Poultry slaughterhouse wastewater as reservoirs for spreading extended-spectrum beta-lactamase-producing Escherichia coli in Abakaliki, Nigeria
##plugins.themes.bootstrap3.article.sidebar##
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution-NonCommercial-ShareAlike 4.0 International License.
##plugins.themes.bootstrap3.article.main##
Abstract
Abstract. Ugbo EN, Jacob JI, Effendi MH, Witaningrum AM, Agumah BN, Ugbo AI, Moses BI. 2023. Poultry slaughterhouse wastewater as reservoirs for spreading extended-spectrum beta-lactamase-producing Escherichia coli in Abakaliki, Nigeria. Biodiversitas 24: 4960-4966. The emergence of antimicrobial and multi-resistance extended-spectrum beta-lactamase-producing organisms (ESBL) from the environment and hospitals is a serious global health concern. This research focused on the role of poultry slaughterhouse wastewater as a reservoir for spreading extended-spectrum beta-lactamase-producing Escherichia coli. Exactly 110 poultry slaughterhouses wastewater was collected using sterile universal containers from abattoirs in Abakaliki. The samples were analyzed microbiological for the presence of E. coli using standard techniques. The E. coli isolates found were subjected to a sensitivity test to antibiotics using the Kirby-Bauer disc diffusion method and further tested for ESBL-producing E. coli using a double disc synergy test and chromogenic media Brilliance ESBL agar. Of 110 wastewater samples analyzed, 55 (50.0%) were positive for E. coli contamination. The E. coli isolates showed antibiotic resistance ranging between 21.8% (amoxicillin clavulanic acid) to 69.1% (tetracycline), and good susceptibility was observed on cefepime (72.7%). Thus, among 55 E. coli isolates, 11(20.0%) were ESBL-producing E. coli with resistance patterns as follows: TET-STX-CAZ-CTX-FEP (four isolates); TET-STX-CAZ-CTX (four isolates); TET-STX-CAZ-CTX-FEP-CRO (three isolates), and average multidrug resistance index of 0.7. This study revealed that poultry slaughterhouse wastewater was a reservoir for multidrug resistance ESBL-producing E. coli. Therefore, properly treating wastewater from poultry production or farms before disposing into the drainage channel or water bodies is highly recommended to avoid spreading ESBL-producing organisms from animal waste products to humans and their environment.
##plugins.themes.bootstrap3.article.details##
References
Adebowale O, Adeyemo OK, Awoyomi O. 2016. Antibiotic use and practices in commercial poultry laying hens in Ogun state Nigeria. Revue delevage et de medicine veterinaire des pays Tropicaux 69:41-44.
Agyare C, Etsiapa-Boamah V, Ngofi ZC, Osei FB. 2019. Antibiotic Use in Poultry Production and Its Effects on Bacterial Resistance : Antimicrobial resistance - A global threat. Intech open 2:5-9. DOI: 10.5772/intechopen.79371
Ansharieta R, Ramandinianto SC, Effendi MH, Plumeriastuti H. 2021. Molecular identification of bla CTX-M and bla TEM genes encoding extended-spectrum ß-lactamase (ESBL) producing Escherichia coliisolated from raw cow’s milk in East Java, Indonesia. Biodiversitas 22(4): 1600-1605. DOI: 10.13057/biodiv/d220402.
Aworh MK, Kwaga J, Okolocha E, Lyndy H, Dawn H, Rene SH. 2020. Extended-spectrum ß-lactamase-producing Escherichia coli among humans, chickens and poultry environments in Abuja, Nigeria.One Health Outlook 2 (8): 2- 11.https://doi.org/10.1186/s42522-020-00014-7
Barrera S,Cardenas P, Jay P. 2019.Changes in dominant Escherichia coli and antimicrobial resistance after 24 hr in fecal matter. Microbiology Open 8:e643 https://doi.org/10.1002/mbo3.643
Benameur Q, Tali-Maamar H, Assaous F Guettou B, Kheira R , Meriem-Hind B. 2019. Detection of multidrug resistant Escherichia coli in the ovaries of healthy broilers breeders with emphasis on extended spectrum beta-lactamases producers. Comparative Immunology, Microbiology and Infectious Disease 64:163-167. DOI: 10.1016/j.cimid.2019.03.009
Clinical and Laboratory Standards Institute. 2020. Performance standards for antimicrobial susceptibility testing; Twenty-second informational supplement; M100-S22. Clinical and Laboratory Standards Institute, Wayne, PA. http://www.clsi.org/source/orders/free/m100-s22.pdf
Cooreman-Algoed M, Boone L, Taelman SE. 2022. Impact of consumer behavior on the environmental sustainability profile of food production and consumption chains. Resources, Conservative and Resources Journal 64:178–184. DOI: 10.1016/j.resconrec.2021.106089
Cyoia PS, Koga VL, Nishio EK. 2019. Distribution of ExPEC virulence factors, blaCTX-M, fos A3, and mcr-1 in Escherichia coli isolated from commercialized chicken carcasses. Front. Microbiol 9, 3254. DOI:10.3389/fmicb.2018.03254
Effendi MH, Tyasningsih W, Yurianti YA, Rahmahani J, Harijani N, Plumeriastuti H.2021.Presence of multidrug resistance (MDR) and extended -spectrum beta-lactamase (ESBL) of Escherichia coli isolated from cloacal swabs of broilers in several wet markets in Surabaya, Indonesia. Biodiversitas 22 (1): 304-310. DOI: 10.13057/biodiv/d220137
Falgenhauer L, Imirzalioglu C, Oppong K, Akenten CW, Hogan B. 2019. Detection and characterization of ESBL-producing Escherichia coli from humans and poultry in Ghana. Frontiers in Microbiology 9:88-87. DOI:10.3389/fmicb.2018.03358
Gomi R, Matsuda T, Matsumura Y. 2017. Whole-genome analysis of antimicrobial-resistant and Extraintestinal pathogenic Escherichia coli in river water. Applied and Environmental Microbiology 83(5):2703–16. DOI: 10.1128/AEM.02703-16
Gupta SK, Padmanabhan BR, Diene SM, Lopez-Rojas R, Kempf M, Landraud L. 2021. Antimicrobial Resistant Gene-annotation,a new bioinformatic tool to discover antibiotic resistance genes in bacterial genomes. Antimicrobial Agents and Chemotherapy 58:212–20. DOI: 10.1128/AAC.01310-13
Gundran RS, Cardenio PA, Villanueva MA, Sison FB, Benigno CC, Kreausukon K, Pichpol D, Punyapornwithaya V. 2019. Prevalence and distribution of blaCTX-M, blaSHV, blaTEM genes in extended- spectrum _- lactamase-producing E. coli isolates from broiler farms in the Philippines. BMC Vet. Res. 15, 227. DOI: 10.1186/s12917-019-1975-9
Homeier-Bachmann T, Heiden SE, Lübcke PK, Bachmann L, Bohnert JA, Zimmermann D, Schaufler K. 2021. Antibiotic-Resistant Enterobacteriaceae in Wastewater of Abattoirs. Antibiotics 10: 568. DOI:10.3390/ antibiotics10050568
Hussain A, Shaik S, Ranjan A, Suresh A, Sarker N, Semmler T. 2019. Genomic and functional characterization of poultry Escherichia coli from India revealed diverse extended-Spectrum ?-lactamase-producing lineages with shared virulence profiles. Frontiers in Microbiology 10:2-6. DOI:10.3389/fmicb.2019.02766
Iliya D, Kwoji J, Athanda M, Nubwa D. 2019. Extended-spectrum beta-lactamase-producing Escherichia coli in chickens from small-scale (backyard) poultry farms in Maiduguri, Nigeria. International Journal of One Health 5: 26-30. DOI: 10.14202/IJOH.2019.26-30
Ieva B, Georgia K, Elena AA, Miguel P, Avelino A. 2020. Extended Spectrum ?-Lactamase (ESBL) Producing Escherichia coli in Pigs and Pork Meat in the European Union. Antibiotics 9; 678; DOI:10.3390/antibiotics9100678.
Kalakuntla S, Nagireddy NK, Panda AK, Jatoth N, Thirunahari R, Vangoor RR. 2017. Effect of dietary incorporation of n-3 PUFA polyunsaturated fatty acids rich oil sources or fatty acid profile, keeping quality and sensory attributes of broiler chicken meat. Animal Nutrition 3(4):386-391. DOI: 10.1016/j.aninu.2017.08.001
Kim H, Kim YA, Seo YH, Lee H, Lee K. 2021. Prevalence and Molecular Epidemiology of Extended-Spectrum-beta-Lactamase (ESBL)-Producing Escherichia coli from Multiple Sectors of Poultry Industry in Korea. Antibiotics 10: 1050. DOI:10.3390/ antibiotics10091050
Mabel KA, Jacob K, Emmanuel O, Lyndy H. 2020. Extended spectrum ß-lactamase producing Escherichia coli among humans, chickens and poultry environments in Abuja, Nigeria. One Health Outlook 2:8-10. ) DOI:10.1186/s42522-020-00014-7
Meki BB, Hebib A, Qada B, 2020. Resistance to multiple first-line antibiotics among Escherichia coli from poultry in Western Algeria. Vet World 13(2): 290–295. doi: 10.14202/vetworld.2020.290-295
Nakayama T, Le-Thi H, Thanh PH, Minh DTN, Hoang ON, Hoai PH, Hase A. 2022. Abundance of colistin-resistant Escherichia coli habouring mcr-1 and extended spectrum beta-lactamase producing E.coli co-habouring with blaTEM isolates from chicken meat in Vietnam. Archives of Clinical Microbiology 204(2):1-9. DOI: 10.1007/s00203-021-02746-0
Nguyen VT, Jamrozy D, Matamoros S, Carrique-Mas JJ, Ho HM, Thai QH. 2019. Limited contribution of non-intensive chicken farming to ESBL-producing Escherichia coli colonization in humans in Vietnam: an epidemiological and genomic analysis. Journal of Antimicrobial Chemotherapy 74:561–70. DOI: 10.1093/jac/dky506
Oduro-Mensah D, Obeng-Nkrumah N, Bonney EY, Oduro-Mensah E, Twum- Danso K, Osei YD. 2016. Genetic characterization of TEM-type ESBLassociated antibacterial resistance in Enterobacteriaceae in a tertiary hospital in Ghana. Ann Clin Microbiol Antimicrob 15:29. DOI:10.1186/s12941-016-0144-2.
Oloso N, Fagbo S, Garbati M, Olonitola S, Awosanya E, Aworh M. 2018. Antimicrobial resistance in food animals and the environment in Nigeria: A review. International Journal of Environmental Research and Public Health 15:1284-1287.
Oluwasile B, Agbaje M, Ojo O, Dipeolu M. 2014. Antibiotic usage pattern in selected poultry farms in Ogun State. Sokoto Journal of Veterinary Science, 12:45-48. DOI:10.4314/sokjvs.v12i1.7
Putra AR, Effendi MH, Koesdarto S,Suwarno S, Tyasningsih W, Estoepangestie AT.2020. Detection of the extended-spectrum ?-lactamase produced by Escherichia coli from dairy cows by using the Vitek-2 method in Tulungagung regency, Indonesia. Iraqi J. Vet. Sci 34(1): 203-207.DOI: 10.33899/ijvs.2019.125707.1134
Rahmahani J, Salamah M, Tyasningsih W, Effendi MH. 2020. Antimicrobial Resistance Profile of Escherichia coli From Cloacal Swab of Domestic Chicken in Surabaya Traditional Market. Biochem. Cell. Arch 20 (1): 2993-2997.DOI: 10.35124/bca.2020.20. S1.2993
Riwu KHP, Effendi MH, Rantam FA. 2020. A review of extended-spectrum ?-Lactamase (ESBL)producing Klebsiella pneumoniae and Multidrug-Resistant (MDR) on companion animals. Syst Rev Pharm 11 (7): 270-277. DOI:10.31838/srp.2020.7.43
Savin M, Bierbaum G, Hammerl JA, Heinemann C, Parcina M, Sib E, Voigt A, Kreyenschmidt J. 2020. ESKAPE bacteria and extended-spectrum-?-lactamase-producing Escherichia coli isolated from wastewater and process water from German poultry slaughterhouses. Appl Environ Microbiol 86:e02748-19. DOI:10.1128/AEM .02748-19.
Savin M, Gabriele B, Judith K, Ricarda M S, Sib E, Schmoger S, Käsbohrer A, Andre JH. 2021. Clinically Relevant Escherichia coli Isolates from Process Waters and Wastewater of Poultry and Pig Slaughterhouses in Germany. Microorganisms 9(4): 698. DOI: 10.3390/microorganisms9040698
Saleem R, Ejaz H, Zafar SY. 2017. Phenotypic characterization of extended-spectrum-beta - lactamase producing E. coli from healthy individuals, patients, sewage sludge, cattle, chickens and raw meat. Journal of Clinical Microbiology 33:81–97. DOI: 10.12669/pjms.334.12647
Suetens C, Latour K, Karki T, Ricchizzi E, Kinross P, Moro ML, Jans B, Hopkins S, Hansen S, Lyytikainen O, Reilly J, Deptula A, Zingg W, Plachouras D. and Monnet DL. 2018. Prevalence of healthcare-associated infections, estimated incidence and composite antimicrobial resistance index in acute care hospitals and long-term care facilities. Results from two European point prevalence surveys, 2016 to 2017. Euro Surveill. 23(46):pii_1800516. DOI:10.2807/1560-7917.ES.2018.23.46.1800516.
Telli AE, Biçer Y, Telli N, Güngör C, Turkal G, Onmaz NE. 2022. Pathogenic Escherichia coli and Salmonella spp. in chicken rinse carcasses: Isolation and genotyping by ERIC-PCR. Pak Vet J, 42(4): 493- 498. DOI:10.29261/pakvetj/2022.049
Tyasningsih W, Ramandinianto SC, Ansharieta R, Witaningrum AM, Permatasari DA, Wardhana DK, Effendi MH, Ugbo EN. 2022. Prevalence and antibiotic resistance of Staphylococcus aureus and Escherichia coli isolated from raw milk in East Java, Indonesia. Veterinary World 15 (8): 2021-2028. DOI: 10.14202/vetworld.2022.2021-2028.
Ugbo EN, Anyamene CO, Moses IB, Iroha IR, Babalola OO, Ukpai EG, Chukwunwejim CR, Egbule CU, Emioye AA, Okata-Nwali OD, Igwe OF. 2020. Prevalence of blaTEM, blaSHV, and blaCTX-M genes among extended spectrum beta-lactamase-producing Escherichia coli and Klebsiella pneumoniae of clinical origin. Gene Reports Dec 1;21:100909. DOI:10.1016/j.genrep.2020.100909
Veenemans J, Overdevest IT, Snelders E, Willemsen I, Hendriks Y, Adesokan A. 2014. Next-generation sequencing for typing and detection of resistance genes: performance of a new commercial method during an outbreak of extended-spectrum-beta-lactamase-producing Escherichia coli. Journal of Clinical Microbiology 52:2454–60. DOI: 10.1128/JCM.00313-14.
Verburg I, Garcia-Cobos S, Leal LH, Waar K, Friedrich AW, Schmitt H. 2019. Abundance and Antimicrobial Resistance of Three Bacterial Species Along a Complete Wastewater Pathway. Microorganisms 7, 312. DOI: 10.3390/microorganisms7090312.
Widodo A, Effendi MH, Khairullah AR, 2020. Extended-spectrum beta-lactamase (ESBL)-producing Eschericia coli from livestock. Sys Rev Pharm11(7): 382-392. DOI: 10.31838/srp.2020.7.57
Widodo A, Lamid M, Effendi MH, Khailrullah AR, Kurniawan SC, Silaen OSM, Riwu KHP, Yustinasari LR, Afnani DA, Dameanti FNAEP, Ramandinianto SC. 2023. Antimicrobial resistance characteristics of multidrug resistance and extended spectrum beta-lactamase producing Escherichia coli from several dairy farms in Probolinggo, Indonesia. Biodiversitas 24 (1): 215-221. DOI: 10.13057/biodiv/d240126.
Yanestria SM, Dameanti FNAEP, Musayannah BG, Pratama JWA, Witaningrum AM, Effendi MH, Ugbo EN. 2022. Antibiotic resistance pattern of extended-spectrum ?-Lactamase (ESBL) producing Escherichia coliisolated from broiler farm environment in Pasuruan district, Indonesia. Biodiversitas 23: 4460-4465. DOI: 10.13057/biodiv/d230911.
Most read articles by the same author(s)
- AGUS WIDODO, MIRNI LAMID, MUSTOFA HELMI EFFENDI, ASWIN RAFIF KHAIRULLAH, KATTY HENDRIANA PRISCILIA RIWU, LITA RAKHMA YUSTINASARI, SHENDY CANADYA KURNIAWAN, ARIF NUR MUHAMMAD ANSORI, OTTO SAHA MARTUA SILAEN, FIDI NUR AINI EKA PUJI DAMEANTI, Antibiotic sensitivity profile of multidrug-resistant (MDR) Escherichia coli isolated from dairy cow's milk in Probolinggo, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 10 (2022)
- RYANKA EDILA, MUSTOFA HELMI EFFENDI, LUCIA TRI SUWANTI, HYUCK-KEUN KWON, ADITYA YUDHANA, APRIL HARI WARDHANA, ANISA ALHADA, A comprehensive study on the occurrence rate and morphology characteristics of the acanthocephalan parasite in Javan spitting cobra (Naja sputatrix) in Sidoarjo, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 2 (2024)
- AGUS WIDODO, MIRNI LAMID, MUSTOFA HELMI EFFENDI, WIWIEK TYASNINGSIH, WURLINA, MOHAMMAD ANAM AL-ARIF, DADIK RAHARJO, SOEHARSONO, ASWIN RAFIF KHAIRULLAH, KATTY HENDRIANA PRISCILIA RIWU, LITA RAKHMA YUSTINASARI, SHENDY CANADYA KURNIAWAN, OTTO SAHAT MARTUA SILAEN, MOSES IKECHUKWU BENJAMIN, DANIAH ASHRI AFNANI, Potential hazards of multidrug resistance Escherichia coli collected from wastewater on dairy farms in East Java, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 3 (2023)
- AGUS WIDODO, MIRNI LAMID, MUSTOFA HELMI EFFENDI, ASWIN RAFIF KHAILRULLAH, SHENDY CANADYA KURNIAWAN, OTTO SAHAT MARTUA SILAEN, KATTY HENDRIANA PRISCILIA RIWU, LITA RAKHMA YUSTINASARI, DANIAH ASHRI AFNANI, FIDI NUR AINI EKA PUJI DAMEANTI, SANCAKA CHASYER RAMANDINIANTO, Antimicrobial resistance characteristics of multidrug resistance and extended-spectrum beta-lactamase producing Escherichia coli from several dairy farms in Probolinggo, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 1 (2023)
- EMMANUEL NNABUIKE UGBO, MUSTOFA HELMI EFFENDI, ADIANA MUTAMSARI WITANINGRUM, WIWIEK TYASNINGSIH, BERNARD NNABUIFE AGUMAH, AGATHA IFUNANYA UGBO, CHARITY CHINYERE NNABUGWU, DIVINEGIFT OLUCHI OKATA-NWALI, Antimicrobial resistance pattern of Salmonella spp. isolated from poultry farms in Abakaliki, Nigeria , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 9 (2023)
- NNABUIFE BERNARD AGUMAH, MUSTOFA HELMI EFFENDI, ADIANA MUTAMSARI WITANINGRUM, WIWIEK TYASNINGSIH, EMMANUEL NNABUIKE UGBO, CHINEKWU SHERRIDAN NWAGWU, IFUNANYA AGATHA UGBO, Antimicrobial resistance in Campylobacter species isolated from commercially sold steak (beef) and raw cow milk in Abakaliki, Nigeria , Biodiversitas Journal of Biological Diversity: Vol. 25 No. 3 (2024)
- DANIAH ASHRI AFNANI, NURULLAH FATIH, MUSTOFA HELMI EFFENDI, WIWIEK TYASNINGSIH, ASWIN RAFIF KHAIRULLAH, SHENDY CANADYA KURNIAWAN, OTTO SAHAT MARTUA SILAEN, SANCAKA CHASYER RAMANDINIANTO, AGUS WIDODO, KATTY HENDRIANA PRISCILIA RIWU, Profile of Multidrug Resistance and Methicillin-Resistant Staphylococcus aureus (MRSA) isolated from cats in Surabaya, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 11 (2022)
- SHEILA MARTY YANESTRIA, FIDI NUR AINI EKA PUJI DAMEANTI, BETI GISTAWATI MUSAYANNAH, JUNIANTO WIKA ADI PRATAMA, ADIANA MUTAMSARI WITANINGRUM, MUSTOFA HELMI EFFENDI, EMMANUEL NNABUIKE UGBO, Antibiotic resistance pattern of Extended-Spectrum ?-Lactamase (ESBL) producing Escherichia coli isolated from broiler farm environment in Pasuruan district, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 23 No. 9 (2022)
- MARIANA FEBRILIANTI RESILINDA PUTRI, IRFAN ALIAS KENDEK, FRESHINTA JELLIA WIBISONO, MUSTOFA HELMI EFFENDI, DADIK RAHARDJO, WIWIEK TYASNINGSIH, EMMANUEL NNABUIKE UGBO, Molecular detection of iron gene on multidrug resistant avian fecal Escherichia coli isolated from broiler on traditional markets, Surabaya, Indonesia , Biodiversitas Journal of Biological Diversity: Vol. 24 No. 12 (2023)