Occurrence of β-Lactamase Enzyme Genes and Integrons in Antibiotic Resistant Escherichia coli Isolates from Pregnant Women with Asymptomatic Bacteriuria in Nairobi, Kenya
Asymptomatic bacteriuria (ASB) is the presence of bacteria in urine without apparent symptoms of urinary tract infections. Antibiotic treatment of asymptomatic bacteriuria in pregnant women is recommended to reduce the risks associated with urinary tract infection during pregnancy. However, antibiotic resistance affects the success of treatment leading to failure with adverse outcomes. The study was to investigate the presence of mobile antibiotic resistant factors in multidrug resistance E. coli isolates. Methods: This was a cross-sectional study involving 1020 women attending antenatal clinic in Nairobi County. The urine specimens were processed using standard methods for isolation and identification of bacteria in urine. The most common uropathogen, E. coli was tested for antimicrobial resistance, using polymerase chain reaction (PCR) to amplify beta-lactamase genes and integrase genes. Plasmid curing using ethidium bromide was performed on plasmid positive multidrug resistant isolates. Results: A total 219 of women tested positive for ASB, resulting to a prevalence of 21.5 % at 95% confidence level. A total of 85 positive samples were caused by Escherichia coli which was at 38.8%. E. coli isolates from this study had resistance to most antibiotics tested except for imipenem. The resistance ranged from 11.6% for gentamycin to 90.6% for ampicillin. PCR was used for amplification of mobile antibiotic resistant determinants and results indicated 21 isolates had integrons while 26 isolates yielded Beta-lactamase enzyme genes (OXA-1 (8)) and CTX-M (18). Conclusion: There was a significant ASB among pregnant women included in the study from the Nairobi county clinics. There is the presence of ESBLs genes and integrons in community-acquired E. coli infections.
References
[1]
Nicolle, L.E., Gupta, K., Bradley, S.F., Colgan, R., DeMuri, G.P., Drekonja, D., et al. (2019) Clinical Practice Guideline for the Management of Asymptomatic Bacteriuria: 2019 Update by the Infectious Diseases Society of America. ClinicalInfectiousDiseases, 68, e83-e110. https://doi.org/10.1093/cid/ciy1121
[2]
Galgano, M., Pellegrini, F., Catalano, E., Capozzi, L., Del Sambro, L., Sposato, A., et al. (2025) Acquired Bacterial Resistance to Antibiotics and Resistance Genes: From Past to Future. Antibiotics, 14, Article 222. https://doi.org/10.3390/antibiotics14030222
[3]
Pouwels, K.B., Freeman, R., Muller-Pebody, B., Rooney, G., Henderson, K.L., Robotham, J.V., et al. (2018) Association between Use of Different Antibiotics and Trimethoprim Resistance: Going Beyond the Obvious Crude Association. JournalofAntimicrobialChemotherapy, 73, 1700-1707. https://doi.org/10.1093/jac/dky031
[4]
Fang, L., Li, X., Li, L., Li, S., Liao, X., Sun, J., et al. (2016) Co-Spread of Metal and Antibiotic Resistance within ST3-IncHI2 Plasmids from E. coli Isolates of Food-Producing Animals. ScientificReports, 6, Article No. 25312. https://doi.org/10.1038/srep25312
[5]
Tokuda, M. and Shintani, M. (2024) Microbial Evolution through Horizontal Gene Transfer by Mobile Genetic Elements. MicrobialBiotechnology, 17, e14408. https://doi.org/10.1111/1751-7915.14408
[6]
Sundar, R.O. (2004) Introduction to Biostatistics and Research Methods Book. 5 TH. http://www.amazon.in/Introduction-Biostatistics-Research-Methods-Rao/dp/8120345207
[7]
CLSI (2023) Performance Standards for Antimicrobial Susceptibility Testing.
[8]
Bauer, A.W., Kirby, W.M.M., Sherris, J.C. and Turck, M. (1966) Antibiotic Susceptibility Testing by a Standardized Single Disk Method. AmericanJournalofClinicalPathology, 45, 493-496. https://doi.org/10.1093/ajcp/45.4_ts.493
[9]
Empel, J., Baraniak, A., Literacka, E., Mrówka, A., Fiett, J., Sadowy, E., et al. (2008) Molecular Survey of β-Lactamases Conferring Resistance to Newer β-Lactams in Enterobacteriaceae Isolates from Polish Hospitals. AntimicrobialAgentsandChemotherapy, 52, 2449-2454. https://doi.org/10.1128/aac.00043-08
[10]
Lim, K., Yasin, R., Yeo, C., Puthucheary, S. and Thong, K. (2009) Characterization of Multidrug Resistant ESBL-Producing Escherichia coli Isolates from Hospitals in Malaysia. BioMedResearchInternational, 2009, Article ID: 165637. https://doi.org/10.1155/2009/165637
[11]
Letchumanan, V., Yin, W., Lee, L. and Chan, K. (2015) Prevalence and Antimicrobial Susceptibility of Vibrio parahaemolyticus Isolated from Retail Shrimps in Malaysia. FrontiersinMicrobiology, 6, Article 33. https://doi.org/10.3389/fmicb.2015.00033
[12]
Machado, E., Cantón, R., Baquero, F., Galán, J., Rollán, A., Peixe, L., et al. (2005) Integron Content of Extended-Spectrum-β-Lactamase-Producing Escherichia coli Strains over 12 Years in a Single Hospital in Madrid, Spain. AntimicrobialAgentsandChemotherapy, 49, 1823-1829. https://doi.org/10.1128/aac.49.5.1823-1829.2005
[13]
Agarwal, A., Pandey, S., Maheshwari, U., Singh, M., Srivastava, J. and Bose, S. (2021) Prevalence of Asymptomatic Bacteriuria and Antimicrobial Resistance Profile among Pregnant Females in a Tertiary Care Hospital. IndianJournalofCommunityMedicine, 46, 469-473. https://doi.org/10.4103/ijcm.ijcm_792_20
[14]
Sheffield, J.S. and Cunningham, F.G. (2005) Urinary Tract Infection in Women. Obstetrics&Gynecology, 106, 1085-1092. https://doi.org/10.1097/01.aog.0000185257.52328.a2
[15]
Amiri, F.N., Rooshan, M.H., Ahmady, M.H. and Soliamani, M.J. (2009) Hygiene Practices and Sexual Activity Associated with Urinary Tract Infection in Pregnant Women. EasternMediterraneanHealthJournal, 15, 104-110. https://doi.org/10.26719/2009.15.1.104
[16]
Moyo, S.J., Aboud, S., Kasubi, M. and Maselle, S.Y. (2010) Bacterial Isolates and Drug Susceptibility Patterns of Urinary Tract Infection among Pregnant Women at Muhimbili National Hospital in Tanzania. Tanzania Journal of Health Research, 12, 236-236. https://doi.org/10.4314/thrb.v12i4.52997
[17]
Kariuki, S., Revathi, G., Corkill, J., Kiiru, J., Mwituria, J., Mirza, N., et al. (2007) Escherichia coli from Community-Acquired Urinary Tract Infections Resistant to Fluoroquinolones and Extended-Spectrum β-Lactams. TheJournalofInfectioninDevelopingCountries, 1, 257-262. https://doi.org/10.3855/jidc.361
[18]
Amábile-Cuevas, C.F. and Arredondo-García, J.L. (2008) High Resistance Prevalence Towards Ampicillin, Co-Trimoxazole and Ciprofloxacin, among Uropathogenic Escherichia coli Isolates in Mexico City. TheJournalofInfectioninDevelopingCountries, 2, 350-353. https://doi.org/10.3855/jidc.195
[19]
Gazouli, M., Tzelepi, E., Sidorenko, S.V. and Tzouvelekis, L.S. (1998) Sequence of the Gene Encoding a Plasmid-Mediated Cefotaxime-Hydrolyzing Class A β-Lactamase (CTX-M-4): Involvement of Serine 237 in Cephalosporin Hydrolysis. Antimicrobial Agents and Chemotherapy, 42, 1259-1262. https://doi.org/10.1128/AAC.42.5.1259
[20]
Kim, J.O., Yoo, I.Y., Yu, J.K., Kwon, J.A., Kim, S.Y. and Park, Y.-J. (2021) Predominance and Clonal Spread of CTX-M-15 in Cefotaxime-Resistant Klebsiella pneumoniae in Korea and Their Association with Plasmid-Mediated Quinolone Resistance Determinants. Journal of Infection and Chemotherapy, 27, 1186-1192. https://doi.org/10.1016/j.jiac.2021.03.014
[21]
Ugwu, M.C., Odimegwu, D.C., Ibezim, E.C., Esimone, C.O., et al. (2009) Antibiotic Resistance Patterns of Staphylococcus aureus Isolated from Nostrils of Healthy Human Subjects in a Southeastern Nigeria Locality. Macedonian Journal of Medical Sciences, 2, 294-300.
[22]
Prakash, D. and Saxena, R.S. (2013) Distribution and Antimicrobial Susceptibility Pattern of Bacterial Pathogens Causing Urinary Tract Infection in Urban Community of Meerut City, India. ISRNMicrobiology, 2013, Article ID: 749629. https://doi.org/10.1155/2013/749629
[23]
Gidamudi, S.S. and Salunke, G.V. (2016) Antibiotic Susceptibility of Bacterial Strains, with Special Reference to Escherichia coli Isolated from Urinary Tract Infections in Rural Maharashtra. AsianJournalofPharmaceuticalandClinicalResearch, 10, 202-205. https://doi.org/10.22159/ajpcr.2017.v10i1.14871
[24]
Hussein, A.I.A., Ahmed, A.M., Sato, M. and Shimamoto, T. (2009) Characterization of Integrons and Antimicrobial Resistance Genes in Clinical Isolates of Gram-Negative Bacteria from Palestinian Hospitals. MicrobiologyandImmunology, 53, 595-602. https://doi.org/10.1111/j.1348-0421.2009.00168.x
[25]
Goudarzi, M., Sabzehali, F., Zahra, T., Azad, M., Boromandi, S., Hashemi, A., et al. (2014) Prevalence of blaCTX-M Gene in Multi-Resistant Escherichia coli Isolated from Urinary Tract Infections, Tehran, Iran. Novelty in Biomedicine, 2, 107-113.
[26]
Barlow, M., Reik, R.A., Jacobs, S.D., Medina, M., Meyer, M.P., McGowan, J.E., et al. (2008) High Rate of Mobilization for blaCTX-Ms. EmergingInfectiousDiseases, 14, 423-428. https://doi.org/10.3201/eid1403.070405
[27]
Kiiru, J., Butaye, P., Goddeeris, B.M. and Kariuki, S. (2013) Analysis for Prevalence and Physical Linkages Amongst Integrons, ISEcp1, ISCR1, Tn21 and Tn7 Encountered in Escherichia coli Strains from Hospitalized and Non-Hospitalized Patients in Kenya during a 19-Year Period (1992-2011). BMCMicrobiology, 13, Article No. 109. https://doi.org/10.1186/1471-2180-13-109
[28]
Muriuki, C.W., Ogonda, L.A., Kyanya, C., Matano, D., Masakhwe, C., Odoyo, E., et al. (2022) Phenotypic and Genotypic Characteristics of Uropathogenic Escherichia coli Isolates from Kenya. MicrobialDrugResistance, 28, 31-38. https://doi.org/10.1089/mdr.2020.0432
[29]
Shropshire, W.C., Aitken, S.L., Pifer, R., Kim, J., Bhatti, M.M., Li, X., Kalia, A., Galloway-Peña, J., Sahasrabhojane, P., Arias, C.A., Greenberg, D.E., Hanson, B.M. and Shelburne, S.A. (2021) IS26-Mediated Amplification of blaOXA-1 and blaCTX-M-15 with Concurrent Outer Membrane Porin Disruption Associated with de Novo Carbapenem Resistance in a Recurrent Bacteraemia Cohort. Journal of Antimicrobial Chemotherapy, 76, 385-395. https://doi.org/10.1093/jac/dkaa447
[30]
Weldhagen, G.F., Poirel, L. and Nordmann, P. (2003) Ambler Class A Extended-Spectrum β-Lactamases in Pseudomonasaeruginosa: Novel Developments and Clinical Impact. AntimicrobialAgentsandChemotherapy, 47, 2385-2392. https://doi.org/10.1128/aac.47.8.2385-2392.2003
[31]
Bush, K., Jacoby, G.A. and Medeiros, A.A. (1995) A Functional Classification Scheme for β-Lactamases and Its Correlation with Molecular Structure. AntimicrobialAgentsandChemotherapy, 39, 1211-1233. https://doi.org/10.1128/aac.39.6.1211
[32]
Poirel, L., Walsh, T.R., Cuvillier, V. and Nordmann, P. (2011) Multiplex PCR for Detection of Acquired Carbapenemase Genes. DiagnosticMicrobiologyandInfectiousDisease, 70, 119-123. https://doi.org/10.1016/j.diagmicrobio.2010.12.002
[33]
Moubareck, C., Daoud, Z., Hakimé, N.I., Hamzé, M., Mangeney, N., Matta, H., et al. (2005) Countrywide Spread of Community-and Hospital-Acquired Extended-Spectrum β-Lactamase (CTX-M-15)-Producing Enterobacteriaceae in Lebanon. JournalofClinicalMicrobiology, 43, 3309-3313. https://doi.org/10.1128/jcm.43.7.3309-3313.2005
[34]
Al-Mayahie, S. and Al Kuriashy, J.J. (2016) Distribution of ESBLs among Escherichia coli Isolates from Outpatients with Recurrent UTIs and Their Antimicrobial Resistance. TheJournalofInfectioninDevelopingCountries, 10, 575-583. https://doi.org/10.3855/jidc.6661
[35]
Dziri, R., Klibi, N., Alonso, C.A., Jouini, A., Ben Said, L., Chairat, S., et al. (2016) Detection of CTX-M-15-Producing Escherichiacoli Isolates of Lineages ST131-B2 and ST167-A in Environmental Samples of a Tunisian Hospital. MicrobialDrugResistance, 22, 399-403. https://doi.org/10.1089/mdr.2015.0354
Farzana, R., Shamsuzzaman, S., Mamun, K. and Shears, P. (2013) Antimicrobial Susceptibility Pattern of Extended Spectrum β-Lactamase Producing Gram-Negative Bacteria Isolated from Wound and Urine in a Tertiary Care Hospital, Dhaka City, Bangladesh. The Southeast Asian Journal of Tropical Medicine and Public Health, 44, 96-103.
[38]
Pitout, J.D.D., Hossain, A. and Hanson, N.D. (2004) Phenotypic and Molecular Detection of CTX-M-β-Lactamases Produced by Escherichia coli and Klebsiella spp. JournalofClinicalMicrobiology, 42, 5715-5721. https://doi.org/10.1128/jcm.42.12.5715-5721.2004
[39]
Coque, T.M., Baquero, F. and Cantón, R. (2008) Increasing Prevalence of ESBL-Producing Enterobacteriaceae in Europe. Eurosurveillance, 13, 1-11. https://doi.org/10.2807/ese.13.47.19044-en
[40]
Chelangat, S., Ngugi, C., Song’oro, E. and Mwaniki, J.N. (2025) Prevalence of Uropathogenic E. coli, Antimicrobial Susceptibility Profiles and Carriage of Extended-Spectrum Beta-Lactamases Genes at Mama Lucy Hospital, Kenya. Global Journal of Health Sciences, 10, 14-37. https://doi.org/10.47604/gjhs.3153
[41]
Nairoukh, Y.R., Mahafzah, A.M., Irshaid, A. and Shehabi, A.A. (2018) Molecular Characterization of Multidrug Resistant Uropathogenic E. coli Isolates from Jordanian Patients. TheOpenMicrobiologyJournal, 12, 1-7. https://doi.org/10.2174/1874285801812010001
[42]
Mohamed, R., Mohmed, I. and Majeed, H. (2023) Curing of Resistant Pseudomonasaeruginosa by Ethidium Bromide. Bionatura, 8, 1-7.
[43]
Thabit, A., Abd El-Sabour, E., Nafie, A., El-Mokhtar, M. and Biomy, Y. (2020) Detection of Proteus Species in Diabetic Wounds and Their Antibiotic Resistance Profile Analysis. BulletinofPharmaceuticalSciences.Assiut, 43, 1-10. https://doi.org/10.21608/bfsa.2020.93523
[44]
Ozdemir, K. (2019) Curing the Drug Resistance Plasmid in E. Coli O157:H7. AppliedEcologyandEnvironmentalResearch, 17, 14715-14727. https://doi.org/10.15666/aeer/1706_1471514727
[45]
Fody, A.M., Bagre, T.S., Dembele, R., Boubou, L., Moussa, A., Sidikou, R., etal. (2023) Characterization of Class 1, 2 and 3 Integrons in Multidrug-Resistant Escherichia coli Isolated from Clinical Samples from Niamey, Niger. Journal of Microbiology and Antimicrobials, 15, 23-28.
[46]
Kargar, M., Mohammadalipour, Z., Doosti, A., Lorzadeh, S. and Japoni-Nejad, A. (2014) High Prevalence of Class 1 to 3 Integrons among Multidrug-Resistant Diarrheagenic Escherichia coli in Southwest of Iran. OsongPublicHealthandResearchPerspectives, 5, 193-198. https://doi.org/10.1016/j.phrp.2014.06.003
[47]
Çopur Çiçek, A., Sandalli, C., Budak, E.E., Yağmur, G., Çizmeci, Z., et al. (2016) Characterization of Class 1 and Class 2 Integron Gene Cassettes in Escherichia coli Strains Isolated from Urine Cultures: A Multicenter Study. MikrobiyolojiBulteni, 50, 175-185. https://doi.org/10.5578/mb.24228
[48]
Chang, C., Chang, Y., Chang, L., Chang, S. and Lee, T. (2000) Characterisation of Drug Resistance Gene Cassettes Associated with Class 1 Integrons in Clinical Isolates of Escherichia coli from Taiwan Region. JournalofMedicalMicrobiology, 49, 1097-1102. https://doi.org/10.1099/0022-1317-49-12-1097
[49]
Walsh, T.R. (2010) Emerging Carbapenemases: A Global Perspective. InternationalJournalofAntimicrobialAgents, 36, S8-S14. https://doi.org/10.1016/s0924-8579(10)70004-2
[50]
Razzaq, R., Sheraz, A., Mohsin, M., Bashir, A. and Haque, A. (2024) Integrons and Multidrug Resistance across Phylogenetic Groups of Clinical Isolates of Escherichiacoli. PakistanJournalofMedicalSciences, 40, 1190-1195. https://doi.org/10.12669/pjms.40.6.8886
[51]
Shariat, A. and Fathpoor, F. (2022) Prevalence of Class I, II and III Integrons in Uropathogenic Escherichia coli Strains Isolated from Patients with Urinary Tract Infection in Shiraz, Iran. JundishapurJournalofMedicalSciences, 21, 500-513. https://doi.org/10.32598/jsmj.21.4.2384
[52]
Onyeadi, D. and Agbagwa, O. (2019) Plasmid Curing in Multi-Drug Resistant Hospital and Community Uropathogenic Escherichiacoli. JournalofAppliedSciencesandEnvironmentalManagement, 23, 29-34. https://doi.org/10.4314/jasem.v23i1.4
[53]
Oliver, A., Weigel, L.M., Rasheed, J.K., McGowan, J.E., Raney, P. and Tenover, F.C. (2002) Mechanisms of Decreased Susceptibility to Cefpodoxime in Escherichiacoli. AntimicrobialAgentsandChemotherapy, 46, 3829-3836. https://doi.org/10.1128/aac.46.12.3829-3836.2002
[54]
Pagani, L., Dell’Amico, E., Migliavacca, R., D’Andrea, M.M., Giacobone, E., Amicosante, G., et al. (2003) Multiple CTX-M-Type Extended-Spectrum β-Lactamases in Nosocomial Isolates of Enterobacteriaceae from a Hospital in Northern Italy. JournalofClinicalMicrobiology, 41, 4264-4269. https://doi.org/10.1128/jcm.41.9.4264-4269.2003
