Sheep and goats are reservoirs of colistin resistant Escherichia coli that co-resist critically important antimicrobials: First study from Jordan
Corresponding Author
Mohammad M. Obaidat
Department of Veterinary Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan
Correspondence
Mohammad M. Obaidat, Department of Veterinary Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan.
Email: [email protected]
Search for more papers by this authorYaser H. Tarazi
Department of Basic Veterinary Medical Sciences, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan
Search for more papers by this authorWalaa M. AlSmadi
Department of Veterinary Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan
Search for more papers by this authorCorresponding Author
Mohammad M. Obaidat
Department of Veterinary Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan
Correspondence
Mohammad M. Obaidat, Department of Veterinary Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan.
Email: [email protected]
Search for more papers by this authorYaser H. Tarazi
Department of Basic Veterinary Medical Sciences, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan
Search for more papers by this authorWalaa M. AlSmadi
Department of Veterinary Pathology and Public Health, Faculty of Veterinary Medicine, Jordan University of Science and Technology, Ar-Ramtha, Irbid, Jordan
Search for more papers by this authorFunding information: Jordan University of Science and Technology
Abstract
There is a knowledge gap on colistin-resistant and mobilized colistin-resistant (mcr) Escherichia coli in sheep and goats worldwide. This study determined the prevalence and antimicrobial resistance of mobilized colistin-resistant (mcr) E. coli in dairy sheep and goat flocks in Jordan. A total of 948 milk samples were collected from 155 flocks across Jordan. The milk samples were pre-enriched in MacConkey broth and then plated on MacConkey agar supplemented with 8 mg/l colistin and the presence of mcr-1 gene in the isolates was tested by polymerase chain reaction. In total, 1,158 E. coli isolates were colistin resistant, with 74.8% herd-level prevalence and 39.5% individual animal prevalence. Sixty-one (5.3%) of 1,158 phenotypically colistin-resistant E. coli harbored mcr-1, with 23.9% herd-level prevalence and 6.6% individual animal prevalence. About 77.1% of the mcr-1 E. coli resisted one or more antimicrobial classes and 37.7% were multidrug resistant. More than 30% of the mcr-1 positive E. coli isolates were resistant to nalidixic acid, tetracycline, ceftazidime, cefpodoxime and ampicillin, whereas 8–20% of the isolates were resistant to cefotaxime, ceftriaxone, gentamicin, tobramycin, sulfamethoxazole-trimethoprim, and amoxicillin-clavulanic acid. This study indicates that small ruminants are reservoirs of colistin-resistant and mcr-1 positive E. coli that exhibit co-resistance to critically important antimicrobials which would pose public health issue and calls for the necessary banning of the use of colistin in small ruminants.
CONFLICT OF INTEREST
The authors declare no conflicts of interests.
Open Research
DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available from the corresponding author upon reasonable request.
Supporting Information
Filename | Description |
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jfs13023-sup-0001-Tables.docxWord 2007 document , 16.9 KB | Table S1: Antimicrobial resistance profiles of mcr-1 positive Escherichia coli isolates from sheep and goat milk samples in Jordan, 2020. (Number of resistance isolates is 47). Table S2: Multi-drug resistance percentages of mcr-1 positive Escherichia coli isolates from sheep and goat milk samples in Jordan, 2020. |
Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article.
REFERENCES
- Aklilu, E., & Raman, K. (2020). mcr-1 gene encoded colistin-resistant Escherichia coli in raw chicken meat and bean sprouts in Malaysia. International Journal of Microbiology, 2020, 8853582. https://doi.org/10.1155/2020/8853582
- Allerberger, F., Weissensteiner, G., Springer, B., Schlagenhaufen, C., Lassnig, H., Ruppitsch, W., & Jelovcan, S. (2016). Plasmid-mediated colistin-resistance in Escherichia coli isolated from poultry and broiler meat in Austria in 2016. International Journal of Infectious Diseases, 53, 36–37. https://doi.org/10.1016/j.ijid.2016.11.0
- Barlaam, A., Parisi, A., Spinelli, E., Caruso, M., Taranto, P. D., & Normanno, G. (2019). Global emergence of colistin-resistant Escherichia coli in food chains and associated food safety implications: A review. Journal of Food Protection, 82, 1440–1448. https://doi.org/10.4315/0362-028X.JFP-19-116
- Braun, S. D., Ahmed, M. F. E., El-Adawy, H., Hotzel, H., Engelmann, I., Weiß, D., … Ehricht, R. (2016). Surveillance of extended-spectrum beta-lactamase-producing Escherichia coli in dairy cattle farms in the Nile Delta, Egypt. Frontiers in Microbiology, 7, 1020. https://doi.org/10.3389/fmicb.2016.01020
- Brennan, E., Martins, M., McCusker, M. P., Wang, J., Alves, B. M., Hurley, D., … Fanning, S. (2016). Multidrug-resistant Escherichia coli in bovine animals, Europe. Emerging Infectious Diseases, 22, 1650–1652. https://doi.org/10.3201/eid2209.160140
- Clinical and Laboratory Standards Institute, (2014). Performance standards for antimicrobial susceptibility testing. Twenty-fourth informational supplement, M100-S24 January, Clinical and Laboratory Standards Institute, Wayne, PA.
- Dandachi, I., Chabou, S., Daoud, Z., & Rolain, J.-M. (2018). Prevalence and emergence of extended-spectrum cephalosporin-, carbapenem- and colistin-resistant gram negative bacteria of animal origin in the Mediterranean Basin. Frontiers in Microbiology, 9, 2299. https://doi.org/10.3389/fmicb.2018.02299
- Dutta, A., Islam, M. Z., Barua, H., Rana, E. A., Jalal, M. S., Dhar, P. K., … Biswas, P. K. (2020). Acquisition of plasmid-mediated colistin resistance gene mcr-1 in Escherichia coli of livestock origin in Bangladesh. Microbial Drug Resistance, 26, 1058–1062. https://doi.org/10.1089/mdr.2019.0304
- Elnahriry, S. S., Khalifa, H. O., Soliman, A. M., Ahmed, A. M., Hussein, A. M., Shimamoto, T., & Shimamoto, T. (2016). Emergence of plasmid-mediated colistin resistance gene mcr-1 in a clinical Escherichia coli isolate from Egypt. Antimicrobial Agents and Chemotherapy, 60, 3249–3250. https://doi.org/10.1128/AAC.00269-16
- El-Sayed Ahmed, M. A. E.-G., Zhong, L.-L., Shen, C., Yang, Y., Doi, Y., & Tian, G.-B. (2020). Colistin and its role in the era of antibiotic resistance: An extended review (2000–2019). Emerging Microbes and Infection, 9, 868–885. https://doi.org/10.1080/22221751.2020.1754133
- Eltayb, A., Barakat, S., Marrone, G., Shaddad, S., & Stalsby Lundborg, C. (2012). Antibiotic use and resistance in animal flocking: A quantitative and qualitative study on knowledge and practices among farmers in Khartoum, Sudan. Zoonoses and Public Health, 59, 330–338. https://doi.org/10.1111/j.1863-2378.2012.01458.x
- Filioussis, G., Kachrimanidou, M., Christodoulopoulos, G., Kyritsi, M., Hadjichristodoulou, C., Adamopoulou, M., … Grinberg, A. (2020). Bovine mastitis caused by a multidrug-resistant, mcr-1-positive (colistin-resistant), extended-spectrum β-lactamase–producing Escherichia coli clone on a Greek dairy flock. Journal of Dairy Science, 103, 852–857. https://doi.org/10.3168/jds.2019-17320
- Ghafur, A., Shankar, C., Gnana Soundari, P., Venkatesan, M., Mani, D., Thirunarayanan, M., & Veeraraghavan, B. (2019). Detection of chromosomal and plasmid-mediated mechanisms of colistin resistance in Escherichia coli and Klebsiella pneumoniae from Indian food samples. Journal of Global Antimicrobial Resistance, 16, 48–52. https://doi.org/10.1016/j.jgar.2018.09.005
- Gharaibeh, M. H., & Shatnawi, S. Q. (2019). An overview of colistin resistance, mobilized colistin resistance genes dissemination, global responses, and the alternatives to colistin: A review. Veterinary World, 12(11), 1735–1746.
- Grami, R., Mansour, W., Mehri, W., Bouallegue, O., Boujaafar, N., Madec, J. Y., & Haenni, M. (2016). Impact of food animal trade on the spread of mcr-1-mediated colistin resistance, Tunisia, July 2015. Eurosurveillance, 21, 30144. https://doi.org/10.2807/1560-7917.ES.2016.21.8.30144
- Haenni, M., Poirel, L., Kieffer, N., Châtre, P., Saras, E., Métayer, V., … Madec, J.-Y. (2016). Co-occurrence of extended spectrum β lactamase and MCR-1 encoding genes on plasmids. Lancet Infectious Diseases, 16, 281–282. https://doi.org/10.1016/S1473-3099(16)00007-4
- Hammad, A. M., Hoffmann, M., Gonzalez-Escalona, N., Abbas, N. H., Yao, K., Koenig, S., … Eppinger, M. (2019). Genomic features of colistin-resistant Escherichia coli ST69 strain harboring mcr-1 on IncHI2 plasmid from raw milk cheese in Egypt. Infection, Genetic and Evolution, 73, 126–131. https://doi.org/10.1016/j.meegid.2019.04.021
- Hasman, H., Hammerum, A. M., Hansen, F., Hendriksen, R. S., Olesen, B., Agerso, Y., … Skov, R. L. (2015). Detection of mcr-1 encoding plasmid-mediated colistin-resistant Escherichia coli isolates from human bloodstream infection and imported chicken meat, Denmark 2015. Eurosurveillance, 20, pii=30085. https://doi.org/10.2807/1560-7917.ES.2015.20.49.30085
- Hassen, B., Hammami, S., Hassen, A., & Abbassi, M. S. (2022). Molecular mechanisms and clonal lineages of colistin-resistant bacteria across the African continent: A scoping review. Letters in Applied Microbiology. https://doi.org/10.1111/lam.13818
- Hassen, B., Saloua, B., Abbassi, M. S., Ruiz-Ripa, L., Mama, O. M., Hassen, A., … Torres, C. (2019). Mcr-1 encoding colistin resistance in CTX-M-1/CTX-M-15- producing Escherichia coli isolates of bovine and caprine origins in Tunisia. First report of CTX-M-15-ST394/D E. coli from goats. Comparative Immunology, Microbiology and Infectious Diseases, 67, 101366. https://doi.org/10.1016/j.cimid.2019.101366
- Hmede, Z., & Kassem, I. I. (2018). The colistin resistance gene, mcr-1, is prevalent in commensal E. coli isolated from Lebanese pre-harvest poultry. Antimicrobial Agents and Chemotherapy, 62, e01304–e01318. https://doi.org/10.1128/AAC.01304-18
- Hooper, D. C., Wolfson, J. S., Ng, E. Y., & Swartz, M. N. (1987). Mechanisms of action of and resistance to ciprofloxacin. American Journal of Medicine, 82, 12–20.
- Irrgang, A., Roschanski, N., Tenhagen, B.-A., Grobbel, M., Skladnikiewicz-Ziemer, T., Thomas, K., … Käsbohrer, A. (2016). Prevalence of mcr-1 in E. coli from livestock and food in Germany, 2010–2015. PLoS One, 11, e0159863. https://doi.org/10.1371/journal.pone.0159863
- Jouy, E., Haenni, M., Le Devendec, L., Le Roux, A., Chatre, P., Madec, J. Y., & Kempf, I. (2017). Improvement in routine detection of colistin resistance in E. coli isolated in veterinary diagnostic laboratories. Journal of Microbiological Methods, 132, 125–127. https://doi.org/10.1016/j.mimet.2016.11.017
- Karki, D., Dhungel, B., Bhandari, S., Kunwar, A., Joshi, P. R., Shrestha, B., … Banjara, M. R. (2021). Antibiotic resistance and detection of plasmid mediated colistin resistance mcr-1 gene among Escherichia coli and Klebsiella pneumoniae isolated from clinical samples. Gut Pathogens, 13, 45. https://doi.org/10.1186/s13099-021-00441-5
- Kawasaki, S., Horikoshi, N., Okada, Y., Takeshita, K., Sameshima, T., & Kawamoto, S. (2005). Multiplex PCR for simultaneous detection of Salmonella spp., Listeria monocytogenes, and Escherichia coli O157:H7 in meat samples. Journal of Food Protection, 68, 551–556. https://doi.org/10.4315/0362-028X-68.3.551
- Li, B., Ke, B., Zhao, X., Guo, Y., Wang, W., Wang, X., & Zhu, H. (2018). Antimicrobial resistance profile of mcr-1 positive clinical isolates of Escherichia coli in China from 2013 to 2016. Frontiers in Microbiology, 9, 2514. https://doi.org/10.3389/fmicb.2018.02514
- Liu, Y.-Y., Wang, Y., Walsh, T. R., Yi, L.-X., Zhang, R., Spencer, J., … Shen, J. (2016). Emergence of plasmid-mediated colistin resistance mechanism mcr-1 in animals and human beings in China: A microbiological and molecular biological study. Lancet Infectious Diseases, 16, 161–168. https://doi.org/10.1016/S1473-3099(15)00424-7
- Maheux, A. F., Picard, F. J., Boissinot, M., Bissonnette, L., Paradis, S., & Bergeron, M. G. (2009). Analytical comparison of nine PCR primer sets designed to detect the presence of Escherichia coli/Shigella in water samples. Water Research, 43, 3019–3028. https://doi.org/10.1016/j.watres.2009.04.017
- Majewski, P., Gutowska, A., Smith, D. G. E., Hauschild, T., Majewska, P., Hryszko, T., … Tryniszewska, E. A. (2021). Plasmid mediated mcr-1.1 colistin-resistance in clinical extraintestinal Escherichia coli strains isolated in Poland. Frontiers in Microbiology, 12, 547020. https://doi.org/10.3389/fmicb.2021.547020
- Malhotra-Kumar, S., Xavier, B. B., Das, A. J., Lammens, C., Butaye, P., & Goossens, H. (2016). Colistin resistance gene mcr-1 harboured on a multidrug resistant plasmid. Lancet Infectious Diseases, 16, 283–284. https://doi.org/10.1016/S1473-3099(16)00012-8
- Monte, D. F., Mem, A., Fernandes, M. R., Cerdeira, L., Esposito, F., Galvão, J. A., … Landgraf, M. (2017). Chicken meat as a reservoir of colistin-resistant Escherichia coli strains carrying mcr-1 genes in South America. Antimicrobial Agents and Chemotherapy, 61, e02718-16. https://doi.org/10.1128/AAC.02718-16
- Nagy, Á., Székelyhidi, R., Hanczné Lakatos, E., & Kapcsándi, V. (2021). Review on the occurrence of the mcr-1 gene causing colistin resistance in cow's milk and dairy products. Heliyon, 7, e06800. https://doi.org/10.1016/j.heliyon.2021.e06800
- Obaidat, M. M. (2019). Seroprevalence and risk factors for Campylobacter jejuni seropositivity in Jordan. Infectious Diseases, 51, 140–146. https://doi.org/10.1080/23744235.2018.1540883
- Obaidat, M. M., Al-Zyoud, A. A., Bani Salman, A. E., & Davis, M. A. (2017). Antimicrobial use and resistance among commensal Escherichia coli and Salmonella enterica in rural Jordan small ruminant herds. Small Ruminant Research, 149, 99–104. https://doi.org/10.1016/j.smallrumres.2017.01.014
- Obaidat, M. M., Malania, L., Imnadze, P., Roess, A. A., Bani Salman, A. E., & Arner, R. J. (2019). Seroprevalence and risk factors for Coxiella burnetii in Jordan. American Journal of Tropical Medicine and Hygiene, 101, 40–44. https://doi.org/10.4269/ajtmh.19-0049
- Ohsaki, Y., Hayashi, W., Saito, S., Osaka, S., Taniguchi, Y., Koide, S., … Nagano, N. (2017). First detection of an Escherichia coli strain harboring the mcr-1 gene in retail domestic chicken meat in Japan. Japanese Journal of Infectious Disease, 70, 590–592. https://doi.org/10.7883/yoken.JJID.2016.572
- Ojo, O. E., Schwarz, S., & Michael, G. B. (2016). Detection and characterization of extended-spectrum β-lactamase-producing Escherichia coli from chicken production chains in Nigeria. Veterinary Microbiology, 194, 62–68. https://doi.org/10.1016/j.vetmic.2016.04.022
- Olaitan, A. O., Thongmalayvong, B., Akkhavong, K., Somphavong, S., Paboriboune, P., Khounsy, S., … Rolain, J. M. (2015). Clonal transmission of a colistin-resistant Escherichia coli from a domesticated pig to a human in Laos. Antimicrobial Agents and Chemotherapy, 70, 3402–3404. https://doi.org/10.1093/jac/dkv252
- Pfeiffer, D. U. (2002). Veterinary epidemiology—An introduction. Oxford: Wiley-Blackwell.
- Poirel, L., Kieffer, N., Brink, A., Coetze, J., Jayol, A., & Nordmann, P. (2016). Genetic features of mcr-1-producing colistin-resistant Escherichia coli isolates in South Africa. Antimicrobial Agents and Chemotherapy, 60, 4394–4397. https://doi.org/10.1128/AAC.00444-16
- Rapoport, M., Faccone, D., Pasteran, F., Ceriana, P., Albornoz, E., Petroni, A., … Corso, A. (2016). First description of mcr-1-mediated colistin resistance in human infections caused by Escherichia coli in Latin America. Antimicrobial Agents and Chemotherapy, 60, 4412–4413. https://doi.org/10.1128/AAC.00573-16
- Rebelo, A. R., Bortolaia, V., Kjeldgaard, J. S., Pedersen, S. K., Leekitcharoenphon, P., Hansen, I. M., … Hendriksen, R. S. (2018). Multiplex PCR for detection of plasmid-mediated colistin resistance determinants, mcr-1, mcr-2, mcr-3, mcr-4 and mcr-5 for surveillance purposes. Eurosurveillance, 23, pii=17-00672. https://doi.org/10.2807/1560-7917.ES.2018.23.6.17-00672
- Redding, L. E., Cubas-Delgado, F., Sammel, M. D., Smith, G., Galligan, D. T., Levy, M. Z., & Hennessy, S. (2014). The use of antibiotics on small dairy flocks in rural Peru. Preventive Veterinary Medicine, 113, 88–95. https://doi.org/10.1016/j.prevetmed.2013.10.012
- Song, Y., Yu, L., Zhang, Y., Dai, Y., Wang, P., Feng, C., … Wang, F. (2020). Prevalence and characteristics of multidrug-resistant mcr-1-positive Escherichia coli isolates from broiler chickens in Tai'an, China. Poultry Science, 99, 1117–1123. https://doi.org/10.1016/j.psj.2019.10.044
- Vasquez, A. M., Montero, N., Laughlin, M., Dancy, E., Melmed, R., Sosa, L., … Walters, M. S. (2016). Investigation of Escherichia coli harboring the mcr-1 resistance gene—Connecticut, 2016. Morbidity and Mortality Weekly Report, 65, 979–980. https://doi.org/10.15585/mmwr.mm6536e3
- Vounba, P., Rhouma, M., Arsenault, J., Bada Alambédji, R., Fravalo, P., & Fairbrother, J. M. (2019). Prevalence of colistin resistance and mcr-1/mcr-2 genes in extended-spectrum β-lactamase/Amp C-producing Escherichia coli isolated from chickens in Canada, Senegal and Vietnam. Journal of Global Antimicrobial Resistance, 19, 222–227. https://doi.org/10.1016/j.jgar.2019.05.002
- World Health Organization. (2019). Critically important antimicrobials for human medicine (6th revision). Accessed September 12, 2021. https://apps.who.int/iris/bitstream/handle/10665/312266/9789241515528-eng.pdf
- Yamaguchi, T., Kawahara, R., Harada, K., Teruya, S., Nakayama, T., Motooka, D., … Yamamoto, Y. (2018). The presence of colistin resistance gene mcr-1 and -3 in ESBL producing Escherichia coli isolated from food in Ho Chi Minh City, Vietnam. FEMS Microbiology Letters, 365, fny100. https://doi.org/10.1093/femsle/fny100