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

Frontiers in Microbiology

Volumn 7, Issue FEB, 2016, Pages

  Seni, Jeremiah ^a   Falgenhauer, Linda ^b,c   Simeo, Nabina ^a   Mirambo, Mariam M ^a   Imirzalioglu, Can ^b,c   Matee, Mecky ^d   Rweyemamu, Mark ^e   Chakraborty, Trinad ^b,c   Mshana, Stephen E ^a  

^a CATHOLIC UNIVERSITY OF HEALTH AND ALLIED SCIENCES   (Tanzania)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY HOSPITAL MARBURG   (Germany)

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

^e SOKOINE UNIVERSITY OF AGRICULTURE   (Tanzania)

Author keywords

Companion animals; Domestic farm animals; ESBL; Farming communities; Mwanza; Tanzania

Indexed keywords

AMINOGLYCOSIDE; CEFOTAXIME; CEFTRIAXONE; CIPROFLOXACIN; COTRIMOXAZOLE; GENTAMICIN; QUINOLONE; TETRACYCLINE;

ANIMAL DISEASE; ANIMAL EXPERIMENT; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL GENE; BACTERIUM IDENTIFICATION; COMPUTER MODEL; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; DOG; ESCHERICHIA COLI INFECTION; EXTENDED SPECTRUM BETA LACTAMASE PRODUCING ESCHERICHIA COLI; FEMALE; GENE FREQUENCY; KLEBSIELLA; MALE; MINIMUM INHIBITORY CONCENTRATION; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PHYLOGENETIC TREE; PIG; PLASMID; PROTEUS; TANZANIA;

EID: 84962159647     PISSN: None     EISSN: 1664302X     Source Type: Journal    
DOI: 10.3389/fmicb.2016.00142     Document Type: Article

References (34)

1. Aibinu, I., Odugbemi, T., Koenig, W., and Ghebremedhin, B. (2012). Sequence type ST131 and ST10 complex (ST617) predominant among CTX-M-15-producing Escherichia coli isolates from Nigeria. Clin. Microbiol. Infect. 18, E49-E51. doi: 10.1111/j.1469-0691.2011.03730.x
2. Alikhan, N.-F., Petty, N. K., Ben Zakour, N. L., 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
3. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
4. 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
5. Bester, L. A., and Essack, S. Y. (2008). Prevalence of antibiotic resistance in Campylobacter isolates from commercial poultry suppliers in KwaZulu-Natal, South Africa. J. Antimicrob. Chemother. 62, 1298-1300. doi: 10.1093/jac/dkn408
6. Bradford, P. A. (2001). Extended-spectrum beta-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clin. Microbiol. Rev. 14, 933-951. doi: 10.1128/CMR.14.4.933-951.2001
7. Carattoli, A., Zankari, E., García-Fernández, A., Voldby 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
8. Clermont, O., Bonacorsi, S., Bingen, E., and Bonacorsi, P. (2000). Rapid and Simple Determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 66, 4555-4558. doi: 10.1128/AEM.66.10.4555-4558.2000.Updated
9. Clinical Laboratory Standards Institute [CLSI] (2011). Performance Standards for Antimicrobial Susceptibility Testing: Twenty-first Informational Supplement. Document M100-S21s. Wayne, PA: Clinical and Laboratory Standards Institute.
10. Darling, A. C. E., Mau, B., Blattner, F. R., and Perna, N. T. (2004). Mauve: multiple alignment of conserved genomic sequence with rearrangements. Genome Res. 14, 1394-1403. doi: 10.1101/gr.2289704
11. Dierikx, C. M., van Duijkeren, E., Schoormans, A. H. W., van Essen-Zandbergen, A., Veldman, K., Kant, A., et al. (2012). Occurrence and characteristics of extended-spectrum-β-lactamase-and AmpC-producing clinical isolates derived from companion animals and horses. J. Antimicrob. Chemother. 67, 1368-1374. doi: 10.1093/jac/dks049
12. Ewers, C., Bethe, A., Semmler, T., Guenther, S., and Wieler, L. H. (2012). Extended-spectrum β-lactamase-producing and AmpC-producing Escherichia coli from livestock and companion animals, and their putative impact on public health: a global perspective. Clin. Microbiol. Infect. 18, 646-655. doi: 10.1111/j.1469-0691.2012.03850.x
13. Fam, N., Leflon-Guibout, V., Fouad, S., Aboul-Fadl, L., Marcon, E., Desouky, D., et al. (2011). CTX-M-15-producing Escherichia coli clinical isolates in Cairo (Egypt), including isolates of clonal complex ST10 and clones ST131, ST73, and ST405 in both community and hospital settings. Microbiol. Drug Resist. 17, 67-73. doi: 10.1089/mdr.2010.0063
14. 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
15. Geser, N., Stephan, R., and Hächler, H. (2012). Occurrence and characteristics of extended-spectrum β-lactamase (ESBL) producing Enterobacteriaceae in food producing animals, minced meat and raw milk. BMC Vet. Res. 8:21. doi: 10.1186/1746-6148-8-21
16. Hall, B. G. (2013). Building phylogenetic trees from molecular data with MEGA. Mol. Biol. Evol. 30, 1229-1235. doi: 10.1093/molbev/mst012
17. Hawkey, P. M., and Jones, A. M. (2009). The changing epidemiology of resistance. J. Antimicrob. Chemother. 64(Suppl. 1), i3-i10. doi: 10.1093/jac/dkp256
18. Katakweba, A. A. S. (2014). Prevalence of Antimicrobial Resistance and Characterization of Fecal Indicator Bacteria and Staphylococcus Aureus from Farm Animals, Wildlife, Pets and Humans in Tanzania, thesis Collection, Sokoine University of Agriculture, Morogoro.
19. 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
20. Koneman, E. W., Allen, S. D., Janda, W. M., and Schreckenberger, P. C. (1997). Color Atlas and Textbook of Diagnostic Microbiology. Washington, DC: Lippincott Williams & Wilkins.
21. 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
22. Li, J.-J., Spychala, C. N., Hu, F., Sheng, J.-F., and Doi, Y. (2015). Complete nucleotide sequences of bla(CTX-M)-harboring IncF plasmids from community-associated Escherichia coli strains in the United States. Antimicrob. Agents Chemother. 59, 3002-3007. doi: 10.1128/AAC.04772-14
23. Lupindu, A. M., Olsen, J. E., Ngowi, H. A., Msoffe, P. L. M., Mtambo, M. M., Scheutz, F., et al. (2014). Occurrence and characterization of Shiga toxin-producing Escherichia coli O157:H7 and other non-sorbitol-fermenting E. coli in cattle and humans in urban areas of Morogoro, Tanzania. Vector Borne Zoonotic Dis. 14, 503-510. doi: 10.1089/vbz.2013.1502
24. Madec, J.-Y., Lazizzera, C., Châtre, P., Meunier, D., Martin, S., Lepage, G., et al. (2008). Prevalence of fecal carriage of acquired expanded-spectrum cephalosporin resistance in Enterobacteriaceae strains from cattle in France. J. Clin. Microbiol. 46, 1566-1567. doi: 10.1128/JCM.02299-07
25. Mshana, S. E., Gerwing, L., Minde, M., Hain, T., Domann, E., Lyamuya, E., et al. (2011a). Outbreak of a novel Enterobacter sp. carrying blaCTX-M-15 in a neonatal unit of a tertiary care hospital in Tanzania. Int. J. Antimicrob. Agents 38, 265-269. doi: 10.1016/j.ijantimicag.2011.05.009
26. Mshana, S. E., Imirzalioglu, C., Hain, T., Domann, E., Lyamuya, E. F., and Chakraborty, T. (2011b). 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
27. Munang'andu, H. M., Kabilika, S. H., Chibomba, O., Munyeme, M., and Muuka, G. M. (2012). Bacteria isolations from broiler and layer chicks in zambia. J. Pathog. 2012:520564. doi: 10.1155/2012/520564
28. Nelson, E., Kayega, J., Seni, J., Mushi, M. F., Kidenya, B. R., Hokororo, A., et al. (2014). Evaluation of existence and transmission of extended spectrum beta lactamase producing bacteria from post-delivery women to neonates at Bugando Medical Center, Mwanza-Tanzania. BMC Res. 7:279. doi: 10.1186/1756-0500-7-279
29. 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. 15:341.
30. Rubin, J. E., and Pitout, J. D. D. (2014). Extended-spectrum β-lactamase, carbapenemase and AmpC producing Enterobacteriaceae in companion animals. Vet. Microbiol. 170, 10-18. doi: 10.1016/j.vetmic.2014.01.017
31. Sallem, R., Ben Slama, K., Ben Estepa, V., Cheikhna, E. O., Mohamed, A. M., Chairat, S., et al. (2015). Detection of CTX-M-15-producing Escherichia coli isolates of lineages ST410-A, ST617-A and ST354-D in faecal samples of hospitalized patients in a Mauritanian hospital. J. Chemother. 27, 114-116. doi: 10.1179/1973947814Y.0000000172
32. 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
33. Wirth, T., Falush, D., Lan, R., Colles, F., Mensa, P., Wieler, L. H., et al. (2006). Sex and virulence in Escherichia coli: an evolutionary perspective. Mol. Microbiol. 60, 1136-1151. doi: 10.1111/j.1365-2958.2006.05172.x
34. 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