 34827138 Free PMC article. Review.
References
-
- Sethi SK, Khuffash FA, Al-Nakib W. Microbial etiology of acute gastroenteritis in hospitalized children in Kuwait. Pediatr Infect Dis. 1989; 8: 593–597. - PubMed
-
- Kidgell C, Reichard U, Wain J, Linz B, Torydahl M, Dougan G, et al. Salmonella Typhi, the causative agent of typhoid fever, is approximately 50,000 years old. Infect Genet Evol. 2002; 2: 39–45. - PubMed
-
- Soumet C, Ermel G, Rose V, Rose N, Drouin P, Salvat G, et al. Identification by a multiplex PCR-based assay of Salmonella Typhimurium and Salmonella Enteritidis strains from environmental swabs of poultry houses. Lett Appl Microbiol. 1999; 29: 1–6. - PubMed
-
- Clinical and Laboratory Standards Institute (CLSI): M100-S26. Performance standards for antimicrobial susceptibility testing; 26th informational supplement. Wayne, PA: CLSI, 2016.
-
- Reller LB, Weinstein M, Jorgensen JH, Ferraro MJ. Antimicrobial susceptibility testing: a review of general principles and contemporary practices. Clin infect Dis. 2009; 49: 1749–1755. - PubMed
-
- Clinical and Laboratory Standards Institute. Performance standards for antimicrobial susceptibility testing; 25th informal supplement, Jan 2015, M100-S25, 35, no. 3, Wayne, PA, USA.
-
- Drieux L, Brossier F, Sougakoff W, Jarlier V. Phenotypic detection of extended-spectrum beta- lactamase production in Enterobacteriaceae: review and bench guide. Clin Microbiol Infect. 2008; 14(Suppl 1): 90–103. - PubMed
-
- Poirel L, Guibert M, Bellais S, Naas T, Nordmann P. Integron- and carbenicillinase-mediated reduced susceptibility to amoxicillin-clavulanic acid in isolates of multidrug-resistant Salmonella enterica serotype Typhimurium DT104 from French patients. Antimicrob Agents Chemother. 1999; 43: 1098–1104. - PMC - PubMed
-
- Coskun S, Altanlar N, Keyvan E. Detection of plasmid mediated AmpC beta-lactamases in clinical isolates of Escherichia coli and Klebsiella pneumoniae. Sch J App Med Sci. 2016; 4: 444–450.
-
- Karunakaran R, Tay ST, Rahim FF, Lim BB, Puthucheary SD. Molecular analysis of ciprofloxacin resistance among nontyphoidal Salmonella with reduced susceptibility to ciprofloxacin isolated from patients at a tertiary care hospital in Kuala Lumpur, Malaysia. Jpn J Infect Dis. 2014; 67: 157–162. - PubMed
-
- Delmani F-A, Jaran AS, Al Tarazi Y, Masaadeh H, Zaki O. Characterization of ampicillin resistant gene (blaTEM-1) isolated from Escherichia coli in northern Jordan. Asian J Biomed Pharmaceut Sci. 2017; 7: 11–15.
-
- Shahunja KM, Leung DT, Ahmed T, Bardhan PK, Ahmed D, Qadri F, et al. Factors associated with non typhoidal Salmonella bacteremia versus typhoidal Salmonella bacteremia in patients presenting for care in an urban diarrheal disease hospital in Bangladesh. PLoS Negl Trop Dis. 2015; 9: e0004066 10.1371/journal.pntd.0004066 - DOI - PMC - PubMed
-
- Nor Azizah A, Fadzilah MN, Mariam M, Anis Siham ZA, Ariza A, Noor Shafina MN, et al. Community acquired bacteremia in paediatrics: epidemiology, aetiology and patterns of antimicrobial resistance in a tertiary care centre, Malaysia. Med J Malaysia. 2016; 71:117–121. - PubMed
-
- Mahon BE, Fields PI. Invasive infections with nontyphoidal Salmonella in Sub-Saharan Africa. Microbiol Spectr. 2016; 4:0015–2016. - PubMed
-
- Tennant SM, MacLennan CA, Levine MM. Invasive nontyphoidal Salmonella disease in Africa: current status. Expert Rev in Anti Infect Ther. 2013; 11: 443–446. - PubMed
-
- Eibach D, Al-Emran HM, Dekker DM, Krumkamp R, Adu-Sarkodie Y, Espinoza MC, et al. The emergence of reduced ciprofloxacin susceptibility in Salmonella enterica causing bloodstream infections in rural Ghana. Clin Infect Dis. 2016; 62 (S1): S32–S36. - PubMed
-
- Wiksvo ME, Kambhampati A, Shioda K, Walsh KA, Bowen A. Outbreaks of acute gastroenteritis transmitted by person to person contact, environmental contamination, and unknown modes of Transmission-United States. MMWR. 2015; 64: 1–16. - PubMed
-
- Thenmozhi S, Moorthy K, Sureshkumar BT, Suresh M. Antibiotic resistance mechanism of ESBL producing Enterobacteriaceae in clinical field. Int J Pure App Biosci. 2014; 2: 207–226.
-
- Robin F, Delmas J, Schweitzer C, Bonnet R. Evaluation of Vitek-2 extended-spectrum beta-lactamase test against non-duplicate strains of Enterobacteriaceae producing a broad diversity of well-characterised beta-lactamases. Clin Microbiol Infect. 2008; 14: 148–154. 10.1111/j.1469-0691.2007.01893.x - DOI - PubMed
-
- Gordon MA, Graham SM, Walsh AL, Wilson L, Phiri A, Molyneux, et al. Epidemics of invasive Salmonella enterica serovar enteritidis and S. enterica serovar typhimurium infection associated with multidrug resistance among adults and children in Malawi. Clin Infect Dis. 2008; 46: 963–969. 10.1086/529146 - DOI - PubMed
-
- Lunguya O, Lejon V, Phoba M-F, Bertrand S, Vanhoof R, Glupczynski Y, et al. Antimicrobial resistance in invasive nontyphoid Salmonella from the Democratic Republic of the Congo: emergence of decreased fluoroquinolone susceptibility and extended-spectrum beta lactamases. PLos Negl Trop Dis. 2013; 7: 14. - PMC - PubMed
-
- Oneko M, Kariuki S, Muturi-Kioi V, Oteino K, Oteino VO, Williamson JM, et al. Emergence of community- acquired, multidrug-resistant invasive nontyphoidal Salmonella disease in rural Western Kenya, 2009–2013. Clin Infect Dis. 2015; 1: S310–S316. - PubMed
-
- Chang YC, Scaria J, Ibraham M, Doiphode S, Chang Y-F, Sultan A, et al. Distribution and factors associated with Salmonella enterica genotypes in a diverse population of humans and animals in Qatar using multi locus sequence typing (MLST). J Infect Pub Health. 2016; 9, 315–323. - PubMed
-
- Lan NPH, Phuong TLT, Huu HN, Le Thuy L, Mather AE, Park SE, et al. Invasive non- typhoidal Salmonella infections in Asia: Clinical observations, disease outcome and dominant serovars from an infectious disease hospital in Vietnam. PLOS Negl Trop Dis. 2016; 10(8): e0004857 10.1371/journal.pntd.0004857 - DOI - PMC - PubMed
-
- Gordon MA, Kaukwatira AMK, Mwafulirwa G, Walsh AL, Hopkins MJ, Parry CM, et al. Invasive non-typhoid salmonellae establish systemic intracellular infection in HIV-infected adults: an emerging disease pathogenesis. Cin Infect Dis. 2010; 50: 953–962. - PubMed