Predominance of CTX-M-15 among ESBL producers from environment and fish gut from the shores of Lake Victoria in Mwanza, Tanzania

Frontiers in Microbiology

Volumn 7, Issue DEC, 2016, Pages

  Moremi, Nyambura ^a   Manda, Elizabeth V ^a   Falgenhauer, Linda ^b,c   Ghosh, Hiren ^b,c   Imirzalioglu, Can ^b,c   Matee, Mecky ^d   Chakraborty, Trinad ^b,c   Mshana, Stephen E ^a  

^a WEILL BUGANDO SCHOOL OF MEDICINE   (Tanzania)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL MARBURG   (Germany)

^d MUHIMBILI UNIVERSITY OF HEALTH AND ALLIED SCIENCES   (Tanzania)

Author keywords

BlaCTX M 15; Environment; Fish

Indexed keywords

BETA LACTAMASE AMPC; BETA LACTAMASE CTX M; EXTENDED SPECTRUM BETA LACTAMASE; QUINOLONE DERIVATIVE; SULFONAMIDE; TETRACYCLINE DERIVATIVE; TRIMETHOPRIM;

ANTIBIOTIC RESISTANCE; ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIUM CONTAMINATION; CONTROLLED STUDY; ENVIRONMENTAL SANITATION; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ENTEROBACTERIACEAE; GENE MUTATION; GENE SEQUENCE; INTESTINE FLORA; LAKE ECOSYSTEM; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PLASMID; SEWAGE; WHOLE GENOME SEQUENCING;

EID: 85009168560     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.01862     Document Type: Article

References (49)

1. Abgottspon, H., Nüesch-Inderbinen, M. T., Zurfluh, K., Althaus, D., Hächler, H., and Stephan, R. (2014). Enterobacteriaceae with extended-spectrum-and pAmpC-type β-lactamase-encoding genes isolated from freshwater fish from two lakes in Switzerland. Antimicrob. Agents Chemother. 58, 2482-2484. doi: 10.1128/AAC.02689-13
2. Ahmed, A. M., and Shimamoto, T. (2008). Emergence of a cefepime-and cefpirome-resistant Citrobacter freundii clinical isolate harbouring a novel chromosomally encoded AmpC β-lactamase, CMY-37. Int. J. Antimicrob. Agents 32, 256-261. doi: 10.1016/j.ijantimicag.2008.04.019
3. Ahmed, S. A., Awosika, J., Baldwin, C., Bishop-Lilly, K. A., Biswas, B., Broomall, S., et al. (2012). Genomic comparison of Escherichia coli O104: H4 isolates from 2009 and 2011 reveals plasmid, and prophage heterogeneity, including shiga toxin encoding phage stx2. PLoS ONE 7:e48228. doi: 10.1371/journal.pone.0048228
4. Alikhan, N. F., Petty, N. K., Zakour, N. L. B., and Beatson, S. A. (2011). BLAST Ring Image Generator (BRIG): simple prokaryote genome comparisons. BMC Genomics 12:402. doi: 10.1186/1471-2164-12-402
5. Arpin, C., Dubois, V., Maugein, J., Jullin, J., Dutilh, B., Brochet, J.-P., et al. (2005). Clinical and molecular analysis of extended-spectrum β-lactamase-producing enterobacteria in the community setting. J. Clin. Microbiol. 43, 5048-5054. doi: 10.1128/JCM.43.10.5048-5054.2005
6. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A. A., Dvorkin, M., Kulikov, A. S., et al. (2012). SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19, 455-477. doi: 10.1089/cmb.2012.0021
7. Beninati, C., Reich, F., Muscolino, D., Giarratana, F., Panebianco, A., Klein, G., et al. (2015). ESBL-producing bacteria and MRSA isolated from poultry and Turkey products imported from Italy. Czech J. Food Sci. 33, 97-102. doi: 10.17221/428/2014-CJFS
8. Blaak, H., de Kruijf, P., Hamidjaja, R. A., van Hoek, A. H., de Roda Husman, A. M., and Schets, F. M. (2014). Prevalence and characteristics of ESBL-producing E. coli in Dutch recreational waters influenced by wastewater treatment plants. Vet. Microbiol. 171, 448-459. doi: 10.1016/j.vetmic.2014.03.007
9. Carattoli, A., Zankari, E., García-Fernández, A., Larsen, M., Lund, O., Villa, L., et al. (2014). In silico detection and typing of plasmids using PlasmidFinder and plasmid multilocus sequence typing. Antimicrob. Agents Chemother. 58, 3895-3903. doi: 10.1128/AAC.02412-14
10. Cheng, A. C., Mcdonald, J. R., and Thielman, N. M. (2005). Infectious diarrhea in developed and developing countries. J. Clin. Gastroenterol. 39, 757-773. doi: 10.1097/01.mcg.0000177231.13770.07
11. Clermont, O., Bonacorsi, S., Bingen, E., and Bonacorsi, P. (2000). Rapid and simple determination of the Escherichia coli phylogenetic. Appl. Environ. Microbiol. 66, 4555-4558. doi: 10.1128/AEM.66.10.4555-4558.2000
12. Dobiasova, H., Videnska, P., and Dolejska, M. (2015). Complete sequences of IncU plasmids harboring quinolone resistance genes qnrS2 and aac(6')-Ib-cr in Aeromonas spp. from ornamental fish. Antimicrob. Agents Chemother. 60, 653-657. doi: 10.1128/AAC.01773-15
13. Dos Santos, G., Solidônio, E., Costa, M., Melo, R., De Souza, I., Silva, G., et al. (2015). "Study of the Enterobacteriaceae group CESP (Citrobacter, Enterobacter, Serratia, Providencia, Morganella and Hafnia): a review, " in The Battle Against Microbial Pathogens: Basic Science, Technological Advances and Educational Programs, ed A. Méndez-Vilas (Badajoz: Formatex), 794-805.
14. Falgenhauer, L., Yao, Y., Fritzenwanker, M., Schmiedel, J., Imirzalioglu, C., and Chakraborty, T. (2014). Complete genome sequence of phage-like plasmid pECOH89, Encoding CTX-M-15. Genome Announc. 2:e00356-14. doi: 10.1128/genomea.00356-14
15. Fitzpatrick, M., Butler, S., Ham, A., and Hardy, P. (2015). Lonely Planet Tanzania Travel Guide. Oakland, CA: Amazon.
16. Fortini, D., Fashae, K., Villa, L., Feudi, C., García-Fernández, A., and Carattoli, A. (2015). A novel plasmid carrying blaCTX-M-15 identified in commensal Escherichia coli from healthy pregnant women in Ibadan, Nigeria. J. Glob. Antimicrob. Resist. 3, 9-12. doi: 10.1016/j.jgar.2014.12.002
17. Guenther, S., Ewers, C., and Wieler, L. H. (2011). Extended-spectrum beta-lactamases producing E. coli in wildlife, yet another form of environmental pollution? Front. Microbiol. 2:246. doi: 10.3389/fmicb.2011.00246
18. Hawkey, P. M., and Jones, A. M. (2009). The changing epidemiology of resistance. J. Antimicrob. Chemother. 64, i3-i10. doi: 10.1093/jac/dkp256
19. Ho, P.-L., Chow, K., Lai, E. L., Lo, W. U., Yeung, M., Chan, J., et al. (2011). Extensive dissemination of CTX-M-producing Escherichia coli with multidrug resistance to 'critically important' antibiotics among food animals in Hong Kong, 2008-10. J. Antimicrob. Chemother. 66, 765-768. doi: 10.1093/jac/dkq539
20. Ibrahim, H. M. M., Ahmed, A. M., El-Seedy, Y. Y., and El-Khodery, S. A. (2015). Distribution of multidrug-resistant gram negative bacteria causing clinical mastitis in dairy Cows. Glob. Vet. 15, 268-277. doi: 10.5829/idosi.gv.2015.15.03.1012
21. Ishida, Y., Ahmed, A. M., Mahfouz, N. B., Kimura, T., El-Khodery, S. A., Moawad, A. A., et al. (2010). Molecular analysis of antimicrobial resistance in Gram-negative bacteria isolated from fish farms in Egypt. J. Vet. Med. Sci. 72, 727-734. doi: 10.1292/jvms.09-0538
22. Jiang, H.-X., Tang, D., Liu, Y.-H., Zhang, X.-H., Zeng, Z.-L., Xu, L., et al. (2012). Prevalence and characteristics of β-lactamase and plasmid-mediated quinolone resistance genes in Escherichia coli isolated from farmed fish in China. J. Antimicrob. Chemother. 67, 2350-2353. doi: 10.1093/jac/dks250
23. Kayange, N., Kamugisha, E., Mwizamholya, D. L., Jeremiah, S., and Mshana, S. E. (2010). Predictors of positive blood culture and deaths among neonates with suspected neonatal sepsis in a tertiary hospital, Mwanza-Tanzania. BMC Pediatr. 10:39. doi: 10.1186/1471-2431-10-39
24. Kümmerer, K. (2009). Antibiotics in the aquatic environment-a review-part I. Chemosphere 75, 417-434. doi: 10.1016/j.chemosphere.2008.11.086
25. Larsen, M. V., Cosentino, S., Rasmussen, S., Friis, C., Hasman, H., Marvig, R. L., et al. (2012). Multilocus sequence typing of total-genome-sequenced bacteria. J. Clin. Microbiol. 50, 1355-1361. doi: 10.1128/JCM.06094-11
26. Laube, H., Friese, A., von Salviati, C., Guerra, B., Käsbohrer, A., Kreienbrock, L., et al. (2013). Longitudinal monitoring of extended-spectrum-beta-lactamase/AmpC-producing Escherichia coli at German broiler chicken fattening farms. Appl. Environ. Microbiol. 79, 4815-4820. doi: 10.1128/AEM.00856-13
27. Liu, B. T., Liao, X. P., Yang, S. S., Wang, X. M., Li, L. L., Sun, J., et al. (2012). Detection of mutations in the gyrA and parC genes in Escherichia coli isolates carrying plasmid-mediated quinolone resistance genes from diseased food-producing animals. J. Med. Microbiol. 61, 1591-1599. doi: 10.1099/jmm.0.043307-0
28. Madec, J.-Y., Poirel, L., Saras, E., Gourguechon, A., Girlich, D., Nordmann, P., et al. (2012). Non-ST131 Escherichia coli from cattle harbouring human-like blaCTX-M-15-carrying plasmids. J. Antimicrob. Chemother. 67, 578-581. doi: 10.1093/jac/dkr542
29. Martinez, J. L. (2009a). Environmental pollution by antibiotics and by antibiotic resistance determinants. Environ. Pollut. 157, 2893-2902. doi: 10.1016/j.envpol.2009.05.051
30. Martinez, J. L. (2009b). The role of natural environments in the evolution of resistance traits in pathogenic bacteria. Proc. R. Soc. Lond. B Biol. Sci. 276, 2521-2530. doi: 10.1098/rspb.2009.0320
31. Moremi, N., Mushi, M. F., Fidelis, M., Chalya, P., Mirambo, M., and Mshana, S. E. (2014). Predominance of multi-resistant gram-negative bacteria colonizing chronic lower limb ulcers (CLLUs) at Bugando Medical Center. BMC Res. Notes 7:211. doi: 10.1186/1756-0500-7-211
32. Mshana, S. E., Falgenhauer, L., Mirambo, M. M., Mushi, M. F., Moremi, N., Julius, R., et al. (2016). Predictors of bl a CTX-M-15 in varieties of Escherichia coli genotypes from humans in community settings in Mwanza, Tanzania. BMC Infect. Dis. 16:187. doi: 10.1186/s12879-016-1527-x
33. Mshana, S. E., Hain, T., Domann, E., Lyamuya, E. F., Chakraborty, T., and Imirzalioglu, C. (2013). Predominance of Klebsiella pneumoniae ST14 carrying CTX-M-15 causing neonatal sepsis in Tanzania. BMC Infect. Dis. 13:466. doi: 10.1186/1471-2334-13-466
34. Mshana, S. E., Kamugisha, E., Mirambo, M., Chakraborty, T., and Lyamuya, E. F. (2009). Prevalence of multiresistant gram-negative organisms in a tertiary hospital in Mwanza, Tanzania. BMC Res. Notes 2:49. doi: 10.1186/1756-0500-2-49
35. Mshana, S., Imirzalioglu, C., Hain, T., Domann, E., Lyamuya, E. F., and Chakraborty, T. (2011). Multiple ST clonal complexes, with a predominance of ST131, of Escherichia coli harbouring blaCTX-M-15 in a tertiary hospital in Tanzania. Clin. Microbiol. Infect. 17, 1279-1282. doi: 10.1111/j.1469-0691.2011.03518.x
36. Murray, P. R., Baron, E. J., Pfaller, M., Tenover, F., Yolken, R. H., and Morgan, D. R. (1995). Manual of clinical microbiology (6th edn). Trends Microbiol. 3, 449-449.
37. Pitout, J. D., Nordmann, P., Laupland, K. B., and Poirel, L. (2005). Emergence of Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs) in the community. J. Antimicrob. Chemother. 56, 52-59. doi: 10.1093/jac/dki166
38. Rafaï, C., Frank, T., Manirakiza, A., Gaudeuille, A., Mbecko, J. R., Nghario, L., et al. (2015). Dissemination of IncF-type plasmids in multiresistant CTX-M-15-producing Enterobacteriaceae isolates from surgical-site infections in Bangui, Central African Republic. BMC Microbiol. 15:15. doi: 10.1186/s12866-015-0348-1
39. Rissman, A. I., Mau, B., Biehl, B. S., Darling, A. E., Glasner, J. D., and Perna, N. T. (2009). Reordering contigs of draft genomes using the Mauve aligner. Bioinformatics 25, 2071-2073. doi: 10.1093/bioinformatics/btp356
40. Seni, J., Falgenhauer, L., Simeo, N., Mirambo, M. M., Imirzalioglu, C., Matee, M., et al. (2016). Multiple ESBL-producing Escherichia coli sequence types carrying quinolone and aminoglycoside resistance genes circulating in companion and domestic farm animals in Mwanza, Tanzania, harbor commonly occurring plasmids Front. Microbiol. 7:142. doi: 10.3389/fmicb.2016.00142
41. Treangen, T. J., Ondov, B. D., Koren, S., and Phillippy, A. M. (2014). The Harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol. 15:524. doi: 10.1186/s13059-014-0524-x
42. van Hoek, A. H., Veenman, C., van Overbeek, W. M., Lynch, G., de Roda Husman, A. M., and Blaak, H. (2015). Prevalence and characterization of ESBL-and AmpC-producing Enterobacteriaceae on retail vegetables. Int. J. Food Microbiol. 204, 1-8. doi: 10.1016/j.ijfoodmicro.2015.03.014
43. Wayne, P. (2012). Performance Standards for Antimicrobial Susceptibility Testing: Twenty-Second Informational Supplement. Clinical and Laboratory Standards Institute. M100-S22. USA.
44. Weigel, L. M., Steward, C. D., and Tenover, F. C. (1998). gyrA mutations associated with fluoroquinolone resistance in eight species of Enterobacteriaceae. Antimicrob. Agents Chemother. 42, 2661-2667.
45. Welch, T. J., Evenhuis, J., White, D. G., Mcdermott, P. F., Harbottle, H., Miller, R. A., et al. (2009). IncA/C plasmid-mediated florfenicol resistance in the catfish pathogen Edwardsiella ictaluri. Antimicrob. Agents Chemother. 53, 845-846. doi: 10.1128/AAC.01312-08
46. Xi, M., Wu, Q., Wang, X., Yang, B., Xia, X., and Li, D. (2015). Characterization of extended-spectrum β-lactamase-producing Escherichia coli strains isolated from retail foods in Shaanxi Province, China. J. Food Prot.78, 1018-1023. doi: 10.4315/0362-028X.JFP-14-490
47. Zankari, E., Hasman, H., Cosentino, S., Vestergaard, M., Rasmussen, S., Lund, O., et al. (2012). Identification of acquired antimicrobial resistance genes. J. Antimicrob. Chemother. 67, 2640-2644. doi: 10.1093/jac/dks261
48. Zhang, L., Lü, X., and Zong, Z. (2013). The emergence of blaCTX-M-15-carrying Escherichia coli of ST131 and new sequence types in Western China. Ann. Clin. Microbiol. Antimicrob. 12:35. doi: 10.1186/1476-0711-12-35
49. Zurfluh, K., Hächler, H., Nüesch-Inderbinen, M., and Stephan, R. (2013). Characteristics of extended-spectrum β-lactamase-and carbapenemase-producing Enterobacteriaceae isolates from rivers and lakes in Switzerland. Appl. Environ. Microbiol. 79, 3021-3026. doi: 10.1128/AEM.00054-13