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European Journal of Medical Research
Published in: European Journal of Medical Research 1/2023

Open Access 01-12-2023 | Imipenem | Research

Co-existence of extended-spectrum β-lactamases blaCTX-M-9 and blaCTX-M-15 genes in Salmonella species isolated from febrile and diarrhoeagenic patients in Lagos, Nigeria: a cross-sectional study

Authors: Christopher O. Fakorede, Kehinde O. Amisu, Morteza Saki, Kabiru O. Akinyemi

Published in: European Journal of Medical Research | Issue 1/2023

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Abstract

Background

Resistance to different antimicrobial classes by Salmonella species has generated a global public health concern. The spread of extended-spectrum β-lactamases (ESBLs) blaCTX gene variants is also increasing. This study aimed to investigate the antibiotic resistance and the carriage of blaCTX-M-9 and blaCTX-M-15 as well as the quinolone resistance gene (qnrB19) among Salmonella species from hospitalised patients in Lagos, Nigeria.

Methods

In this cross-sectional study from April 2021 to August 2021, a total of 508 samples were collected from hospitalised patients. The samples were subjected to standard microbiological investigation. All the isolates were identified using API 20E kits and real-time polymerase chain reaction (RT-PCR). The in vitro antibiotic susceptibility testing (AST) was investigated using the disk diffusion method. Detection of antibiotic resistance and virulence gene makers was conducted using RT-PCR.

Results

In total, 24 Salmonella species were identified. All the isolates were non-typhoidal Salmonella isolates. None of the isolates screened was S. Typhi and S. Paratyphi. Most of the isolates were susceptible to imipenem, ciprofloxacin, ofloxacin and gentamycin, while a high level of resistance to all cephalosporins, penicillin, and some carbapenems was observed. In total, 79.2% (19/24) of the Salmonella isolates harboured the blaCTX-M variant including 54.2% (13/24) blaCTX-M-9 and 12.5% (3/24) blaCTX-M-15, while co-habitation of blaCTX-M-9 and blaCTX-M-15 was observed in 12.5% (3/24) of the isolates, respectively. None of the isolates harboured quinolone-resistant qnrB19 gene and virulence gene stn. However, invA gene was present in 66.7% (16/24) of all isolates.

Conclusions

This study is considered the first report of blaCTX-M-9 and blaCTX-M-15 variants in Salmonella species in Nigeria. The continued existence of cefotaximase (CTX-M)-producing Salmonella within our environment calls for the prudent use of cephalosporins.
Literature
1.
Raymond M, Gibani MM, Day NPJ, Cheah PY. Typhoidal Salmonella human challenge studies: ethical and practical challenges and considerations for low-resource settings. Trials. 2019;20(2):704.CrossRef
2.
Borges KA, Furian TQ, Souza SN, Salle CTP, Moraes HLS, Nasimento VP. Antimicrobial resistance and molecular characterization of Salmonella enterica serotypes from poultry sources in Brazil. Braz J Poult Sci. 2019;21(1):1–8.CrossRef
3.
Keestra-Gounder AM, Tsolis RM, Baumler AJ. Now you see me, now you don’t: the interaction of Salmonella with innate immune receptors. Nat Rev Microbiol. 2019;13:206–16.CrossRef
4.
Abate D, Abate KH, Abay SM, Abbafati C, Abbasi N, GBD 2017 Disease and Injury Incidence and Prevalence Collaborators, et al. Global, regional, and national incidence, prevalence, and years lived with disability for 354 diseases and injuries for 195 countries and territories, 1990–2017: a systematic analysis for the Global Burden of Disease Study 2017. Lancet (London, England). 2018;392:1789–858.CrossRef
5.
Tack B, Vanaenrode J, Verbakel JY, Toelen J, Jacobs J. Invasive non-typhoidal Salmonella infections in sub-Saharan Africa: a systematic review on antimicrobial resistance and treatment. BMC Med. 2020;18:212.CrossRef
6.
7.
8.
Katiyo S, Muller-Pebody B, Minaji M, Powell D, Johnson AP, De Pinna E, Day M, Harris R, Godbole G. Epidemiology and outcomes of nontyphoidal Salmonella bacteremias from England, 2004 to 2015. J Clin Microbiol. 2019;57(1):e01189-e1218.CrossRef
9.
Ramachandran A, Shanthi M, Sekar U. Detection of blaCTX-M extended spectrum beta-lactamase producing Salmonella enterica serotype Typhi in a tertiary care centre. J Clin Diagn Res. 2017;11(9):DC21-24.
10.
Bialvaei AZ, Kafil HS, Asgharzadeh M, Aghazadeh M, Yousefi M. CTX-M extended-spectrum β-lactamase-producing Klebsiella spp, Salmonella spp, Shigella spp and Escherichia coli isolates in Iranian hospitals. Braz J Microbiol. 2016;47(3):706–11.CrossRef
11.
Simarro E, Navarro F, Ruiz J, Miró E, Gómez J, Mirelis B. Salmonella enterica Serovar Virchow with CTX-M-Like β-Lactamase in Spain. J Clin Micro. 2000;38(12):4676–8.CrossRef
12.
Jin Y. CTX-M-producing Salmonella spp in Hong Kong: an emerging problem. J Med Microbiol. 2006;55(9):1245–50.CrossRef
13.
Nagshetty K, Shilpa B, Patil S, Shivannavar C, Manjula N. An overview of extended spectrum beta lactamases and metallo beta lactamases. Adv Microbiol. 2021;11:37–62.CrossRef
14.
Saravanan M, Ramachandran B, Barabadi H. The prevalence and drug resistance pattern of extended spectrum β–lactamases (ESBLs) producing Enterobacteriaceae in Africa. Microb Pathog. 2018;114:180–92.CrossRef
15.
Akinyemi KO, Iwalokun BA, Alafe OO, Mudashiru SA, Fakorede CO. BlaCTX-M-I group extended spectrum beta lactamase-producing Salmonella Typhi from hospitalized patients in Lagos, Nigeria. Infect Drug Resist. 2015;8:99–106.CrossRef
16.
Akinyemi KO, Fakorede CO, Abegunrin RO, Ajoseh SO, Anjorin AA, Amisu KO, et al. Detection of invA and blaCTM-genes in Salmonella spp. isolated from febrile patients in Lagos hospitals in Nigeria. Ger J Microbiol. 2021;1(3):1–10.CrossRef
17.
Fortini D, Fashae K, Villa L, Feudi C, Garcıa-Fernandez A, Carattoli A. A novel plasmid carrying blaCTX-M-15 identified in commensal Escherichia coli from healthy pregnant women in Ibadan, Nigeria. J Glob Antimicrob Resist. 2015;3(1):9–12.CrossRef
18.
Fashae K, Engelmann I, Monecke S, Braun SD, Ehricht R. Molecular characterisation of extended spectrum ß-lactamase producing Escherichia coli in wild birds and cattle, Ibadan, Nigeria. BMC Vet Res. 2021;17:33.CrossRef
19.
Eguale T, Birungi J, Asrat D, et al. Genetic markers associated with resistance to beta-lactam and quinolone antimicrobials in non-typhoidal Salmonella isolates from humans and animals in central Ethiopia. Antimicrob Resist Infect Control. 2017;6:13.CrossRef
20.
Badr H, Reda RM, Hagag NM, Kamel E, Elnomrosy SM, Mansour AI, et al. Multidrug-resistant and genetic characterization of extended-spectrum beta-lactamase-producing E. coli recovered from chickens and humans in Egypt. Animals (Basel). 2022;12(3):346.CrossRef
21.
Moawad AA, Hotzel H, Hafez HM, Ramadan H, Tomaso H, Braun SD, et al. Occurrence, phenotypic and molecular characteristics of extended-spectrum beta-lactamase-producing Escherichia coli in healthy turkeys in Northern Egypt. Antibiotics. 2022;11(8):1075.CrossRef
22.
Smith S, Opere B, Fowora M, Aderohunmu A, Ibrahim R, Omonigbehin E, et al. Molecular characterization of Salmonella spp directly from snack and food commonly sold in Lagos, Nigeria. Southeast Asian J Trop Med. 2012;43:718–23.
23.
Clinical Laboratory Standard Institute (CLSI). Performance standards for antimicrobial susceptibility testing, 31th edn. Clinical and Laboratory Standards Institute, M100: PA, USA.2021.
24.
Novais A, Canton R, Valverde A, Machado E, Galán JC, Peixe L, et al. Dissemination and persistence of blaCTX-M-9 are linked to class 1 integrons containing CR1 associated with defective transposon derivatives from Tn402 located in early antibiotic resistance plasmids of IncHI2, IncP1-alpha, and IncFI groups. Antimicrob Agents Chemother. 2006;50(8):2741–50.CrossRef
25.
Weill F, Perrier-Gros-Claude J-D, Demartin M, Coignard S, Grimont PA. Characterization of extended-spectrum- β-lactamase (CTX-M-15)-producing strains of Salmonella enterica isolated in France and Senegal. FEMS Microbiol. 2004;238(2):353–8.
26.
Choudhury M, Borah P, Sarma HK, Barkalita LM, Deka NM, Hussain I, et al. Multiplex-PCR assay for detection of some major virulence genes of Salmonella enterica serovars from diverse sources. Curr Sci. 2016;111(7):1252–8.CrossRef
27.
Nagarajan AG, Karnam G, Lahiri A, Allam US, Chakravortty D. Reliable means of diagnosis and serovar determination of blood-borne Salmonella strains: quick PCR amplification of unique genomic loci by novel primer sets. J Clin Microbiol. 2009;47(8):2435–41.CrossRef
28.
Akinyemi KO, Ajoseh SO, Fakorede CO. A systemic review of literature on human Salmonella enterica serovars in Nigeria (1999–2018). J Infect Dev Ctries. 2021;15(9):1222–35.CrossRef
29.
Akinyemi KO, Ajoseh SO, Iwalokun BA, Oyefolu AOB, Fakorede CO, Abegunrin RO, et al. Antimicrobial resistance and plasmid profiles of Salmonella enterica serovars from different sources in Lagos. Nigeria Health. 2018;10:758–72.
30.
Akinyemi KO, Bamiro BS, Coker AO. Salmonellosis in Lagos, Nigeria: incidence of Plasmodium falciparum-associated co-infection, patterns of antimicrobial resistance, and the emergence of reduced susceptibility to fluoroquinolones. J Health Popul Nutr. 2007;25(3):351.
31.
Eguale T, Gebreyes WA, Asrat D, Alemayehu H, Gunn JS, Engidawork E. Non-typhoidal Salmonella serotypes, antimicrobial resistance and co-infection with parasites among patients with diarrhoea and other gastrointestinal complaints in Addis Ababa, Ethiopia. BMC Infect Dis. 2015;15:497.CrossRef
32.
Tosisa W, Mihret A, Ararsa A, Eguale T, Abebe T. Prevalence and antimicrobial susceptibility of Salmonella and Shigella species isolated from diarrheic children in Ambo town. BMC Pediatr. 2020;20:91.CrossRef
33.
Deksissa T, Gebremedhin Z. A cross sectional study of enteric fever among patients at Ambo hospital: prevalence, risk factors comparison of Widal test and stool culture antimicrobials susceptibility pattern of isolates. BMC Infect Dis. 2019;19:288.CrossRef
34.
Paton S, Nicolle L, Mwongera M, Kabiru P, Mirza N, Plummer F, Wamola I. Salmonella and Shigella Gastroenteritis at a Public Teaching Hospital in Nairobi. Kenya: Published online by Cambridge University Press; 2006.
35.
Kadry M, Nader SM, Dorgham SM, Kandil MM. Molecular diversity of the invA gene obtained from human and egg samples. Vet World. 2019;12(7):1033–8.CrossRef
36.
Ngogo FA, Joachim A, Abade AM, Rumisha SF, Mizinduko MM, Majigo MV. Factors associated with Salmonella infection in patients with gastrointestinal complaints seeking health care at a regional hospital in Southern Highland of Tanzania. BMC Infect Dis. 2020;20:135.CrossRef
37.
Wu X, Angkititrakul S, Richards LA, Pulsrikarn C, Khaengair S, Keosengthong A, et al. Risk of antimicrobial resistant non-typhoidal Salmonella during asymptomatic infection passage between pet dogs and their human caregivers in Khon Kaen, Thailand. Antibiotics (Basel). 2020;9:477.CrossRef
38.
Gong B, Li H, Feng Y, Zeng S, Zhuo Z, Luo J, Chen X, Li X. Prevalence, serotype distribution and antimicrobial resistance of non-typhoidal Salmonella in hospitalized patients in Conghua District of Guangzhou, China. Front Cell Infect Microbiol. 2022;12: 805384.CrossRef
39.
Obaro SK, Hassan-Hanga F, Olateju EK, Umoru D, Lawson L, Olanipekun G, et al. Salmonella bacteraemia among children in central and northwest Nigeria, 2008–2015. Clin Infect Dis. 2015;61(4):S325–31.CrossRef
40.
Liu YH, Zhang Y, Hu JQ. Clinical epidemiological characteristics of non-typhoid Salmonella infection in children in Guangzhou from 2016 to 2018. Guangdong Med J. 2021;42:936–9.
41.
Mascaro V, Pileggi C, Crinò M, Proroga YTR, Carullo MR, Graziani C, et al. Non-typhoidal Salmonella in Calabria, Italy: a laboratory and patient-based survey. BMJ Open. 2017;7: e017037.CrossRef
42.
Adamu U, Yusha’u M, Usman AD, Abdulhadi SK. Antibiotic resistance pattern of Salmonella species isolated from Typhoid patients in Jigawa state, Nigeria. Novel Res Microbiol J. 2020;4:696–703.CrossRef
43.
Igbinosa EO, Beshiru A, Igbinosa IH, Okoh AI. Antimicrobial resistance and genetic characterisation of Salmonella enterica from retail poultry meats in Benin City. Nigeria LWT. 2022;169: 114049.CrossRef
44.
Harakeh S, Yassine H, Gharios M, Barbour E, Hajjar S, El-Fadel M, et al. Isolation, molecular characterization and antimicrobial resistance patterns of Salmonella and Escherichia coli isolates from meat-based fast food in Lebanon. Sci Total Environ. 2005;341(1–3):33–44.CrossRef
45.
Bonkoungou IJ, Haukka K, Österblad M, Hakanen AJ, Traoré AS, Barro N, et al. Bacterial and viral aetiology of childhood diarrhoea in Ouagadougou. Burkina Faso BMC Pediatr. 2013;13:36.
46.
McEwen SA, Prescott JF, Boerlin P. Antibiotics and poultry—a comment. Can Vet J. 2010;51:561–2.
47.
M’ikanatha NM, Sandt CH, Localio AR, Tewari D, Rankin SC, Whichard JM, et al. Multidrug-resistant Salmonella isolates from retail chicken meat compared with human clinical isolates. Foodborne Pathog Dis. 2010;7:929–34.CrossRef
48.
Crump JA, Sjölund-Karlsson M, Gordon MA, Parry CM. Epidemiology, clinical presentation, laboratory diagnosis, antimicrobial resistance, and antimicrobial management of invasive Salmonella infections. Clin Microbiol Rev. 2015;28:901–37.CrossRef
49.
Palma E, Tilocca B, Roncada P. Antimicrobial resistance in veterinary medicine: an overview. Int J Mol Sci. 2020;21:1914.CrossRef
50.
Asfaw Ali D, Tadesse B, Ebabu A. Prevalence and antibiotic resistance pattern of Salmonella isolated from caecal contents of exotic chicken in Debre Zeit and Modjo. Ethiopia Int J Microbiol. 2020;2020:1910630.
51.
Polsfuss S, Bloemberg GV, Giger J, Meyer V, Böttger EC, Hombach M. Evaluation of a diagnostic flow chart for detection and confirmation of extended spectrum β-lactamases (ESBL) in Enterobacteriaceae. Clin Microbiol Infect. 2012;18(12):1194–204.CrossRef
52.
Tajbakhsh M, Avini MY, Alikhajeh J, Tajeddin E, Rahbar M, Eslami P, et al. Emergence of blaCTX-M-15, blaTEM-169 and blaPER-1 extended-spectrum β-lactamase genes among different Salmonella enterica serovars from human faecal samples. Infect Dis (Lond). 2016;48(7):550–6.CrossRef
53.
Ramatla T, Mileng K, Ndou R, Mphuti N, Syakalima M, Lekota KE, et al. Molecular detection of integrons, colistin and b-lactamase resistant genes in Salmonella enterica serovars Enteritidis and Typhimurium isolated from chickens and rats inhabiting poultry farms. Microorganisms. 2022;10:313.CrossRef
54.
Rotimi V, Jamal W, Pal T, Sovenned A, Albert M. Emergence of CTX-M-15 type extended-spectrum beta-lactamase producing Salmonella spp. in Kuwait and the United Arab Emirates. J Med Microbiol. 2008;57(7):881–6.CrossRef
55.
Fischer J, Rodrıguez I, Baumann B, Guiral E, Beutin L, Schroeter A, et al. blaCTX-M-15 carrying Escherichia coli and Salmonella isolates from livestock and food in Germany. J Antimicrob Chemother. 2014;69(11):2951–8.CrossRef
56.
Arlet G, Barrett TJ, Butaye P, Cloeckaert A, Mulvey MR, White DG. Salmonella resistant to extended-spectrum cephalosporin: prevalence and epidemiology. Microb Infect. 2006;8:1945–54.CrossRef
57.
Acheampong G, Owusu M, Owusu-Ofori A, Osei I, Sarpong N, Sylverken A, et al. Chromosomal and plasmid-mediated fluoroquinolone resistance in human Salmonella enterica infection in Ghana. BMC Infect Dis. 2019;19:898.CrossRef
58.
De Jong B, Ekdahl K. The comparative burden of salmonellosis in the European Union member states, associated and candidate countries. BMC Public Health. 2006;6:4.CrossRef
59.
Akinyemi KO, Iwalokun BA, Foli F, Oshodi K, Coker AO. Prevalence of multiple drug resistance and screening of enterotoxin (stn) gene in Salmonella enterica serovars from water sources in Lagos, Nigeria. Public Health. 2011;125:65–71.CrossRef
60.
Abou Elez R, Elsohaby I, El-Gazzar N, Tolba H, Abdelfatah EN, Abdellatif SS, et al. Antimicrobial resistance of Salmonella Enteritidis and Salmonella Typhimurium isolated from laying hens, table eggs, and humans with respect to antimicrobial activity of biosynthesized silver nanoparticles. Animals. 2021;11(12):3554.CrossRef
61.
Anejo-Okopi JA, Isa SE, Audu O, Fagbamila IO, Iornenge JC, Smith IS. Isolation and polymerase chain reaction detection of virulence invA gene in Salmonella spp. from poultry farms in Jos Nigeria. J Med Trop. 2016;18:98–102.CrossRef
62.
Sharma I, Das K. Detection of invA Gene in isolated Salmonella from marketed poultry meat by PCR assay. J Food Process Technol. 2016;7:564.CrossRef
Metadata
Title
Co-existence of extended-spectrum β-lactamases blaCTX-M-9 and blaCTX-M-15 genes in Salmonella species isolated from febrile and diarrhoeagenic patients in Lagos, Nigeria: a cross-sectional study
Authors
Christopher O. Fakorede
Kehinde O. Amisu
Morteza Saki
Kabiru O. Akinyemi
Publication date
01-12-2023
Publisher
BioMed Central
Published in
European Journal of Medical Research / Issue 1/2023
Electronic ISSN: 2047-783X
DOI
https://doi.org/10.1186/s40001-022-00960-0

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