Comparison of Antibiotic-Resistant Pattern of Extended Spectrum Beta-Lactamase and Carbapenem-Resistant Escherichia Coli Isolates from Clinical and Non-Clinical Sources
Abstract
The increasing rate of antibiotic resistance among E. coli especially those mediated by extended spectrum beta-lactamases and carbapenem-resistant (CR) presents a major threat to public health and healthcare delivery globally. The aim of this research was to compare the antibiotic resistant pattern of extended spectrum beta-lactamase and carbapenem-resistant Escherichia coli isolates from clinical and non-clinical sources. A total of two hundred and fifteen (215) clinical and non-clinical samples were collected for the study. The collected samples were analysis using Standard Microbiological protocol for isolation and identification. Phenotypic detection of ESBL Production and carbapenem resistant was performed using Double Disk Synergy Test (DDST) and Modified Hodge Test (MHT) respectively. Antibiogram studies of ESBL producing and Carbapenem-resistant E. coli was determined using the Kirby–Bauer disk diffusion method. The result of isolation and characterization revealed higher occurrence rate of clinical isolates of E. coli 66.1 % over non-clinical sample 54.0%. Phenotypic ESBL screening of isolated E. coli revealed overall detection rate of 35(30.4 %) and 13(13.0 %) in clinical and non-clinical source respectively while overall detection rate of carbapenem resistant ESBL producers accounted 9.6 % and 8.0 % in clinical and non-clinical isolates respectively. The isolates exhibited high percentage of resistance to nitrofurantion 100 %, cefepime 100 % colistin 66.7 %, amikacin 50.0 % and also exhibit MDR with MARI value of ≥ 0.5. Comparison of antibiotic resistant pattern of carbapenem-resistant extended spectrum beta-lactamase producing E. coli isolates from clinical and non-clinical sources showed no statistical significant difference P-value < 0.05 but were 100 % susceptible to ciprofloxacin and gentamicin. The pattern of similar MDR portrayed by clinical and non-clinical isolate should not be overlooked due to its hyper-motility and virulence domination leading to possible AMR transfer to other bacterial organisms and also, appropriate measures such as pretreatment of animal excrement before being used as fertilizers and the quality of irrigation water, hospital effluent discharge need to be taken into consideration to prevent the spread of resistant determinant.
Keywords: Escherichia coli, Extended Spectrum Beta-Lactamase, Carbapenem-Resistant, clinical, non-clinical
Keywords:
Escherichia coli, Extended Spectrum Beta-Lactamase, Carbapenem-Resistant, clinical, non-clinicalDOI
https://doi.org/10.22270/jddt.v13i7.5918References
El-Shaer S, Abdel-Rhman SH, Barwa R, Hassan R, Genetic Characterization of Extended-spectrum β-Lactamase- and Carbapenemase-producing Escherichia coli Isolated from Egyptian Hospitals and Environments, Public Library of Science One, 2021; 16(7):255-219. https://doi.org/10.1371/journal.pone.0255219
Roussel C, Sivignon A, de Wiele T V, Blanquet-Diot S, Foodborne Enterotoxigenic Escherichia coli: from Gut Pathogenesis to New Preventive Strategies involving Probiotics. Future Microbiology, 2017; 12:73- 93. https://doi.org/10.2217/fmb-2016-0101
Clermont O, Christenson J K, Denamur E, Gordon DM, The Clermont Escherichia coli Phylo-typing Method Revisited: Improvement of Specificity and Detection of New Phylo-groups. Environmental Microbiology Report, 2013; 5(1):58-65. https://doi.org/10.1111/1758-2229.12019
Sabate M, Moreno E, Perez T, Andreu A, Prats G, Pathogenicity Island Markers in Commensal and Uropathogenic Escherichia coli Isolates. Clinical Microbiology and Infection, 2006; 12(9):880-6. https://doi.org/10.1111/j.1469-0691.2006.01461.x
World Health Organization (WHO), http://www.who.int/drugresistance/documents/surveillancereport/en/. 2014
Ingti B, Upadhyay S, Hazarika M, Khyriem A B, Paul D, Bhattacharya P, Distribution of Carbapenem Resistant Acinetobacter baumannii with blaADC-30 and Induction of ADC-30 in Response to Beta-lactam Antibiotics. Research Microbiology Journal, 2020; 20:1-29. https://doi.org/10.1016/j.resmic.2020.01.002
Doi Y, Iovleva A, Bonomo, R A, The Ecology of Extended-spectrum beta-lactamases (ESBLs) in the Developed World, Journal of Travel Medicine, 2017; 24(1):44-51. https://doi.org/10.1093/jtm/taw102
Saleem R, Ejaz H, Zafar A, Younas, S, Rathore A W, Phenotypic Characterization of Extended-spectrum- beta-lactamase producing E. coli from Healthy Individuals, Patients, Sewage Sludge, Cattle, Chickens and Raw Meat. Pakistan Journal of Medical Science, 2017; 33(4):886-90. https://doi.org/10.12669/pjms.334.12647
Nordmann P, Naas T, Poirel L, Global spread of carbapenemase-producing Enterobacteriaceae, Emerging Infectious Disease, 2011; 17:1791-8. https://doi.org/10.3201/eid1710.110655
Nomeh OL, Federica OI, Joseph OV, Moneth E C, Ogba R C, Nkechi O A, Peter I U, Akpu P O, Edemekong, C I, Iroha IR, Detection of Carbapenemase-Producing Escherichia coli and Klebsiella pneumoniae Implicated in Urinary Tract Infection. Asian Journal of Research in Infectious Diseases, 2023; 12 (1):15-23
https://doi.org/10.9734/ajrid/2023/v12i1234
Ogba RC, Nomeh O L, Edemekong C I, Nwuzo, A C and Akpu, P O, Peter I U, Iroha IR, Molecular Characterization of Carbapenemase Encoding Genes in Pseudomonas aeruginosa from Tertiary Healthcare in South Eastern Nigeria. Asian Journal of Biochemistry, Genetics and Molecular Biology, 2022a; 12 (4):161-168. https://doi.org/10.9734/ajbgmb/2022/v12i4281
Vila J, Saez-Lopez E, Johnson J R, Romling U, Dobrindt U, Canton R, Escherichia coli: An Old Friend with New Tidings, Federation of European Medical Societies of Microbiology Review, 2016; 40(4):437-63. https://doi.org/10.1093/femsre/fuw005
Tshitshi L, Manganyi M C, Montso P C, Mbewe M, Ateba C N, Extended Spectrum Beta-Lactamase-Resistant Determinants among Carbapenem-Resistant Enterobacteriaceae from Beef Cattle in the North West Province, South Africa: A Critical Assessment of Their Possible Public Health Implications, Antibiotics, 2020; 9:8-20. https://doi.org/10.3390/antibiotics9110820
Solgi H, Nematzadeh S, Giske C G, Badmasti F, Westerlund F, Lin Y L, Goyal G, Nikbin V S, Nemati A H, Shahcheraghi F, Molecular Epidemiology of OXA-48 and NDM-1 Producing Enterobacterales Species at a University Hospital in Tehran, Iran, Between 2015 and 2016, Frontier in Microbiology, 2020; 11:9-36. https://doi.org/10.3389/fmicb.2020.00936
Teixeira P, Tacão M, Pureza L, Gonçalves J, Silva A, Cruz-Schneider, M P, Henriques I, Occurrence of Carbapenemase-producing Enterobacteriaceae in a Portuguese River: blaNDM, blaKPC and blaGES Among the Detected Genes. Environmental Pollution, 2020; 260:113-913. https://doi.org/10.1016/j.envpol.2020.113913
Giamarellou H, Treatment Options for Multidrug Resistant Bacteria. Expert Review Anti-Infection Therapy, 2006; 601:18-23. https://doi.org/10.1586/14787210.4.4.601
Morrill H J, Pogue J M, Kaye K S, LaPlante, K L. Treatment options for carbapenem-resistant Enterobacteriaceae infections, Open Forum of Infection and Disease, 2015; 2:50-100 https://doi.org/10.1093/ofid/ofv050
Teklu D S, Negeri A A, Legese M H, Bedada, T L, Woldemariam H K, Tullu K D, Extended-spectrum beta-lactamase Production and Multi-drug Resistance among Enterobacteriaceae Isolated in Addis Ababa, Ethiopia, Antimicrobial Resistance and Infection Control, 2019; 8:39-67. https://doi.org/10.1186/s13756-019-0488-4
Cheesbrough M, District Laboratory Practice in Tropical Countries (Part II), Cambridge University, 2006. p.19-110. https://doi.org/10.1017/CBO9780511543470
Clinical and Laboratory Standards Institute (CLSI) Performance Standards for Antimicrobial Susceptibility Testing, 28th ed.; Supplement M100; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2019.
Nomeh OL, Chukwu EB, Ogba RC, Akpu PO, Peter IU, Nwuzo AC, Iroha IR, Prevalence and Antibiogram Profile of Carbapenem-resistant Escherichia coli and Klebsiella pneumoniae among Patients with Urinary Tract Infection in Abakaliki, Nigeria, International Journal Pathogen Research, 2022; 11 (3):14-28. https://doi.org/10.9734/ijpr/2022/v11i3212
Ogba RC, Akpu PO, Nwuzo AC, Peter IU, Nomeh OL, Iroha IR, Antibiotic Susceptibility Profile of Clinical Isolate of Carbapenem-Resistant Pseudomonas aeruginosa. South Asian Journal of Research in Microbiology, 2022b; 14 (2):14-23. https://doi.org/10.9734/sajrm/2022/v14i2267
Akpu PO, Nomeh OL, Moneth EC, Stella AO and Ogba RC, Peter IU, Iroha IR, Phenotypic Detection of AmpC beta-lactamase Producing Escherichia coli among Patients in Hospital Wards, Journal of Advance in Microbiology, 2023; 23 (1):26-34 https://doi.org/10.9734/jamb/2023/v23i1702
Peter IU, Ngwu JN, Edemekong CI, Ugwueke IV, Uzoeto HO, Joseph OV, Mohammed ID, Mbong EO, Nomeh OL, Ikusika BA, Ubom IJ, Inyogu JC, Ntekpe ME, Obodoechi IF, NseAbasi, PL., Ogbonna IP, Didiugwu CM, Akpu PO, Alagba EE, Ogba RC, Iroha, IR First report prevalence of Livestock Acquired Methicillin Resistant Staphylococcus aureus (LA-MRSA) strain in South Eastern, Nigeria, IOSR Journal of Nursing and Health Science, 2022; 11(1):50-56.
Kibret M & Abera B, Antimicrobial Susceptibility Patterns of E. coli from Clinical sources in Northeast Ethiopia, Journal of African Health Science, 2011;11(1):40-45. https://doi.org/10.4314/ahs.v11i3.70069
Ghaima K K, Khalaf Z, S, Abdulhassan, A, Salman NY, Prevalence and Antibiotic Resistance of Bacteria Isolated from Urinary Tract Infections of Pregnant Women in Baghdad Hospitals. Biomedical and Pharmacology Journal, 2018; 11(4): 1989-1994. https://doi.org/10.13005/bpj/1573
Alsharapy S A, Yanat B, Lopez-Cerero L, Nasher S S. Díaz-De-Alba P, Pascual A, Rodríguez-Martínez J, Touati A, Prevalence of ST131 Clone Producing Both ESBL CTX-M-15 and AAC(6′)Ib-cr among Ciprofloxacin-Resistant Escherichia coli Isolates from Yemen, Journal of Food Science Microbial Drug Resistance, 2018; 24:10-15. https://doi.org/10.1089/mdr.2018.0024
Kpalap J A, Nwokah E G, Alo M N, Distribution of Some Antibiotics Resistance Genes in Multi-drug Resistant E. coli Isolates from the Urogenitals of Women in Port Harcourt, Nigeria, Asian Journal of Research in Infectious Diseases, 2019; 2(1):1-7. https://doi.org/10.9734/ajrid/2019/v2i130091
Dela H, Egyir B, Majekodunmi A O, Behene E, Yeboah C, Ackah D, Diarrhoeagenic E. coli occurrence and antimicrobial resistance of Extended Spectrum Beta-Lactamases isolated from diarrhoea patients attending health facilities in Accra, Ghana, Public Library of Science One, 2022; 17(5):268-991. https://doi.org/10.1371/journal.pone.0268991
Gatya Al-Mayahie S M, Al-Guranie D R T, Hussein A A, Bachai Z A, Prevalence of common carbapenemase genes and multidrug resistance among uropathogenic Escherichia coli phylogroup B2 isolates from outpatients in Wasit Province/ Iraq, Public Library of Science One, 2022; 17(1): 262-984 https://doi.org/10.1371/journal.pone.0262984
World Health Organization (WHO). Guidelines for Drinking-Water Quality. Geneva, Switzerland: World Health Organization, 2004 Available at: http:// www.who.int/water_sanitation_health/dwq/GDWQ2004web.pdf.
Ateba C N, Tabi N M, Fri J, Bissong M E A, Bezuidenhout C C, Occurrence of Antibiotic-Resistant Bacteria and Genes in Two Drinking Water Treatment and Distribution Systems in the North-West Province of South Africa, Antibiotics, 2020; 9: 7-45. https://doi.org/10.3390/antibiotics9110745
Mogren L, Windstam S, Boqvist S, Vagsholm I, Söderqvist K, Rosberg A K, Lindén J, Mulaosmanovic E, Karlsson M, Uhlig E, The Hurdle Approach-A Holistic Concept for Controlling Food Safety Risks Associated with Pathogenic Bacterial Contamination of Leafy Green Vegetables: A Review, Frontier in Microbiology, 2018; 9:19-65. https://doi.org/10.3389/fmicb.2018.01965
Chelaghma W, Loucif L, Bendjama E, Cherak Z, Bendahou M, Rolain J M, Occurrence of Extended Spectrum Cephalosporin-, Carbapenem- and Colistin-Resistant Gram-Negative Bacteria in Fresh Vegetables, an Increasing Human Health Concern in Algeria, Antibiotics, 2022; 11:9-88. https://doi.org/10.3390/antibiotics11080988
Chen Z, Yu D, He S, Ye H, Zhang L, Wen Y, Zhang W, Shu L, Chen, S, Prevalence of Antibiotic-Resistant Escherichia coli in Drinking Water Sources in Hangzhou City, Frontier in Microbiology, 2017; 8:1133 https://doi.org/10.3389/fmicb.2017.01133
World Health Organization (WHO), Food Safety 2020; Available:https://www.who.int.
World Health Organization (WHO). Food-borne disease Outbreaks, Guidelines for Investigation and Control. World Health Organization. 2008; ISBN 978 92 41547222.
Beshiru A, Okoh A I, Igbinosa E O, Processed Ready-to-eat (RTE) Foods Sold in Yenagoa Nigeria were Colonized by diarrheagenic Escherichia coli which Constitute a Probable Hazard to Human Health, Public Library of Science One, 2022; 17(4):266-59. https://doi.org/10.1371/journal.pone.0266059
Holzel C S, Tetens J L, Schwaiger K, Unraveling the Role of Vegetables in Spreading Antimicrobial-resistant Bacteria: A Need for Quantitative Risk Assessment, Foodborne Pathogen and Disease, 2018; 15:671-688. https://doi.org/10.1089/fpd.2018.2501
Van Hoek A H, Veenman C, Van Overbeek W M, Lynch G, De Roda Husman A M, Blaak H, Prevalence and characterization of ESBL- and AmpC-producing Enterobacteriaceae on Retail Vegetables, International Journal of Food Microbiology, 2015; 204:1-8. https://doi.org/10.1016/j.ijfoodmicro.2015.03.014
Nasiri M J, Mirsaeidi M, Mousavi S M J, Arshadi M, Fardsanei F, Deihim B, Davoudabadi S, Zamani S, Hajikhani B, Goudarzi H, Goudarzi M, Seghatoleslami Z S, Dabiri H, Tabarsi P, Prevalence and Mechanisms of Carbapenem Resistance in Klebsiella pneumoniae and Escherichia coli: A Systematic Review and Meta-Analysis of Cross-Sectional Studies from Iran, Microbial Drug Resistance, 2020; 12:34-56. https://doi.org/10.1089/mdr.2019.0440
Thapa A, Upreti M K, Bimali N K, Shrestha B, Sah A K, Nepal K, Dhungel B, Adhikari S, Adhikari N, Lekhak, B, Rijal K R, Detection of NDM Variants (blaNDM-1, blaNDM-2, blaNDM-3) from Carbapenem-Resistant Escherichia coli and Klebsiella pneumoniae: First Report from Nepal, Infection and Drug Resistance, 2022; 15:4419-4434. https://doi.org/10.2147/IDR.S369934
Aminu A, Daneji I M, Yusuf M A, Jalo R I, Tsiga-Ahmed F I, Yahaya M, Carbapenem-resistant Enterobacteriaceae Infections among Patients Admitted to Intensive Care Units in Kano, Nigeria, Sahel Medical Journal, 2021; 24:1-9.
Alegría A, Arias-Temprano A, Fernández-Natal I, Rodríguez-Calleja J M, García-López M, Santos J A, Molecular Diversity of ESBL-Producing Escherichia coli from Foods of Animal Origin and Human Patients, International Journal Environment Research and Public Health, 2020; 17:1312-1367. https://doi.org/10.3390/ijerph17041312
Adabara N U, Bakinde N D, Enejiyon S O, Salami T, Iorzua D, Detection of Extended Spectrum Beta-Lactamase Producing Escherichia coli from Urinary Tract Infection in General Hospital, Minna, Tanzania Journal of Science, 2020; 46(3): 613-619.
Ortega A, Sa'ez D, Bautista V, Ferna'ndez-Romero S, Lara N, Aracil, B, Carbapenemase-producing Escherichia coli is becoming more Prevalent in Spain mainly because of the Polyclonal Dissemination of OXA-48, Journal of Antimicrobial Agent and Chemotherapy, 2016; 71:2131-8 https://doi.org/10.1093/jac/dkw148
Shaik S, Ranjan A, Tiwari S K, Hussain A, Nandanwar N, Kumar N, Comparative Genomic Analysis of Globally Dominant ST131 Clone with other Epidemiologically Successful Extraintestinal Pathogenic Escherichia coli (ExPEC) Lineages. mBiology, 2017; 8:1596-17. https://doi.org/10.1128/mBio.01596-17
Moxon CA & Paulus S, Beta-lactamases in Enterobacteriaceae Infections in Children, Journal of Infectious, 2016; 72:41-49 https://doi.org/10.1016/j.jinf.2016.04.021
Yigrem C, Fisseha R, Eribo B, Characterization of Carbapenem and β-lactam Resistance in Klebsiella pneumoniae Associated with Leafy Vegetables and Clinical Isolates from Gondar, Ethiopia, Journal of Microbiology Research, 2021; 11(1):21-32
Liu B T, Zhang X Y, Wan S W, Hao J J, Jiang R D, Song F J, Characteristics of Carbapenem-Resistant Enterobacteriaceae in Ready-to-Eat Vegetables in China, Frontier in Microbiology, 2018; 9:1147. https://doi.org/10.3389/fmicb.2018.01147
Amato M, Dasí D, Gonz'alez A, Ferrús M A, Castillo M, Occurrence of Antibiotic Resistant Bacteria and Resistance Genes in Agricultural Irrigation Waters from Valencia City (Spain), Agricultural Water Management, 2021; 256:107-097 https://doi.org/10.1016/j.agwat.2021.107097
Berger C N, Sodha SV, Shaw R K, Griffin P M, Pink D, Hand P and Frankel G, Fresh Fruit and Vegetables as Vehicles for the Transmission of Human Pathogens, Environmental Microbiology, 2010; 12:2385-2397. https://doi.org/10.1111/j.1462-2920.2010.02297.x
Antwi-Agyei P, Cairncross S, Peasey A, Price V, Bruce J, Baker K, Moe C, Ampofo J, Armah G, Ensink J, A Farm to Fork Risk Assessment for the Use of Wastewater in Agriculture in Accra, Ghana, Public Library of Science One, 2015; 10:142-346. https://doi.org/10.1371/journal.pone.0142346
Makkaew P, Miller M, Fallowfield H J, Cromar N J, Microbial Risk in Wastewater Irrigated Lettuce: Comparing Escherichia coli Contamination from an Experimental Site with a Laboratory Approach, Water Science and Technology, 2016; 74:749-755. https://doi.org/10.2166/wst.2016.237
Mahmoud N E, Altayb H N, Gurashi R M, Detection of Carbapenem-Resistant Genes in Escherichia coli Isolated from Drinking Water in Khartoum, Sudan, Journal of Environmental and Public Health, 2020; 6 57-1293. https://doi.org/10.1155/2020/2571293
Amaya E, Reyes D, Paniagua M. Antibiotic resistance patterns of Escherichia coli isolates from different aquatic environmental sources in Leon, Nicaragua, Clinical Microbiology and Infection, 2012; 18(9):347-354. https://doi.org/10.1111/j.1469-0691.2012.03930.x
Tanner W D, VanDerslice J A, Gundlapalli A V, Multi-state Study of Enterobacteriaceae Harboring Extended spectrum Beta-lactamase and Carbapenemase genes in U.S. Drinking Water, Scientific Reports, 2019; 9:20-21. https://doi.org/10.1038/s41598-019-40420-0
Haberecht H B, Nealon N J, Gilliland J R, Antimicrobial- resistant Escherichia coli from Environmental Waters in Northern Colorado, Journal of Environmental and Public Health, 2019; 13:45-82. https://doi.org/10.1155/2019/3862949
De Boeck H, Miwanda B, Lunguya-Metila O, Muyembe-Tamfum J J, Stobberingh E, Glupczynski Y, Jacobs J, ESBL-positive enterobacteria Isolates in Drinking Water, Emerging Infectious Disease, 2012; 18:1019-1020. https://doi.org/10.3201/eid1806.111214
Abera B, Kibret M Mulu W, Extended-spectrum beta (β)-lactamases and antibiogram in Enterobacteriaceae from clinical and drinking water sources from Bahir Dar City, Ethiopia, Public Library of Science One, 2016; 11:166-519. https://doi.org/10.1371/journal.pone.0166519
Madec J Y, Haenni M, Ponsin C, Kieffer N, Rion E, Gassilloud B, Sequence Type-48 Escherichia coli Carrying the blaCTXM-1 IncI1/ST3 Plasmid in Drinking Water in France. Journal of Antimicrobial Agent and Chemotherapy, 2016; 60:6430-6432. https://doi.org/10.1128/AAC.01135-16
Larson A, Hartinger S M, Riveros M, Salmon-Mulanovich G, Hattendorf J, Verastegui H, Huaylinos M L, Ma¨usezahl D, Antibiotic-Resistant Escherichia coli in Drinking Water Samples from Rural Andean Households in Cajamarca, Peru, American Journal of Tropical Medicine Hygiene, 2019; 100(6):1363-1368. https://doi.org/10.4269/ajtmh.18-0776
Martinez-Medina M, Special Issue: Pathogenic Escherichia coli: Infections and Therapies, Antibiotics, 2021; 10:112-116. https://doi.org/10.3390/antibiotics10020112
Akuffo R, Armah G, Clemens M, Kronmann K C, Jones A H, Agbenohevi P, Prevalence of Enteric Infections Among Hospitalized Patients in Two Referral Hospitals in Ghana, BMC Research Notes, 2017; 10:292-300. https://doi.org/10.1186/s13104-017-2621-x
Blaak H, Van Hoek A H, Veenman C, Docters Van Leeuwen A E, Lynch, G, Van Overbeek W M, De Roda Husman A M, Extended Spectrum Beta-lactamase- and Constitutively AmpC-producing Enterobacteriaceae on Fresh Produce and in the Agricultural Environment, International Journal of Food Microbiology, 2014; 169:8-16. https://doi.org/10.1016/j.ijfoodmicro.2013.10.006
Stockwell V O & Duffy B, Use of Antibiotics in Plant Agriculture, Revise Science and Technology, 2012; 31:199-210. https://doi.org/10.20506/rst.31.1.2104
Iseppi R, De Nu S, Bondi M, Messi P, Sabia C, Extended-Spectrum Beta-lactamase, AmpC, and MBL-Producing Gram-Negative Bacteria on Fresh Vegetables and Ready-to-Eat Salads Sold in Local Markets, Microbial Drug Resistance, 2018; 24:1156-1164. https://doi.org/10.1089/mdr.2017.0198
Zalewska M, Blazejewska A, Czapko A, Popowska M, Antibiotics and Antibiotic Resistance Genes in Animal Manure- Consequences of Its Application in Agriculture, Frontier in Microbiology, 2021; 12: 61-656. https://doi.org/10.3389/fmicb.2021.610656
Adegoke A A, Amoah I D, Stenstrom T A, Verbyla M E, Mihelcic J, Epidemiological Evidence and Health Risks Associated with Agricultural Reuse of Partially Treated and Untreated Wastewater: A Review, Frontier in Public Health, 2018; 6:337-339. https://doi.org/10.3389/fpubh.2018.00337
Cerqueira F, Matamoros V, Bayona J, Elsingab G, Hornstrab L M, Pina B, Distribution of Antibiotic Resistance Genes in Soils and Crops. A field Study in Legume Plants (Vicia faba L.) Grown Under Different Watering Regimes, Environmental Research Journal, 2019a; 170:16-25.
https://doi.org/10.1016/j.envres.2018.12.007
Cerqueira F, Matamoros V, Bayona J, Pina B, Antibiotic Resistance Genes Distribution in Microbiomes from the Soil-plant-fruit continuum in commercial Lycopersicon esculentum Fields under Different Agricultural Practices, Science Total Environment, 2019b; 652:660-670. https://doi.org/10.1016/j.scitotenv.2018.10.268
Holzel C S, Tetens J L, Schwaiger K, Unraveling the Role of Vegetables in Spreading Antimicrobial-resistant Bacteria: A Need for Quantitative Risk Assessment, Foodborne Pathogen and Disease, 2018, 15:671-688. https://doi.org/10.1089/fpd.2018.2501
Araújo S, Silva I AT, Tacao M, Patinha C, Alves A, Henriques I, Characterization of Antibiotic Resistant and Pathogenic Escherichia coli in Irrigation Water and Vegetables in Household Farms. International Journal of Food Microbiology, 2017; 257:192-200 https://doi.org/10.1016/j.ijfoodmicro.2017.06.020
Jongman M, Korsten L, Genetic Diversity and Antibiotic Resistance of Escherichia coli Isolates from Different Leafy Green Production Systems, Journal of Food Protocol, 2016; 79:1846-1853. https://doi.org/10.4315/0362-028X.JFP-16-117
Conde-Cid M, Alvarez-Esmorís C, Paradelo-Nú˜nez R, Novoa-Mu˜noz J C, Arias-Est'evez M, Alvarez-Rodríguez E, Fernandez-Sanjurjo M J, Nú˜nez-Delgado A, Occurrence of Tetracyclines and Sulfonamides in Manures, Agricultural Soils and Crops from Different Areas in Galicia (NW Spain), Journal of Clean Production, 2018; 197:491-500. https://doi.org/10.1016/j.jclepro.2018.06.217
Fallah N, Ghaemi M, Ghazvini K, Rad M, Jamshidi A, Occurrence, Pathotypes, and Antimicrobial Resistance Profiles of Diarrheagenic Escherichia coli Strains in Animal Source Food Products from Public Markets in Mashhad, Iran, Food Control, 2021; 121:107640. https://doi.org/10.1016/j.foodcont.2020.107640
Mhawesh A A, Hamid D M, Ghasemian A. Phylogrouping, serogrouping, virulence factors and carbapenemase genes among carbapenemase-producing Escherichia coli from Urinary Tract Infections, Indian Journal of Forensic Medical Toxicology, 2021; 15(2):2979-3003
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