Antimicrobial Profiles of Selected Gram-Negative Bacteria Recoverable from Sewage and Sludge from Juja and Kibera Informal Settlements of the Larger Nairobi Metropolis

John Maina; Perpetual Ndung’u; Anne Muigai; Helen Onyango; Joel K. Mukaya; Susan Wambui; Terry Judah; Joyce Kinyua; Joystella Muriuki; Lynne Chesenge; Lydia Kisoo; Rebecca Thuku; Boniface Wachira; Vincent Bett; Thomas Gachuki; John Kiiru

doi:10.4236/aim.2019.96031

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Antimicrobial Profiles of Selected Gram-Negative Bacteria Recoverable from Sewage and Sludge from Juja and Kibera Informal Settlements of the Larger Nairobi Metropolis

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DOI: 10.4236/aim.2019.96031 295 Downloads 632 Views

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John Maina^1,2*, Perpetual Ndung’u¹, Anne Muigai¹, Helen Onyango¹, Joel K. Mukaya¹, Susan Wambui², Terry Judah², Joyce Kinyua¹, Joystella Muriuki¹, Lynne Chesenge¹, Lydia Kisoo¹, Rebecca Thuku¹, Boniface Wachira¹, Vincent Bett², Thomas Gachuki¹, John Kiiru^2*

Affiliation(s)

¹Jomo Kenyatta University of Agriculture and Technology, Juja, Kiambu County, Central Kenya, Kenya.
²Center for Microbiology Research, Kenya Medical Research, Nairobi, Kenya.

ABSTRACT

Africa has experienced rapid urban migration in the past two decades. New informal settlements continue to emerge and expand but the sanitation provision of facilities has not improved at the same pace and this poses a serious health concern to the public especially the urban poor. Open sewage systems and sludge-clogged drainage systems as well as soil contaminated with industrial and domestic wastes are possible sources of germs that probably cause clinical infections and epidemics. In this cross-sectional study, we recorded diverse genera of Gram-negative non-fastidious bacteria that included; Escherichia coli (23%), Klebsiella spp (21%), Enterobacter spp (19%), Citrobacter spp (10%), Pseudomonas aeruginosa (8%), Proteus spp (7%), Salmonella (3%), Yersinia spp (3%), Shigella spp (2%), Morganella morganii (2%), Edwardisella spp (1%), Hafnia spp (1%), Serratia marcesence (0.5%), and Acinetobacter baumannii (0.5%). Most of these isolates were resistant to ampicillin while imipenem and ciprofloxacin were the most effective antimicrobial agents. Resistance combination towards ampicillin, trimethoprim, sulfamethoxazole and streptomycin was also noted in recovered isolates (16%). An overall high antimicrobial resistance was recorded among isolates from slum as compared to those recovered from Juja, a middle-class settlement located at the edge of Nairobi metropolis. The prevalence of isolates with a combined resistance to 3^rd generation cephalosporins (cefotaxime, ceftriaxone and ceftazidime), gentamicin and ciprofloxacin was the highest among P. aeruginosa isolates (13%) but none of the Yersinia species and Edwardisella tarda exhibited this resistance. Carriage of bla_TEM (52%) was most prevalent in all bacteria species followed by bla_CTX-M (20%), bla_SHV (18%) while bla_OXA (17%) was the least common. The phylogeny analysis revealed significant genetic similarity among strains belonging to E. coli, K. pneumoniae, E. agglomerans and P. mirabilis strains but less relatedness was noted among strains belonging to C. freundii. Further analysis showed possible clonal expansion of E. agglomerans and K. pneumoniae within the environmental ecosystems.

KEYWORDS

Antimicrobial Resistance, Multiple-Drug Resistance (MDR), Extended Spectrum β-Lactamases (ESBL), Enterobacteriaceae, Sewage and Sludge

Conflicts of Interest

The authors declare no conflicts of interest regarding the publication of this paper.

Cite this paper

Maina, J. , Ndung’u, P. , Muigai, A. , Onyango, H. , Mukaya, J. , Wambui, S. , Judah, T. , Kinyua, J. , Muriuki, J. , Chesenge, L. , Kisoo, L. , Thuku, R. , Wachira, B. , Bett, V. , Gachuki, T. and Kiiru, J. (2019) Antimicrobial Profiles of Selected Gram-Negative Bacteria Recoverable from Sewage and Sludge from Juja and Kibera Informal Settlements of the Larger Nairobi Metropolis. Advances in Microbiology, 9, 507-524. doi: 10.4236/aim.2019.96031.

References

[1]	O’Neill, J. (2016) Tackling Drug-Resistant Infections Globally: Final Report and Recommendations. http://amr-review.org/sites/default/files/160525_Final%20paper_with%20cover.pdf

[2]	Picao, R.C., Cardoso, J.P., Campana, E.H., Nicoletti, A.G., Petrolini, F.V., Assis, D.M., et al. (2013) The Route of Antimicrobial Resistance from the Hospital Effluent to the Environment: Focus on the Occurrence of KPC-Producing Aeromonas spp. and Enterobacteriaceae in Sewage. Diagnostic Microbiology and Infectious Disease, 76, 80-85. https://doi.org/10.1016/j.diagmicrobio.2013.02.001

[3]	Fresia, P., Antelo, V., Salazar, C., Gimenez, M., D’Alessandro, B., Afshinnekoo, E., et al. (2019) Urban Metagenomics Uncover Antibiotic Resistance Reservoirs in Coastal Beach and Sewage Waters. Microbiome, 7, 35. https://doi.org/10.1186/s40168-019-0648-z

[4]	Novo, A., Andre, S., Viana, P., Nunes, O.C. and Manaia, C.M. (2013) Antibiotic Resistance, Antimicrobial Residues and Bacterial Community Composition in Urban Wastewater. Water Research, 47, 1875-1887. https://doi.org/10.1016/j.watres.2013.01.010

[5]	White, P.A., McIver, C.J. and Rawlinson, W.D. (2001) Integrons and Gene Cassettes in the Enterobacteriaceae. Antimicrobial Agents and Chemotherapy, 45, 2658-2661. https://doi.org/10.1128/AAC.45.9.2658-2661.2001

[6]	Sarmah, A.K., Meyer, M.T. and Boxall, A.B. (2006) A Global Perspective on the Use, Sales, Exposure Pathways, Occurrence, Fate and Effects of Veterinary Antibiotics (VAs) in the Environment. Chemosphere, 65, 725-759. https://doi.org/10.1016/j.chemosphere.2006.03.026

[7]	Wellington, E.M., Boxall, A.B., Cross, P., Feil, E.J., Gaze, W.H., Hawkey, P.M., et al. (2013) The Role of the Natural Environment in the Emergence of Antibiotic Resistance in Gram-Negative Bacteria. The Lancet Infectious Diseases, 13, 155-165. https://doi.org/10.1016/S1473-3099(12)70317-1

[8]	Cleary, D.W., Bishop, A.H., Zhang, L., Topp, E., Wellington, E.M. and Gaze, W.H. (2016) Long-Term Antibiotic Exposure in Soil Is Associated with Changes in Microbial Community Structure and Prevalence of Class 1 Integrons. FEMS Microbiology Ecology, 92, fiw159. https://doi.org/10.1093/femsec/fiw159

[9]	Okeke, I.N., Aboderin, O.A., Byarugaba, D.K., Ojo, K.K. and Opintan, J.A. (2007) Growing Problem of Multidrug-Resistant Enteric Pathogens in Africa. Emerging Infectious Diseases, 13, 1640-1646. https://doi.org/10.3201/eid1311.070674

[10]	Yong, D.C., Thompson, J.S. and Prytula, A. (1985) Rapid Microbiochemical Method for Presumptive Identification of Gastroenteritis-Associated Members of the Family Enterobacteriaceae. Journal of Clinical Microbiology, 21, 914-918.

[11]	El-Sokkary, M.M.A. and Abdelmegeed, E.S. (2015) Characterisation of Class 1 Integron among Escherichia coli Isolated from Mansoura University Hospitals in Egypt. Advances in Microbiology, 5, 269-277. https://doi.org/10.4236/aim.2015.54025

[12]	Hasman, H., Mevius, D., Veldman, K., Olesen, I. and Aarestrup, F.M. (2005) β-Lactamases among Extended-Spectrum β-Lactamase (ESBL)-Resistant Salmonella from Poultry, Poultry Products and Human Patients in The Netherlands. Journal of Antimicrobial Chemotherapy, 56, 115-121. https://doi.org/10.1093/jac/dki190

[13]	Mohapatra, B.R., Broersma, K. and Mazumder, A. (2007) Comparison of Five Rep-PCR Genomic Fingerprinting Methods for Differentiation of Fecal Escherichia coli from Humans, Poultry and Wild Birds. FEMS Microbiology Letters, 277, 98-106. https://doi.org/10.1111/j.1574-6968.2007.00948.x

[14]	Vaez, H., Moghim, S., Nasr, E.B. and Ghasemian, S.H. (2015) Clonal Relatedness among Imipenem-Resistant Pseudomonas aeruginosa Isolated from ICU-Hospitalized Patients. Critical Care Research and Practice, 2015, Article ID: 983207. https://doi.org/10.1155/2015/983207

[15]	Alirol, E., Getaz, L., Stoll, B., Chappuis, F. and Loutan, L. (2011) Urbanisation and Infectious Diseases in a Globalised World. The Lancet Infectious Diseases, 11, 131-141. https://doi.org/10.1016/S1473-3099(10)70223-1

[16]	Hutton, G. and Chase, C. (2017) Water Supply, Sanitation, and Hygiene. In: Disease Control Priorities, 3rd Edition (Volume 7): Injury Prevention and Environmental Health, The World Bank, Washington DC, 171-198. https://doi.org/10.1596/978-1-4648-0522-6_ch9

[17]	Akullian, A., Ng’eno, E., Matheson, A.I., Cosmas, L., Macharia, D., Fields, B., et al. (2015) Environmental Transmission of Typhoid Fever in an Urban Slum. PLOS Neglected Tropical Diseases, 9, e0004212. https://doi.org/10.1371/journal.pntd.0004212

[18]	Bonomo, R.A. and Szabo, D. (2006) Mechanisms of Multidrug Resistance in Acinetobacter Species and Pseudomonas aeruginosa. Clinical Infectious Diseases, 43, S49-S56. https://doi.org/10.1086/504477

[19]	Musyoki, A.M., Suleiman, M.A., Mbithi, J.N. and John, M. (2013) Water-Borne Bacterial Pathogens in Surface Waters of Nairobi River and Health Implication to Communities Downstream Athi River. Environmental Microbiology, 3, 4-10.

[20]	Christabel, M., Budambula, N., Kiiru, J. and Kariuki, S. (2012) Characterization of Antibiotic Resistance in Environmental Enteric Pathogens from Kibera Slum in Nairobi-Kenya. African Journal of Bacteriology Research, 4, 46-54. https://doi.org/10.5897/JBR12.008

[21]	Kummerer, K. (2009) Antibiotics in the Aquatic Environment—A Review—Part I. Chemosphere, 75, 417-434. https://doi.org/10.1016/j.chemosphere.2008.11.086

[22]	Manaia, C.M., Macedo, G., Fatta-Kassinos, D. and Nunes, O.C. (2016) Antibiotic Resistance in Urban Aquatic Environments: Can It Be Controlled? Applied Microbiology and Biotechnology, 100, 1543-1557. https://doi.org/10.1007/s00253-015-7202-0

[23]	Yan, Q., Gao, X., Chen, Y.-P., Peng, X.-Y., Zhang, Y.-X., Gan, X.-M., et al. (2014) Occurrence, Fate and Ecotoxicological Assessment of Pharmaceutically Active Compounds in Wastewater and Sludge from Wastewater Treatment Plants in Chongqing, the Three Gorges Reservoir Area. Science of the Total Environment, 470-471, 618-630. https://doi.org/10.1016/j.scitotenv.2013.09.032

[24]	Sarmah, A.K., Meyer, M.T. and Boxall, A.B. (2006) A Global Perspective on the Use, Sales, Exposure Pathways, Occurrence, Fate and Effects of Veterinary Antibiotics (VAs) in the Environment. Chemosphere, 65, 725-759. https://doi.org/10.1016/j.chemosphere.2006.03.026

[25]	Onyango, H.A., Ngugi, C., Maina, J. and Kiiru, J. (2018) Urinary Tract Infection among Pregnant Women at Pumwani Maternity Hospital, Nairobi, Kenya: Bacterial Etiologic Agents, Antimicrobial Susceptibility Profiles and Associated Risk Factors. Advances in Microbiology, 8, 175-187. https://doi.org/10.4236/aim.2018.83012

[26]	Kilivwa, Mukaya, J.S., Maina, J., Museve, B., Nyerere, A.K. and Kiiru, J. (2018) Antimicrobial Resistance Profile and Genetic Profiling of Pseudomonas aeruginosa Strains Obtained from Different Inpatient Wards at Kenyatta National Hospital. IOSR Journal of Pharmacy and Biological Sciences, 13, 1-9.

[27]	Malaho, C., Wawire, S.A. and Shivoga, W.A. (2018) Antimicrobial Resistance Patterns of Enterobacteriaceae Recovered from Wastewater, Sludge and Dumpsite Environments in Kakamega Town, Kenya. African Journal of Microbiology Research, 12, 673-680.

[28]	Spanu, T., Luzzaro, F., Perilli, M., Amicosante, G., Toniolo, A. and Fadda, G. (2002) Occurrence of Extended-Spectrum Beta-Lactamases in Members of the Family Enterobacteriaceae in Italy: Implications for Resistance to β-Lactams and Other Antimicrobial Drugs. Antimicrobial Agents and Chemotherapy, 46, 196-202. https://doi.org/10.1128/AAC.46.1.196-202.2002

[29]	Vounba, P., Arsenault, J., Bada-Alambedji, R. and Fairbrother, J.M. (2019) Pathogenic Potential and the Role of Clones and Plasmids in β-Lactamase-Producing E. coli from Chicken Faeces in Vietnam. BMC Veterinary Research, 15, 106. https://doi.org/10.1186/s12917-019-1849-1