The Antibiotic Resistance Profile of Escherichia coli from Selected Estuaries in the City of Manila, Philippines

Surface waters from estuaries were reported to disseminate antibiotic resistance (AR), particularly from faecal coliforms of human origin introduced via domestic wastewater and surface runoffs. Thus, this study aimed to determine the concentration and antimicrobial susceptibility profiles of Escherichia coli isolated from surface waters of selected estuaries in the City of Manila. From a total of 48 water samples collected from six estuaries over a two-month period, the estimated average concentration of E. coli and total coliform are 4.3 x 104 CFU/100 mL and 11.0 × 104 CFU/100 mL, respectively. Among the isolates, 14.6% were identified as multidrug-resistant, while 6.3% were classified as extended-spectrum β-lactamase producers. Moreover, 18.8% of the isolates had a multiple antibiotic resistance index of ≥0.2. The findings indicate that AR E. coli contamination likely originates from human excretions, including those from informal settlements and hospital patients treated with multiple antibiotics. This makes these estuaries unsuitable for beneficial use due to the potential risk of exposure to MDR/ ESBL E. coli and other faecal coliforms. Thus, urgent measures including law-enforced monitoring, management, rehabilitation, and education are necessary to curb faecal pollution and limit the spread of AR in these waters.
Abia, A.L.K., Ubomba-Jaswa, E. and M.N.B. Momba(2015). Impact of seasonal variation on Escherichia coli concentrations in the riverbed sediments in the Apies River, South Africa. Science of the Total Environment, 537: 462-469. https://doi.org/10.1016/j.scitotenv.2015.07.132 Alawi, M., Torrijos, T.V. and F. Walsh (2022). Plasmid- mediated antimicrobial resistance in drinking water. Environmental Advances, 8: 100191. https://doi. org/10.1016/j.envadv.2022.100191
Ancheta, A.A. (2021). Sustaining esturial creeks: Water corridors in mitigating flooding in Manila, Philippines.
IOP Conference Series: Earth and Environmental Science, 799(1): 012004. https://doi.org/10.1088/1755-1315/799/1/012004
ARSP (2023). Antimicrobial Resistance Surveillance Program Annual Report - 2022. In: Department of Health - Research Institute for Tropical Medicine. Available from: https://arsp.com.ph/publications/
Azuma, T., Uchiyama, T., Zhang, D., Usui, M. and T. Hayashi(2022). Distribution and characteristics of carbapenem- resistant and extended-spectrum β-lactamase (ESBL) producing Escherichia coli in hospital effluents, sewage treatment plants, and river water in an urban area of Japan. Science of the Total Environment, 839: 156232. https://doi. org/10.1016/j.scitotenv.2022.156232
Azzam, M.I., Ezzat, S.M., Othman, B.A. and K.A. El- Dougdoug (2017). Antibiotics resistance phenomenon and virulence ability in bacteria from water environment. Water Science, 31(2): 109-121. https://doi.org/10.1016/j. wsj.2017.10.001
Bringula, R.P., Canlas, R.L., Afable, J.M., Gajo, R., Santos, M.C. and A.A. Ancheta, (2015). How do people view the estuary and the technology management practices to rehabilitate it?: The case of Estero de Paco in Manila. In:Proceedings of 2014 2nd International Conference on Technology, Informatics, Management, Engineering and Environment, TIME-E 2014, pp. 128-134. https://doi. org/10.1109/TIME-E.2014.7011605
Chen, Z., Yu, D., He, S., Ye, H., Zhang, L., Wen, Y., Zhang, W., Shu, L. and S. Chen (2017). Prevalence of antibiotic- resistant Escherichia coli in drinking water sources in Hangzhou City. Frontiers in Microbiology, 8: 1-11. https:// doi.org/10.3389/fmicb.2017.01133
Clemente, E.D. (2020). Evaluating the water quality contribution of Estero de Paco to Pasig River and Manila Bay, Philippines. E3S Web of Conferences, 148: 1-7. https://doi.org/10.1051/e3sconf/202014807010
CLSI. (2021). M100 Performance Standards for Antimicrobial Susceptobility Testing (31st ed.). Clinical Laboratory Standards Institute.
DENR. (2015). DENR MC 2015-006 Guidelines for Recreational Waters Monitoring Program. Department of Environment and Natural Resources, Republic of the Philippines.
DENR. (2016). DENR AO 2016-08. Water Quality Guidelines and General Effluent Standards of 2016. Department of Environment and Natural Resources, Republic of the Philippines.
Diallo, O.O., Baron, S.A., Abat, C., Colson, P., Chaudet, H. and J.M. Rolain (2020). Antibiotic resistance surveillance systems: A review. Journal of Global Antimicrobial Resistance, 23: 430-438. https://doi.org/10.1016/j. jgar.2020.10.009
EPA. (2012). Recreational Water Quality Criteria. In: U. S. Environmental Protection Agency. Health and Ecological Criteria Division, Office of Science and Technology, United States (U.S.).
Fu, C., Xu, B., Chen, H., Zhao, X., Li, G., Zheng, Y., Qiu, W., Zheng, C., Duan, L. and W. Wang (2022). Occurrence and distribution of antibiotics in groundwater, surface water, and sediment in Xiong’an New Area, China, and their relationship with antibiotic resistance genes. Science of the Total Environment, 807: 151011. https://doi.org/10.1016/j. scitotenv.2021.151011
Garcia, B.C.B., Dimasupil, M.A.A.Z., Vital, P.G., Widmer, K.W. and W.L. Rivera (2015). Fecal contamination in irrigation water and microbial quality of vegetable primary production in urban farms of Metro Manila, Philippines.
Journal of Environmental Science and Health - Part B Pesticides, Food Contaminants, and Agricultural Wastes,
50(10): 734-743. https://doi.org/10.1080/03601234.201 5.1048107
Guidelines on recreational water quality. Volume 1: coastal and fresh waters. Geneva: (2021). In Geneva: World Health Organization. https://www.who.int/publications/i/ item/9789240031302
Ham, Y.S., Kobori, H., Kang, J.H., Matsuzaki, T., Iino, M. and H. Nomura (2012). Distribution of antibiotic resistance in urban watershed in Japan. Environmental Pollution,162: 98-103. https://doi.org/10.1016/j.envpol.2011.11.002
Henriot, C. P., Celle, H., Klaba, V., Biguenet, A., Miège, C., Daval, A., Amiotte-Suchet, P., Beugnot, J. C., Karbowiak, T. and X. Bertrand (2023). Effect of a karst system(France) on extended spectrum beta-lactamase (ESBL)- producing Escherichia coli. Water Research, 230: 119582. https://doi.org/10.1016/j.watres.2023.119582
Ho, J.Y., Jong, M.C., Acharya, K., Liew, S.S.X., Smith, D.R., Noor, Z.Z., Goodson, M.L., Werner, D., Graham, D.W. and J. Eswaran (2021). Multidrug-resistant bacteria and microbial communities in a river estuary with fragmented suburban waste management. Journal of Hazardous Materials, 405: 124687. https://doi.org/10.1016/j. jhazmat.2020.124687
Irfan, M., Almotiri, A. and Z.A. AlZeyadi (2022). Antimicrobial resistance and its drivers—A review. Antibiotics, 11(10):1132.https://doi.org/10.3390/antibiotics11101362
Jiang, X., Liu, L., Chen, J., Fan, X., Xie, S., Huang, J. and G. Yu (2021). Antibiotic resistance genes and mobile genetic elements in a rural river in Southeast China: Occurrence, seasonal variation and association with the antibiotics. Science of the Total Environment, 778: 146131. https:// doi.org/10.1016/j.scitotenv.2021.146131
Kumar, M., Ram, B., Sewwandi, H., Sulfikar, Honda, R. and T. Chaminda (2020). Treatment enhances the prevalence of antibiotic-resistant bacteria and antibiotic resistance genes in the wastewater of Sri Lanka, and India. Environmental Research, 183: 109179. https://doi.org/10.1016/j. envres.2020.109179
Larsson, D.G.J. and C.F. Flach (2022). Antibiotic resistance in the environment. Nature Reviews Microbiology, 20(5): 257-269. https://doi.org/10.1038/s41579-021-00649-x
Liang, X., Guan, F., Chen, B., Luo, P., Guo, C., Wu, G., Ye, Y., Zhou, Q. and H. Fang (2020). Spatial and seasonal variations of antibiotic resistance genes and antibiotics in the surface waters of Poyang Lake in China. Ecotoxicology and Environmental Safety, 196: 110543. https://doi. org/10.1016/j.ecoenv.2020.110543
Ma, C. Y., Ihara, M., Liu, S., Sugie, Y. and H. Tanaka (2022). Tracking the source of antibiotic-resistant Escherichia coli in the aquatic environment in Shiga, Japan, through whole- genome sequencing. Environmental Advances, 8: 100185. https://doi.org/10.1016/j.envadv.2022.100185
Morley, I. (2018). Manila. Cities, 72: 17-33. https://doi. org/10.1016/j.cities.2017.07.022
Palmares, A.J. and J. De los Reyes (2016). Diagnostic Microbiology Workbook (1st ed.). C&E Publishing, Inc.
Puljko, A., Milaković, M., Križanović, S., Kosić-Vukšić, J., Babić, I., Petrić, I., Maravić, A., Jelić, M. and N. Udiković-Kolić (2022). Prevalence of enteric opportunistic pathogens and extended-spectrum cephalosporin- and carbapenem-resistant coliforms and genes in wastewater from municipal wastewater treatment plants in Croatia. Journal of Hazardous Materials, 427: 128155. https://doi. org/10.1016/j.jhazmat.2021.128155
Quintela-Baluja, M., Abouelnaga, M., Romalde, J., Su, J.Q., Yu, Y., Gomez-Lopez, M., Smets, B., Zhu, Y.G., and D.W. Graham (2019). Spatial ecology of a wastewater network defines the antibiotic resistance genes in downstream receiving waters. Water Research, 162: 347-357. https:// doi.org/10.1016/j.watres.2019.06.075
Rousham, E.K., Unicomb, L. and M.A. Islam (2018). Human, animal and environmental contributors to antibiotic resistance in low-resource settings: Integrating behavioural, epidemiological and one health approaches. Proceedings of the Royal Society B: Biological Sciences, 285(1876):20180332. https://doi.org/10.1098/rspb.2018.0332
Şahin, S., Sivri, N., Akpinar, I., Çinçin, Z.B. and V.Z. Sönmez (2021). A comprehensive bibliometric overview: antibiotic resistance and Escherichia coli in natural water. Environmental Science and Pollution Research, 28(25): 32256-32263. https://doi.org/10.1007/s11356-021-14084-1
Sanderson, C.E., Fox, J.T., Dougherty, E.R., Cameron, A.D.S. and K.A. Alexander (2018). The changing face of water: A dynamic reflection of antibiotic resistance across landscapes. Frontiers in Microbiology, 9: 1894. https://doi. org/10.3389/fmicb.2018.01894
Sharahi, J.Y., Hashemi, A., Ardebili, A. and S. Davoudabadi (2021). Molecular characteristics of antibiotic-resistant Escherichia coli and Klebsiella pneumoniae strains isolated from hospitalized patients in Tehran, Iran. Annals of Clinical Microbiology and Antimicrobials, 20: 32. https://doi.org/10.1186/s12941-021-00437-8
Stocker, M.D., Smith, J.E., Hernandez, C., Macarisin, D. and Y. Pachepsky (2019). Seasonality of E. coli and Enterococci concentrations in creek water, sediment, and periphyton. Water, Air, and Soil Pollution, 230(9): 1-12. https://doi.org/10.1007/s11270-019-4263-1
Thaden, J.T., Li, Y., Ruffin, F., Maskarinec, S.A., Hill-Rorie, J.M., Wanda, L.C., Reed, S.D. and V.G. Fowler (2017). Increased costs associated with bloodstream infections caused by multidrug-resistant gram-negative bacteria are due primarily to patients with hospital-acquired infections. Antimicrobial Agents and Chemotherapy, 61(3): e01709-16. https://doi.org/10.1128/AAC.01709-16
Titilawo, Y., Sibanda, T., Obi, L. and A. Okoh (2015). Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of faecal contamination of water. Environmental Science and Pollution Research,
22(14): 10969-10980. https://doi.org/10.1007/s11356-014-3887-3
Turolla, A., Cattaneo, M., Marazzi, F., Mezzanotte, V. and M. Antonelli (2018). Antibiotic resistant bacteria in urban sewage: Role of full-scale wastewater treatment plants on environmental spreading. Chemosphere, 191: 761-769. https://doi.org/10.1016/j.chemosphere.2017.10.099
Wang, Z., Han, M., Li, E., Liu, X., Wei, H., Yang, C., Lu, S. and K. Ning (2020). Distribution of antibiotic resistance genes in an agriculturally disturbed lake in China: Their links with microbial communities, antibiotics, and water quality. Journal of Hazardous Materials, 393: 122426. https://doi.org/10.1016/j.jhazmat.2020.122426
Zhang, H., Wang, Y., Liu, P., Sun, Y., Dong, X. and X. Hu(2022). Unveiling the occurrence, hosts and mobility potential of antibiotic resistance genes in the deep ocean. Science of the Total Environment, 816: 151539. https:// doi.org/10.1016/j.scitotenv.2021.151539
Zheng, D., Yin, G., Liu, M., Chen, C., Jiang, Y., Hou, L. and Y. Zheng (2021). A systematic review of antibiotics and antibiotic resistance genes in estuarine and coastal environments. Science of the Total Environment, 777:146009https://doi.org/10.1016/j.scitotenv.2021.146009