Fecal carriage of extended spectrum beta-lactamase and fluoroquinolone resistant gene in non-typhoidal Salmonella enterica isolates from food-producing animals and humans
Abstract
This study seeks to determine the feacal carriage of extended spectrum beta-lactamase and fluoroquinolone resistant non-typhoidal Salmonella enterica isolates from food-producing animals and humans. A total of three hundred (300) fecal samples were collected using sterile universal containers from food-producing animals namely (Chicken [100], Pig [100] and humans (100) from Onicha Local Government Area of Ebonyi State and analyzed for the presence of non-typhoidal Salmonella enterica using standard microbiological techniques. Phenotypic detection of extended-spectrum beta-lactamase (ESBL) were done by disc diffusion and Double Disk Synergy Test. Molecular characterization for ESBL and fluoroquinolone-resistant genes were done by PCR with specific primers. The result shows that non-typhoidal Salmonella species (NTS) accounted for 25 % and 17 % in poultry and pig fecal sample respectively while 60 % and 40% were phenotypic ESBL producers respectively. When compared statistically there is significant difference among isolates confirmed ESBL-positive (P˂ 0.05). Also, none of the 16 (58 %) NTS isolated from humans harbored ESBL phenotype. PCR analysis with β-lactam specific primer detected the presence of blaOXA 50 % and 50 %, blaSHV 36 %, and 64 %, blaTEM 43 % and 57 %, blaCTX-M 36 % and 64 % in poultry and pig respectively. Fluoroquinolone resistant gene QnrA was present in 0 and 100 % of poultry and pig respectively. QnrB was 40 % and 60 % in poultry and pig isolates respectively. QnrS was present in 64 % isolates of poultry and 13 % isolates in pig. The high prevalence of genes encoding beta-lactamases and fluoroquinolone resistance (TEM, SHV, CTX-M and OXA, (qnrA, qnrB and qnrS) were present more in poultry and pig than in humans and demonstrate a significant public health threat from consumption of food-producing animal harboring such pathogenic resistant genotype if not properly controlled.
Keywords: Extended spectrum beta-lactamase, Fluoroquinolone, non-typhoidal Salmonella enterica, feacal carriage
Keywords:
Extended spectrum beta-lactamase, Fluoroquinolone, non-typhoidal Salmonella enterica, feacal carriage
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References
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2. Majowicz SE, Musto J, Scallan E, Angulo FJ, Kirk M, O'Brien SJ, Jones TF, Fazil A, Hoekstra RM, Studies ICoEDBoI: The global burden of nontyphoidal Salmonella gastroenteritis, Clinical Infectious Disease, 2020; 50(6):882-889. https://doi.org/10.1086/650733 PMid:20158401
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4. Hendriksen RS, Vieira AR, Karlsmose S, Lo Fo Wong DM, Jensen AB, Wegener HC, Aarestrup FM. Global monitoring of Salmonella serovar distribution from the world health organization global foodborne infections network country data bank: results of quality assured laboratories from 2001 to 2007, Foodborne Pathogens and Disease, 2011; 8:887-900. https://doi.org/10.1089/fpd.2010.0787 PMid:21492021
5. Crump JA, Medalla FM, Joyce KW, Krueger AL, Hoekstra RM, Whichard JM, Barzilay EJ, Emerging Infections Program NARMS Working Group, 2011, Antimicrobial resistance among invasive nontyphoidal Salmonellaenterica isolates in the United States: National Antimicrobial Resistance Monitoring System, 1996 to 2007, Antimicrobial Agents and Chemotherapy, 2011; 55:1148-1154. https://doi.org/10.1128/AAC.01333-10 PMid:21199924 PMCid:PMC3067073
6. Jones TF, Ingram LA, Cieslak PR, Vugia DJ, Tobin-D'Angelo M, Hurd S, Medus C, Cronquist A, Angulo FJ, Salmonellosis outcomes differ substantially by serotype, Journal of Infectious Diseases, 2008; 198:109-114. https://doi.org/10.1086/588823 PMid:18462137
7. Fashae K, Ogunsola F, Aarestrup FM, Hendriksen RS, Antimicrobial susceptibility and serovars of Salmonella from chickens and humans in Ibadan, Nigeria, Journal of Infection in Developing Countries, 2010; 4:484-494 https://doi.org/10.3855/jidc.909 PMid:20818100
8. Lee HY, Su LH, Tsai MH, Kim SW, Chang HH, Jung SI, Park KH, Perera J, Carlos C, Tan BH, Kumarasinghe G, So T, Chongthaleong A, Hsueh PR, Liu JW, Song JH, Chiu CH, High rate of reduced susceptibility to ciprofloxacin and ceftriaxone among nontyphoid Salmonella clinical isolates in Asia, Antimicrobial Agents and Chemotherapy, 2009; 53:2696-2699. https://doi.org/10.1128/AAC.01297-08 PMid:19332677 PMCid:PMC2687261
9. Hohmann E L, Nontyphoidal Salmonellosis, Clinical Infectious Diseases, 2001; 32(2):263-9 https://doi.org/10.1086/318457 PMid:11170916
10. Braden CR, Salmonella enterica serotype Enteritidis and eggs: a national epidemic in the United States, Clinical Infectious Diseases, 2006; 43(4):512-517. https://doi.org/10.1086/505973 PMid:16838242
11. Heredia N, García S, Animals as sources of food-borne pathogens: A review. Animal Nutrition, 2018; 4(3):250-255. https://doi.org/10.1016/j.aninu.2018.04.006 PMid:30175252 PMCid:PMC6116329
12. Álvarez-Fernández E, Alonso-Calleja C, Garcia-Fernández C, Capita R, Prevalence and antimicrobial resistance of Salmonella serotypes isolated from poultry in Spain: comparison between 1993 and 2006, International Journal of Food Microbiology, 2012; 153(3):281-7 https://doi.org/10.1016/j.ijfoodmicro.2011.11.011 PMid:22208955
13. Smith, S, Braun S, Akintimehin F, Fesobi T, Bamidele M, Coker A, Monecke S, Ehricht R, Serogenotyping and antimicrobial susceptibility testing of Salmonella species isolated from retail meat samples in Lagos, Nigeria. Molecular and Cellular Probes, 2016; 30(4):189-194 https://doi.org/10.1016/j.mcp.2016.04.001 PMid:27133921
14. Agbaje M, Lettini AA, Ojo OE, Longo A, Marafin E, Antonello K, Dipeolu MA. Antimicrobial resistance profiles of Salmonella serovars isolated from dressed chicken meat at slaughter in Kaduna, Nigeria, Revue d'elevage et de medecine veterinaire des pays tropicaux, 2019; 72(4):1-8 https://doi.org/10.19182/remvt.31484
15. Ojo OE, Awosile B, Agbaje M, Sonibare AO, Oyekunle MA, Kasali OB, Quinolone resistance in bacterial isolates from chicken carcasses in Abeokuta, Nigeria: A retrospective study from 2005-2011, Nigerian Veterinary Journal, 2012; 33(2):483- 491.
16. Omoshaba EO, Olufemi FO, Ojo OE, Sonibare AO, Agbaje M, Multidrug-resistant Salmonellae isolated in Japanese quails reared in Abeokuta, Nigeria, Tropical Animal Health and Production, 2017; 49(7):1455-1460. https://doi.org/10.1007/s11250-017-1347-z PMid:28717851
17. Onyenwe NE, Nnamani ND, Okoro JC, Nwofor CN, Jesumirhewe C, Prevalence and gene sequencing of extended spectrum β-lactamases producing Salmonella enterica serovar. Typhi from South-East Nigeria, African Journal of Pharmacy and Pharmacology, 2020; 14(7):192-202 https://doi.org/10.5897/AJPP2020.5115
18. Joseph I S, Okolo I O, Udenweze E C, Nwankwo C E, Peter I U, Ogbonna I P, Iroha I R, Comparison of Antibiotic-Resistant Pattern of Extended Spectrum Beta-Lactamase and Carbapenem- Resistant Escherichia coli Isolates from Clinical and Non-Clinical Sources, Journal of Drug Delivery and Therapeutics, 2023; 13(7):107-118 https://doi.org/10.22270/jddt.v13i7.5918
19. Yhiler NY, Bassey BE, Paul I, Francis U M, Anne A, Okocha-Ejeko A, Antimicrobial resistance pattern in Salmonella enterica from clinical and poultry sources in Calabar, Nigeria, Journal of Microbiology and Antimicrobials, 2019; 11(2):5-10. https://doi.org/10.5897/JMA2019.0413
20. Sharma J, Sharma M, Ray P, Detection of TEM and amp; SHV genes in Escherichia coli and amp; Klebsiella pneumoniae Isolates in a Tertiary Care Hospital from India, Indian Journal of Medical Research, 2010; 132:332-336.
21. Eguale T, Birungi J, Asrat D, Njahira M N, Njuguna J, Gebreyes, G, Wondwossen, A, Gunn JS, Appolinaire-Djikeng, A, Engidawork E, Genetic markers associated with resistance to beta-lactam and quinolone antimicrobials in non-typhoidal Salmonella isolates from humans and animals in central Ethiopia, Antimicrobial Resistance and Infection Control, 2017; 6:13-14. https://doi.org/10.1186/s13756-017-0171-6 PMid:28105330 PMCid:PMC5240271
22. Dupouy V, Abdelli M, Moyano G, Arpaillange N, Bibbal D, Cadiergues, M. C, Prevalence of beta-lactam and quinolone/fluoroquinolone resistance in enterobacteriaceae from dogs in France and Spain: Characterization of ESBL/pAmpC isolates, genes and conjugative plasmids, Frontier in Veterinary Science, 2019; 6:279-281 https://doi.org/10.3389/fvets.2019.00279 PMid:31544108 PMCid:PMC6730528
23. Martínez-Martínez L, Pascual A, Jacoby GA, Quinolone resistance from a transferable plasmid, Lancet of Infectious Disease, 1998; 351:797-799, https://doi.org/10.1016/S0140-6736(97)07322-4 PMid:9519952
24. Jeong HS, Prevalence of plasmid-mediated quinolone resistance and its association with extended-spectrum beta-lactamase and AmpC beta-lactamase in Enterobacteriaceae, Korean Journal of Laboratory Medicine, 2011; 31:257-264 https://doi.org/10.3343/kjlm.2011.31.4.257 PMid:22016679 PMCid:PMC3190004
25. Newire E A, Ahmed S F, House B, Valiente E, Pimentel G, Detection of new SHV-12, SHV-5 and SHV-2a variants of extended spectrum beta-lactamase in Klebsiella pneumoniae in Egypt, Annal of Clinical Microbiology and Antimicrobial Agent, 2013; 12:16-340, https://doi.org/10.1186/1476-0711-12-16 PMid:23866018 PMCid:PMC3723734
26. Aasm¨ae B, H¨akkinen L, Kaart T, Kalmus P, Antimicrobial resistance of Escherichia coli and Enterococcus species isolated from Estonian cattle and swine from 2010 to 2015, Acta Veterinary Scandinavian, 2019; 61:5-34, https://doi.org/10.1186/s13028-019-0441-9 PMid:30665443 PMCid:PMC6341677
27. Ugbo EN, Anyamene CO, Moses IB, Iroha IR, Babalola OO, Ukpai EG, Chukwunwejim CR, Egbule CU, Emioye AA, Okata-Nwali OD, Igwe OF, Ugadu, IO, Prevalence of blaTEM, blaSHV, and blaCTX-M genes among extended spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae of clinical origin, Gene Report, 2020; 21:34-45. https://doi.org/10.1016/j.genrep.2020.100909
28. Iroha IR, Orji JO, Onwa NC, Nwuzo AC, Okonkwo EC, Ibiam EO, Nwachi AC, Afuikwa FN, Agah VM, Ejikeugwu EPC, Agumah NB, Moses IB, Ugbo E, Ukpai EG, Nwakaeze E A, Oke B, Ogbu L and Nwunna E, Microbiology practical handbook. (Editor; Ogbu. O), 1st Edition. Charlieteximage Africa (CiAfrica Press), 2019; 344.
29. Egwu, E, Ibiam FA, Moses IB, Iroha CS, Orji I, Okafor-Alu F N, Eze CO, Iroha IR, Antimicrobial susceptibility and molecular characteristics of beta-lactam- and fluoroquinolone-resistant E. coli from human clinical samples in Nigeria, Scientific African, 2023; 21:18-63. https://doi.org/10.1016/j.sciaf.2023.e01863
30. Ahmed AM, Motoi Y, Sato M, Maruyama A, Watanabe H, Fukumoto Y, Shimamoto T, Zoo animals as reservoirs of Gram-negative bacteria harboring integrons and antimicrobial resistance genes, Applied Environmental Microbiology, 2007; 73:6686-6690. https://doi.org/10.1128/AEM.01054-07 PMid:17720829 PMCid:PMC2075039
31. Robicsek A, Jacoby GA, Hooper DC, The Worldwide Emergence of Plasmid-mediated Quinolone Resistance, Lancet Infectious Disease, 2006; 6:629-640. https://doi.org/10.1016/S1473-3099(06)70599-0 PMid:17008172
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Nwosu UO, Ibiam FA, Amadi-Ibiam CO, Iroha CS, Edemekong CI, Peter IU, Iroha IR. Fecal carriage of extended spectrum beta-lactamase and fluoroquinolone resistant gene in non-typhoidal Salmonella enterica isolates from food-producing animals and humans. JDDT [Internet]. 15Sep.2023 [cited 2Oct.2023];13(9):128-3. Available from: https://jddtonline.info/index.php/jddt/article/view/5964
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