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Carriage of Plasmid-Mediated Colistin Resistance-1-Positive Escherichia coli in Humans, Animals, and Environment on Farms in Vietnam
Phuong Thi Lan Nguyen
Phuong Thi Lan Nguyen
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Hung Thi Mai Tran
Hung Thi Mai Tran
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Hai Anh Tran
Hai Anh Tran
Hanoi Medical University, Hanoi, Vietnam;
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Thai Duy Pham
Thai Duy Pham
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Tan Minh Luong
Tan Minh Luong
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Thanh Ha Nguyen
Thanh Ha Nguyen
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Lien Thi Phuong Nguyen
Lien Thi Phuong Nguyen
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Tho Thi Thi Nguyen
Tho Thi Thi Nguyen
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Ha Thi An Hoang
Ha Thi An Hoang
Vinh Medical University, Nghe An, Vietnam;
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Chi Nguyen
Chi Nguyen
National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
Association of Public Health Laboratories, Silver Spring, Maryland;
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Association of Public Health Laboratories, Silver Spring, Maryland;
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Duong Nhu Tran
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National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Anh Duc Dang
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National Institute of Hygiene and Epidemiology, Hanoi, Vietnam;
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Masato Suzuki
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National Institute of Infectious Diseases, Tokyo, Japan;
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Thanh Viet Le
Thanh Viet Le
Oxford University Clinical Research Unit, Hanoi, Vietnam;
Quadram Institute Bioscience, Norwich Research Park, Norwich, United Kingdom;
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Quadram Institute Bioscience, Norwich Research Park, Norwich, United Kingdom;
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Anne-Laure Bañuls
Anne-Laure Bañuls
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Marc Choisy
Marc Choisy
Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam;
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Rogier H. Van Doorn
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Huy Hoang Tran
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ABSTRACT.
Plasmid-Mediated Colistin Resistance 1 (mcr-1) was first reported in 2015 and is a great concern to human health. In this study, we investigated the prevalence of mcr-1 and mcr-1-positive Escherichia coli (MCRPEC) and the association in infection status among various reservoirs connected to livestock. The study was conducted in 70 poultry and swine farms in a commune in Ha Nam province, northern Vietnam. Samples were collected from farmers, food animals, domestic animals, and farm environments (flies and wastewater) for polymerase chain reaction (PCR) screening for mcr-1 gene and species identification of PCR positive isolates. Among 379 obtained mcr-1 positives isolates, Escherichia coli was the major identified, varying from 50% (2/4) in dog feces to 100% (31/31) in humans feces isolates. The prevalence of MCRPEC was 14.4% (20/139), 49.7% (96/193), 31.3% (25/80), 36.7% (40/109), 26.9% (18/67), and 3.9% (2/51) in humans, chickens, pigs, flies, wastewater, and dogs, respectively. The study identified association between MCRPEC infection status in humans and flies (OR = 3.4), between flies and chickens (OR = 5.3), and between flies and pigs (OR = 9.0). Farmers’ age and farm livestock unit were also associated factors of MCRPEC infection status in humans (OR = 5.1 and 1.05, respectively). These findings bring new knowledge on antibiotic resistance in livestock setting and important suggestions on potential role of flies in the transmission of mcr-1 resistance gene.
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Author Notes
These authors contributed equally to this work.
Financial Support: This work was supported by the Vietnam National Foundation for Science and Technology Development (NAFOSTED) under grant number 108.02-2017.320, GCRF OneHealth Poultry Hub (Royal Veterinary College, United Kingdom) under grant number BB/S001269/1, The Japan Agency for Medical Research and Development (AMED) under grant numbers JP21fk0108093, JP21fk0108139, JP21fk0108133, JP21wm0325003, JP21wm0325022, JP21wm0225004, JP21wm0225008, and JP21gm1610003 and from IRD and LMI DRISA.
Authors’ addresses: Phuong Thi Lan Nguyen, Hung Thi Mai Tran, Thai Duy Pham, Tan Minh Luong, Thanh Ha Nguyen, Lien Thi Phuong Nguyen, Tho Thi Thi Nguyen, Duong Nhu Tran, and Anh Duc Dang, National Institute of Hygiene and Epidemiology, Hanoi, Vietnam, E-mails: ntlp@nihe.org.vn, ttmh@nihe.org.vn, phamduythai8289@gmail.com, lmt@nihe.org.vn, hathanh160199@gmail.com, ntpl@nihe.org.vn, nttt2@nihe.org.vn, trannhuduong@gmail.com, and dda@nihe.org.vn. Hai Anh Tran, Hanoi Medical University, Hanoi, Vietnam, E-mail: haianhtran.med@gmail.com. Ha Thi An Hoang, Vinh Medical University, Nghe An, Vietnam, E-mail: anha@vmu.edu.vn. Chi Nguyen, National Institute of Hygiene and Epidemiology, Hanoi, Vietnam, Association of Public Health Laboratories, Silver Spring, MD, E-mail: lanchi0709@gmail.com. Masato Suzuki, National Institute of Infectious Diseases, Tokyo, Japan, E-mail: suzuki-m@nihe.go.jp. Thanh Viet Le, Oxford University Clinical Research Unit, Hanoi, Vietnam, Quadram Institute Bioscience, Norwich Research Park, Norwich, United Kingdom, E-mail: thanh.le-viet@quadram.ac.uk. Anne-Laure Bañuls, MIVEGEC (IRD-CNRS-Université de Montpellier), LMI DRISA, Centre IRD, Montpellier, France, E-mail: anne-laure.banuls@ird.fr. Marc Choisy, Oxford University Clinical Research Unit, Ho Chi Minh City, Vietnam, and Centre for Tropical Medicine and Global Health, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, United Kingdom, E-mail: mchoisy@oucru.org. Rogier H. Van Doorn, Oxford University Clinical Research Unit, Hanoi, Vietnam, Centre for Tropical Medicine and Global Health, Nuffield Department of Clinical Medicine, University of Oxford, Oxford, United Kingdom, E-mail: rvandoorn@oucru.org. Huy Hoang Tran, National Institute of Hygiene and Epidemiology, Hanoi, Vietnam, and Hanoi Medical University, Hanoi, Vietnam, E-mail: tth@nihe.org.vn.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
Zurfluh K, Nüesch-Inderbinen M, Morach M, Berner AZ, Hächler H, Stephan R , 2015. Extended-spectrum-β-lactamase-producing Enterobacteriaceae isolated from vegetables imported from the Dominican Republic, India, Thailand, and Vietnam. Appl Environ Microbiol 81: 3115–3120.
-
2.
Wang Y, Tian G-B, Zhang R, Shen Y, Tyrrell JM, Huang X, Zhou H, Lei L, Li H-Y, Doi Y , 2017. Prevalence, risk factors, outcomes, and molecular epidemiology of mcr-1-positive Enterobacteriaceae in patients and healthy adults from China: an epidemiological and clinical study. Lancet Infect Dis 17: 390–399.
-
3.
Hu Y, Liu F, Lin IY, Gao GF, Zhu B , 2016. Dissemination of the mcr-1 colistin resistance gene. Lancet Infect Dis 16: 146–147.
-
4.
Perrin-Guyomard A, Bruneau M, Houée P, Deleurme K, Legrandois P, Poirier C, Soumet C, Sanders P, 2016. Prevalence of mcr-1 in Commensal Escherichia coli from French Livestock, 2007 to 2014.
-
5.
Carrique‐Mas JJ, Trung NV, Hoa NT, Mai HH, Thanh TH, Campbell JI, Wagenaar JA, Hardon A, Hieu TQ, Schultsz C , 2014. Antimicrobial usage in chicken production in the Mekong Delta of Vietnam. Zoonoses Public Health 62: 70–78.
-
6.
Nhung N, Cuong N, Campbell J, Hoa N, Bryant J, Truc V, Kiet B, Jombart T, Trung N, Hien V , 2015. High levels of antimicrobial resistance among Escherichia coli isolates from livestock farms and synanthropic rats and shrews in the Mekong Delta of Vietnam. Appl Environ Microbiol 81: 812–820.
-
7.
Nguyen VT, Carrique-Mas JJ, Ngo TH, Ho HM, Ha TT, Campbell JI, Nguyen TN, Hoang NN, Pham VM, Wagenaar JA , 2015. Prevalence and risk factors for carriage of antimicrobial-resistant Escherichia coli on household and small-scale chicken farms in the Mekong Delta of Vietnam. J Antimicrob Chemother 70: 2144–2152.
-
8.
Trung NV, Matamoros S, Carrique-Mas JJ, Nghia NH, Nhung NT, Chieu TTB, Mai HH, van Rooijen W, Campbell J, Wagenaar JA , 2017. Zoonotic transmission of mcr-1 colistin resistance gene from small-scale poultry farms, Vietnam. Emerg Infect Dis 23: 529–532.
-
9.
Dang STT, Truong DTQ, Olsen JE, Tran NT, Truong GTH, Vu HTK, Dalsgaard A , 2020. Research note: occurrence of mcr-encoded colistin resistance in Escherichia coli from pigs and pig farm workers in Vietnam. FEMS Microbes 1: xtaa003.
-
10.
Wang Y, Zhang R, Li J, Wu Z, Yin W, Schwarz S, Tyrrell JM, Zheng Y, Wang S, Shen Z , 2017. Comprehensive resistome analysis reveals the prevalence of NDM and MCR-1 in Chinese poultry production. Nat Microbiol 2: 16260.
-
11.
European Committee on Antimicrobial Susceptibility Testing (EUCAST) , 2017. Breakpoint Tables for Interpretation of MICs and Zone Diameters. Version 7.1.
-
12.
Liu Y-Y, Wang Y, Walsh TR, Yi L-X, Zhang R, Spencer J, Doi Y, Tian G, Dong B, Huang X , 2016. Emergence of plasmid-mediated colistin resistance mechanism MCR-1 in animals and human beings in China: a microbiological and molecular biological study. Lancet Infect Dis 16: 161–168.
-
13.
Vietnamese Government , 2020. Decree 13/2020/NĐ-CP Detail Guideline of Livestock Law.
-
14.
Geser N, Stephan R, Korczak BM, Beutin L, Hächler H, 2011. Molecular identification of blaESBL genes from Enterobacteriaceae isolated from healthy human carriers in Switzerland. Antimicrob Agents Chemother: AAC. 05539-11.
-
15.
Kaye KS, Pogue JM , 2015. Infections caused by resistant Gram‐negative bacteria: epidemiology and management. Pharmacotherapy 35: 949–962.
-
16.
Barguigua A, El Otmani F, Talmi M, Bourjilat F, Haouzane F, Zerouali K, Timinouni M , 2011. Characterization of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella pneumoniae isolates from the community in Morocco. J Med Microbiol 60: 1344–1352.
-
17.
Laxminarayan R, Heymann DL , 2012. Challenges of drug resistance in the developing world. BMJ 344: e1567.
-
18.
Andreu A, Planells I , 2008. Etiology of community-acquired lower urinary infections and antimicrobial resistance of Escherichia coli: a national surveillance study. Med Clin (Barc) 130: 481–486.
-
19.
Arpin C, Quentin C, Grobost F, Cambau E, Robert J, Dubois V, Coulange L, Andre C , 2009. Nationwide survey of extended-spectrum β-lactamase-producing Enterobacteriaceae in the French community setting. J Antimicrob Chemother 63: 1205–1214.
-
20.
Bonten M, Stobberingh E, Philips J, Houben A , 1992. Antibiotic resistance of Escherichia coli in fecal samples of healthy people in two different areas in an industrialized country. Infection 20: 258–262.
-
21.
Calva JJ, Sifuentes-Osornio J, Céron C , 1996. Antimicrobial resistance in fecal flora: longitudinal community-based surveillance of children from urban Mexico. Antimicrob Agents Chemother 40: 1699–1702.
-
22.
Stürmer T, Erb A, Marre R, Brenner H , 2004. Prevalence and determinants of antibiotic resistance in faecal Escherichia coli among unselected patients attending general practitioners in southwest Germany. Pharmacoepidemiol Drug Saf 13: 303–308.
-
23.
Yumuk Z, Afacan G, Nicolas-Chanoine M-H, Sotto A, Lavigne J-P , 2008. Turkey: a further country concerned by community-acquired Escherichia coli clone O25-ST131 producing CTX-M-15. J Antimicrob Chemother 62: 284–288.
-
24.
Rahman M, Husna A, Elshabrawy HA, Alam J, Runa NY, Badruzzaman A, Banu NA, Al Mamun M, Paul B, Das S , 2020. Isolation and molecular characterization of multidrug-resistant Escherichia coli from chicken meat. Sci Rep 10: 21999.
-
25.
Tawyabur M, Islam M, Sobur M, Hossain M, Mahmud M, Paul S, Hossain MT, Ashour HM, Rahman M , 2020. Isolation and characterization of multidrug-resistant Escherichia coli and Salmonella spp. from healthy and diseased turkeys. Antibiotics (Basel) 9: 770.
-
26.
Azad M, Rahman A, Rahman M, Amin R, Begum M, Ara I, Fries R, Husna A, Khairalla AS, Badruzzaman A , 2019. Susceptibility and multidrug resistance patterns of Escherichia coli isolated from cloacal swabs of live broiler chickens in Bangladesh. Pathogens 8: 118.
-
27.
Van den Bogaard A, London N, Driessen C, Stobberingh E , 2001. Antibiotic resistance of faecal Escherichia coli in poultry, poultry farmers and poultry slaughterers. J Antimicrob Chemother 47: 763–771.
-
28.
Miles TD, McLaughlin W, Brown PD , 2006. Antimicrobial resistance of Escherichia coli isolates from broiler chickens and humans. BMC Vet Res 2: 7–9.
-
29.
Malhotra-Kumar S, Xavier BB, Das AJ, Lammens C, Hoang HTT, Pham NT, Goossens H , 2016. Colistin-resistant Escherichia coli harbouring mcr-1 isolated from food animals in Hanoi, Vietnam. Lancet Infect Dis 16: 286–287.
-
30.
Nguyen NT, Nguyen HM, Nguyen CV, Nguyen TV, Nguyen MT, Thai HQ, Ho MH, Thwaites G, Ngo HT, Baker S , 2016. Use of colistin and other critical antimicrobials on pig and chicken farms in southern Vietnam and its association with resistance in commensal Escherichia coli bacteria. Appl Environ Microbiol 82: 3727–3735.
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