1. Food and Health
  2. Archive
  3. Volume 6, Issue 3
Year 2020, Volume 6 , Issue 3, Pages 160 - 169 2020-05-16

Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015

Mustafa GUZEL [1] , M. Dilek AVSAROGLU [2] , Yeşim SOYER [3]

Abstract

Antimicrobial resistance of pathogenic microorganisms is an emerging public health concern. Intensive use of antibiotics in food animals might increase antimicrobial resistance in foodborne pathogens. Colistin is a last resort antibiotic for treatment of multidrug resistant (MDR) Gram negative pathogens. The recent antimicrobial resistance studies revealed a mobile antimicrobial resistance gene (mcr) that provides resistance to colistin. Furthermore, the gene has been found in different genera. Therefore, the aim of this study was to determine colistin resistance of Escherichia coli isolates (N=48) isolated in between 2011 and 2015 from food samples in Turkey. In addition, 5 mcr genes and their variants were screened by performing PCR on resistant isolates. 4 E. coli isolates were found resistant to colistin above the epidemiological cut-off value (Minimum inhibitory concentration (MIC) > 2mg/L). None of the resistant isolates had the mcr genes. Further studies with human and food isolates should be conducted to figure out which gene or genes are responsible for colistin resistance.

Keywords

Antimicrobial resistance, Colistin, Escherichia coli,

References

  • Arcilla, M.S., van Hattem, J.M., Matamoros, S., Melles, D.C., Penders, J., de Jong, M.D., Schultsz, C. (2016). Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases, 16(2), 147-149. https://doi.org/10.1016/S1473-3099(15)00541-1
  • Borowiak, M., Fischer, J., Hammer, J.A., Hendriksen, R.S., Szabo, I., Malorny, B. (2017). Identification of a novel transposon-associated phosphoethanolamine transferase gene, mcr-5, conferring colistin resistance in d-tartrate fermenting Salmonella enterica subsp. enterica serovar Paratyphi B. Journal of Antimicrobial Chemotherapy, 72(12), 3317-3324. https://doi.org/10.1093/jac/dkx327
  • Carattoli, A., Villa, L., Feudi, C., Curcio, L., Orsini, S., Luppi, A., Pezzotti, G., Magistrali, C.F. (2017). Novel plasmid-mediated colistin resistance mcr-4 gene in Salmonella and Escherichia coli, Italy 2013, Spain and Belgium, 2015 to 2016. Eurosurveillance, 22(31), 30589. https://doi.org/10.2807/1560-7917.ES.2017.22.31.30589
  • Carroll, L.M., Gaballa, A., Guldimann, C., Sullivan, G., Henderson, L.O., Wiedmann, M. (2019). Identification of novel mobilized colistin resistance gene mcr-9 in a multidrug-resistant, colistin-susceptible Salmonella enterica serotype Typhimurium isolate. mBio, 10(3), e00853-19. https://doi.org/10.1128/mBio.00853-19
  • Centers for Disease Control and Prevention (CDC). (2013). Antibiotic resistance threats in the United States. http://www.cdc.gov/drugresistance/threat-report-2013/pdf/ar-threats-2013-508.pdf (accessed 11/21/2018).
  • Chen, K., Chan, E.W.C., Xe, M,. Ye, L., Dong, N., Chen, S. (2017). Widespread distribution of mcr-1-bearing bacteria in the ecosystem, 2015 to 2016. Eurosurveillance, 22(39), 17-00206. https://doi.org/10.2807/1560-7917.ES.2017.22.39.17-00206
  • Clinical and Laboratory Standards Institute (CLSI) (2014). Performance standards for antimicrobial susceptibility testing; Twenty-fourth informational supplement. CLSI document M100-S24. Clinical and Laboratory Standards Institute Wayne, PA.
  • Cui, M., Zhang, J., Zhang, C., Li, R., Chan, E.W., Wu, C., Wu, C., Chen, S. (2017). Distinct mechanisms of acquisition of mcr-1 -bearing plasmid by Salmonella strains recovered from animals and food samples. Scientific Reports, 7, 13199. https://doi.org/10.1038/s41598-017-01810-4
  • Doumith, M., Godbole, G.A., Philip, L., Lesley, D., Tim, D., Martin, D., Michaela, M-P., Berit, E., Matthew, J de P, Elizabeth, J., Alan, P.H., Katie, L.W. (2016). Detection of the plasmid-mediated mcr-1 gene conferring colistin resistance in human and food isolates of Salmonella enterica and Escherichia coli in England and Wales. Journal of Antimicrobial Chemotherapy, 71(8), 2300-2305. https://doi.org/10.1093/jac/dkw093
  • El Garch, F., Sauget, M., Hocquet, D., LeChaudee, D., Woehrle, F., Bertrand, X. (2017). mcr-1is borne by highly diverse Escherichia coli isolates since 2004 in food-producing animals in Europe. Clinical Microbiology and Infection, 23(1), 51.e1-51.e4. https://doi.org/10.1016/j.cmi.2016.08.033
  • European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2016). Recomendations for MIC determination colistin (polymixin E) Eucast.org, http://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/General_documents/Recommendations_for_MIC_determination_of_colistin_March_2016.pdf (accessed 29 March 2016).
  • Falgenhauer, L., Waezsada, S-E., Yao, Y., Imirzalioglu, C., Käsbohrer, A., Roesler, U., Michael, G.B., Schwarz, S., Werner, G., Kreienbrock, L., Chakraborty, T. (2016). Colistin resistance gene mcr-1 in extended-spectrum β-lactamase-producing and carbapenemase-producing Gram-negative bacteria in Germany. The Lancet Infectious Diseases, 16(3), 282-283. https://doi.org/10.1016/S1473-3099(16)00009-8
  • Feng, P., Weagant, S.D., Jinneman, K. (2011). BAM: diarrheagenic Escherichia coli. Silver Spring (MD), United States Food and Drug Administration. https://www.fda.gov/food/laboratory-methods-food/bam-diarrheagenic-escherichia-coli (accessed 11/21/2018).
  • Fernandes, M.R., McCulloch, J.A., Vianello, M.A., Moura, Q., Pérez-Chaparro, P.J., Esposito, F., Lincopan, N. (2016). First report of the globally disseminated IncX4 plasmid carrying the mcr-1 gene in a colistin-resistant Escherichia coli sequence type 101 isolate from a human infection in Brazil. Antimicrobial Agents and Chemotherapy, 60, 6415-6417. https://doi.org/10.1128/AAC.01325-16
  • García, V., García-Meniño, I., Mora, A., Flament-Simon, S.C., Díaz-Jiménez, D., Blanco, J.E., Blanco, J. (2018). Co-occurrence of mcr-1, mcr-4 and mcr-5 genes in multidrug-resistant ST10 Enterotoxigenic and Shiga toxin-producing Escherichia coli in Spain (2006-2017). International Journal of Antimicrobial Agents, 52(1), 104-108. https://doi.org/10.1016/j.ijantimicag.2018.03.022
  • Hasman, H., Hammerum, A.M., Hansen, F., Hendriksen, R.S., Olesen, B., Agerso, Y., Zankari, E., Leekitchharoenphon, P., Stegger, M., Kaas, R.S., Cavaco, L.M., Hansen D.S., Aarestrup, F.M., Skov, R.L. (2015). Detection of mcr-1 encoding plasmid mediated colistin resistant Escherischia coli isolates from human bloodstream infection and imported chicken meat, Denmark 2015. Eurosurveillance, 20(49), 1-5. https://doi.org/10.2807/1560-7917.ES.2015.20.49.30085
  • Hernández, M., Iglesias, M.R., Rodríguez-Lázaro, D., Gallardo, A., Quijada, N.M., Miguela-Villoldo, P., Campos, M.J., Píriz, S., López-Orozco, G., de Frutos, C,, Sáez, J.L., Ugarte-Ruiz, M., Domínguez, L., Quesada, A. (2017). Co-occurrence of colistin-resistance genes mcr-1 and mcr-3 among multidrug-resistant Escherichia coli isolated from cattle, Spain, September 2015. Eurosurveillance, 22(31), pii=30586. https://doi.org/10.2807/1560-7917.ES.2017.22.31.30586
  • Hu, Y., Liu, F., Lin, I.Y.C., Gao, G.F., Zhu, B. (2016). Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases, 16(2), 146-147. https://doi.org/10.1016/S1473-3099(15)00533-2
  • Kyere, E.O, Bulut, E., Avşaroğlu, M.D., Soyer, Y. (2015). Molecular evaluation and antimicrobial susceptibility testing of Escherichia coli isolates from food products in Turkey. Food Science and Biotechnology, 24(3), 1001-1009. https://doi.org/10.1007/s10068-015-0128-6
  • Li, A., Yang, Y., Miao, M., Chavda, K.D., Xie, X., Feng, P., Tang, Y. (2016). Complete sequences of mcr-1-Harboring plasmids from extended spectrum b-lactamase and carbapenemase producing Enterobacteriaceae. Antimicrobial Agents and Chemotherapy, 60(7), 4351-4354. https://doi.org/10.1128/AAC.00550-16
  • Li, X.P., Fang, L.X., Jiang, P., Pan, D., Xia, J., Liao, X.P., Sun, J. (2017). Emergence of the colistin resistance gene mcr-1 in Citrobacter freundii. International Journal of Antimicrobial Agents, 49(6), 786-787. https://doi.org/10.1016/j.ijantimicag.2017.04.004
  • Litrup, E., Kiil, K., Hammerum, A.M., Roer, L., Nielsen, E.M., Torpdahl, M. (2017). Plasmid-borne colistin resistance gene mcr-3 in Salmonella isolates from human infections, Denmark, 2009-17. Eurosurveillance, 22(31), pii=30587. https://doi.org/10.2807/1560-7917.ES.2017.22.31.30587
  • Liu, Y.-Y., Wang, Y., Walsh, T.R., Yi, L.X., Zhang, R., Spencer, J., Doi, Y., Tian, G., Dong, B., Huang, X., Yu, L.F., Gu, D., Ren, H., Chen, X., Lv, L., He, D., Zhou, H., Liang, Z., Liu, J.H., 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. The Lancet Infectious Diseases, 16(2), 161-168. https://doi.org/10.1016/S1473-3099(15)00424-7
  • 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. The Lancet Infectious Diseases, 16(3), 283-284. https://doi.org/10.1016/S1473-3099(16)00012-8
  • McGann P, Snesrud E, Maybank R, Corey B, Ong AC, Clifford R, Hinkle M, Whitman T, Lesho E, Schaecher KE. (2016). Escherichia coli harboring mcr-1 and blaCTX-M on a novel IncF plasmid: First report of mcr-1 in the USA. Antimicrobial agents and Chemotherapy, 60(7), 4420-4421. https://doi.org/10.1128/AAC.01103-16
  • Mulvey, M.R., Matajese, L.F., Robertson, J., Nash, J.H.E., Boerlin, P., Toye, B., Irwin, R., Melano, R.G. (2016). Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases, 16(3), 289-290. https://doi.org/10.1016/S1473-3099(16)00067-0
  • Olaitan AO, Chabou S, Okdah L, Morand S, Rolain JM. (2016). Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases, 16(2), 147. https://doi.org/10.1016/S1473-3099(15)00540-X
  • Ordooei, J.A., Shokouhi, S., Sahraei, Z. (2015). A review on colistin nephrotoxicity. European Journal of Clinical Pharmacology, 71(7), 801-810. https://doi.org/10.1007/s00228-015-1865-4
  • 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. Eurosurveillance, 21(6); pii=30135. https://doi.org/10.2807/1560-7917.ES.2016.21.6.30135
  • Prim, N., Rivera, A., Rodríguez-Navarro, J., Español, M., Turbau, M., Coll, P., Mirelis, B. (2016). Detection of mcr-1 colistin resistance gene in polyclonal Escherichia coli isolates in Barcelona, Spain, 2012 to 2015. Eurosurveillance, 21(13), pii=30183. https://doi.org/10.2807/1560-7917.ES.2016.21.13.30183
  • Rebelo, A.R., Bortolaia, V., Kjeldgaard, J.S., Pedersen, S.K., Leekitcharoenphon, P., Hansen, I.M., Battisti, A. (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(6), pii=17-00672. https://doi.org/10.2807/1560-7917.ES.2018.23.6.17-00672
  • Roer, L., Hansen, F., Stegger, M., Sönksen, U.W., Hasman, H., Hammerum, A.M. (2017). Novel mcr-3 variant, encoding mobile colistin resistance, in an ST131 Escherichia coli isolate from bloodstream infection, Denmark, 2014. Eurosurveillance, 22(31), pii=30584. https://doi.org/10.2807/1560-7917.ES.2017.22.31.30584
  • Sennati, S., Di Pilato, V., Riccobono, E., Di Maggio, T., Villagran, A.L., Pallecchi, L., Giani, T. (2017). Citrobacter braakii carrying plasmid-borne mcr-1 colistin resistance gene from ready-to-eat food from a market in the Chaco region of Bolivia. Journal of Antimicrobial Chemotherapy, 72(7), 2127-2129. https://doi.org/10.1093/jac/dkx078
  • Sun, J., Li, X-P., Yang, R-S., Fang, L-X., Huo, W., Li, S-M., Liu, Y-H. (2016). Complete nucleotide sequence of inci2 plasmid co-harboring bla CTX-M-55 and mcr-1. Antimicrobial Agents and Chemotherapy, 60, AAC.00774-16. https://doi.org/10.1128/AAC.00774-16
  • Suzuki, S., Ohnishi, M., Kawanishi, M., Akiba, M., Kuroda, M. (2016). Investigation of a plasmid genome database for colistin-resistance gene mcr-1. The Lancet Infectious Diseases, 16(3), 284-285. https://doi.org/10.1016/S1473-3099(16)00008-6
  • Tang, Y., Dai, L., Sahin, O., Wu, Z., Liu, M., Zhang, Q. (2017). Emergence of a plasmid-borne multidrug resistance gene cfr (C) in foodborne pathogen Campylobacter. Journal of Antimicrobial Chemotherapy, 72(6), 1581-1588. https://doi.org/10.1093/jac/dkx023
  • Tse, H., Yuen, K.Y. (2016). Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases, 16(2), 145-146. https://doi.org/10.1016/S1473-3099(15)00532-0
  • Wang, R., Dorp, L., Shaw, L.P., Bradley, P., Wang, Q., Wang, X., Dorai-Schneiders, T. (2018a). The global distribution and spread of the mobilized colistin resistance gene mcr-1. Nature Communications, 9(1), 1179.https://doi.org/10.1 038/s41467-018-03205-z
  • Wang, X., Wang, Y., Zhou, Y., Li, J., Yin, W., Wang, S., Zhang, S., Shen, J., Wang Y. (2018b). Emergence of a novel mobile colistin resistance gene, mcr-8, in NDM-producing Klebsiella pneumonia. Emerging Microbes & Infections, 7(1), 1-9. https://doi.org/10.1038/s41426-018-0124-z
  • Webb, H.E., Granier, S.A., Marault, M., Millemann, Y., den Bakker, H.C., Nightingale, K.K., Loneragan, G.H. (2016). Dissemination of the mcr-1 colistin resistance gene. The Lancet Infectious Diseases, 16(2), 144-145. https://doi.org/10.1016/S1473-3099(15)00538-1
  • Xavier, B.B., Lammens, C., Ruhal, R., Kumar-Singh, S., Butaye, P., Goossens, H., Malhotra-Kumar, S. (2016). Identification of a novel plasmid-mediated colistin-resistance gene, mcr-2, in Escherichia coli, Belgium, June 2016. Eurosurveillance, 21(27), pii=30280. https://doi.org/10.2807/1560-7917.ES.2016.21.27.30280
  • Yang, Y.Q., Li, Y.X., Lei, C.W., Zhang, A,Y., Wang, H.N. (2018). Novel plasmid-mediated colistin resistance gene mcr-7.1 in Klebsiella pneumoniae. Journal of Antimicrobial Chemotherapy, 73(7), 1791-1795. https://doi.org/10.1093/jac/dky111
  • Yang, Y.Q., Zhang, A.Y., Ma, S,Z., Kong, L.H., Li, Y. X., Liu, J.X., Wang, H.N. (2016). Co-occurrence of mcr-1 and ESBL on a single plasmid in Salmonella enterica. Journal of Antimicrobial Chemotherapy, 71(8), 2336-2338.https://doi.org/10.1093/jac/dkw243
  • Yao, X., Doi, Y., Zeng, L., Lv, L., Liu, J.H. (2016). Carbapenem-resistant and colistin-resistant Escherichia coli co-producing NDM-9 and mcr-1. The Lancet Infectious Diseases, 16(3), 288-289. https://doi.org/10.1016/S1473-3099(16)00057-8
  • Ye, H., Li, Y., Li, Z., Gao, R., Zhang, H., Wen, R., Gao, G.F., Hu, Q., Feng, Y. (2016). Diversified mcr-1 harbouring plasmid reservoirs confer resistance to colistin in human gut microbiota. mBio, 7(2), e00177-16. https://doi.org/10.1128/mBio.00177-16
  • Yin, W., Li, H., Shen, Y., Liu, Z., Wang, S., Shen, Z., Wang, Y. (2017). Novel plasmid-mediated colistin resistance gene mcr-3 in Escherichia coli. mBio, 8(3), e00543-17. https://doi.org/10.1128/mBio.00543-17 Zeng, K-J., Doi, Y., Pati,l S., Huang, X., Tian, G-B. (2016). Emergence of the plasmid-mediated mcr-1 gene in colistin-resistant Enterobacter aerogenes and Enterobacter cloacae. Antimicrobial Agents Chemotherapy, 60, 3862-3863. https://doi.org/10.1128/AAC.00345-16
  • Zurfuh, K., Poirel, L., Nordmann, P. (2016). Occurrence of the plasmid-borne mcr-1 colistin resistance gene in ESBL-producing Enterobacteriaceae in river water and imported vegetable samples in Switzerland. Antimicrobial Agents and Chemotherapy, 60(4), 2594-2595. https://doi.org/10.1128/AAC.00066-16

Details

Primary Language en
Subjects Food Science and Technology
Journal Section Research Articles
Authors

Orcid: 0000-0002-4750-7488
Author: Mustafa GUZEL
Institution: Hitit University, Faculty of Engineering, Department of Food Engineering
Country: Turkey

Orcid: 0000-0002-3106-9206
Author: M. Dilek AVSAROGLU
Institution: Ahi Evran University, Faculty of Agriculture, Department of Agricultural Biotechnology
Country: Turkey

Orcid: 0000-0001-9687-9715
Author: Yeşim SOYER (Primary Author)
Institution: Middle East Technical University, Faculty of Engineering, Department of Food Engineering
Country: Turkey
Dates

Application Date : November 15, 2019
Acceptance Date : March 7, 2020
Publication Date : May 16, 2020

Cite

Bibtex @research article { jfhs647371, journal = {Food and Health}, issn = {}, eissn = {2602-2834}, address = {Vidin Caddesi No:28 D:4 Kocamustafapaşa 34107 Fatih İstanbul}, publisher = {Özkan ÖZDEN}, year = {2020}, volume = {6}, pages = {160 - 169}, doi = {}, title = {Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015}, key = {cite}, author = {Guzel, Mustafa and Avsaroglu, M. Dilek and Soyer, Yeşim} }
APA Guzel, M , Avsaroglu, M , Soyer, Y . (2020). Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015 . Food and Health , 6 (3) , 160-169 . Retrieved from http://jfhs.scientificwebjournals.com/en/pub/issue/53118/647371
MLA Guzel, M , Avsaroglu, M , Soyer, Y . "Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015" . Food and Health 6 (2020 ): 160-169 <http://jfhs.scientificwebjournals.com/en/pub/issue/53118/647371>
Chicago Guzel, M , Avsaroglu, M , Soyer, Y . "Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015". Food and Health 6 (2020 ): 160-169
RIS TY - JOUR T1 - Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015 AU - Mustafa Guzel , M. Dilek Avsaroglu , Yeşim Soyer Y1 - 2020 PY - 2020 N1 - DO - T2 - Food and Health JF - Journal JO - JOR SP - 160 EP - 169 VL - 6 IS - 3 SN - -2602-2834 M3 - UR - Y2 - 2020 ER -
EndNote %0 Food and Health Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015 %A Mustafa Guzel , M. Dilek Avsaroglu , Yeşim Soyer %T Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015 %D 2020 %J Food and Health %P -2602-2834 %V 6 %N 3 %R %U
ISNAD Guzel, Mustafa , Avsaroglu, M. Dilek , Soyer, Yeşim . "Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015". Food and Health 6 / 3 (May 2020): 160-169 .
AMA Guzel M , Avsaroglu M , Soyer Y . Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015. Food Health. 2020; 6(3): 160-169.
Vancouver Guzel M , Avsaroglu M , Soyer Y . Determination of colistin resistance in Escherichia coli isolates from foods in Turkey, 2011-2015. Food and Health. 2020; 6(3): 160-169.
Authors of the Article
Mustafa GUZEL [1]
M. Dilek AVSAROGLU [2]
Yeşim SOYER [3]
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