1. bookVolume 71 (2021): Issue 4 (December 2021)
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
access type Open Access

Characterisation of AmpC / ESBL genes in some pathogen gram-negatives isolated from clinical cases of livestock and companion animals

Published Online: 30 Dec 2021
Volume & Issue: Volume 71 (2021) - Issue 4 (December 2021)
Page range: 435 - 450
Accepted: 14 Oct 2021
Journal Details
License
Format
Journal
eISSN
1820-7448
First Published
25 Mar 2014
Publication timeframe
4 times per year
Languages
English
Abstract

This study was aimed to search and characterize the AmpC and/or ESBL genes of Escherichia coli, Klebsiella pneumoniae and Pseudomonas aeruginosa isolated from clinical cases of local livestock and companion animals between 2017 and 2019. A total of eight ceftiofur-resistant E. coli (n= 7) and ceftiofur-resistant K. pneumoniae (n= 1) and seven P. aeruginosa were isolated from different cases in local animals. By combination disc method, six E. coli isolates and one K. pneumoniae isolate were found to be ESBL producers. By combination of the disc method and double disc synergy test, no P. aeruginosa isolates were found as ESBL producers. In the agar disc diffusion test (ADDT) performed with cefoxitin and cefoxitin-boronic, only one E. coli was determined as AmpC producer. In ESBL-producing isolates, only the CTX-M class gene was detected by polymerase chain reaction (PCR) and subsequent sequence analysis revealed CTX-M-3 and CTX-M-15 variants. An AmpC positive E. coli isolate was found to carry plasmidic ampC gene in cmy-2 variant from CIT family. It was observed that P. aeruginosa isolates did not carry the plasmidic ampC gene. After the chromosomal ampC gene of one P. aeruginosa was amplified by PCR and sequenced, R79Q and T105A mutations in the chromosomal ampC gene was revealed. This showed that overproduction of the ampC enzyme is involved in the resistance to β-lactams in P. aeruginosa isolates in the study.

Keywords

1. Bradford PA: Extended-spectrum β-lactamases in the 21th century: Characterisation, epidemiology, and detection of this important resistance threat. Clin Microbiol Rev 2001, 14: 933-951.10.1128/CMR.14.4.933-951.20018900911585791 Search in Google Scholar

2. Jacoby GA: AmpC β-lactamases. Clin Microbiol Rev 2009, 22 (1): 161-182.10.1128/CMR.00036-08262063719136439 Search in Google Scholar

3. Philippon A, Arlet G, Jacoby GA: Plasmid-determined AmpC-type β-lactamases. Antimicrob Agents Chemother 2002, 46(1): 1-11.10.1128/AAC.46.1.1-11.200212699311751104 Search in Google Scholar

4. Sadeeq R, Tariq A, Ijaz A, Nazir AK, Bo H, Jian G: The growing genetic and functional diversity of extended spectrum beta lactamases. Biomed Res Int 2018, March 26: 9519718.10.1155/2018/9519718589227029780833 Search in Google Scholar

5. Perez-Perez FJ, Hanson ND: Detection of plasmid-mediated AmpC β-lactamase genes in clinical isolates by using multiplex PCR. J Clin Microbiol 2002, 40: 2153-2162.10.1128/JCM.40.6.2153-2162.200213080412037080 Search in Google Scholar

6. Poole K: Pseudomonas aeruginosa: Resistance to the max. Front Microbiol 2011 (April 5), 2: 65.10.3389/fmicb.2011.00065312897621747788 Search in Google Scholar

7. Berrazeg M, Jeannot K, Ntsogo Enguéné VY, Broutin I, Loeffert S, Fournier D, Plésiat P: Mutations in β-lactamase AmpC increase resistance of Pseudomonas aeruginosa isolates to antipseudomonal cephalosporins. Antimicrob Agents Chemother 2015, 59: 6248-6255.10.1128/AAC.00825-15457605826248364 Search in Google Scholar

8. Paterson DL: Recommendation for treatment of severe infections caused by Enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs). Clin Microbiol Infect 2000, 6: 460-463.10.1046/j.1469-0691.2000.00107.x11168179 Search in Google Scholar

9. Ali T, ur Rahman S, Zhang L, Shahid M, Zhang S, Liu G, Gao J, Han B: ESBL-producing Escherichia coli from cows suffering mastitis in China contain clinical class 1 integrons with CTX-M linked to ISCR1. Front Microbiol 2016, 7: 1931.10.3389/fmicb.2016.01931512780827965653 Search in Google Scholar

10. Saidani M, Messadi L, Soudani A, Daaloul-Jedidi M, Chatre P, Chehida FB, Mamlouk A, Mahjoub W, Madec J-Y, Haenni M: Epidemiology, antimicrobial resistance, and entended-spectrum β-lactamase-producing Enterobacterales in clinical bovine mastitis in Tunisa. Microb Drug Resist 2018, 24 (8): 1242-1248.10.1089/mdr.2018.004929757079 Search in Google Scholar

11. Ghatak S, Singha A, Sen A, Guha C, Ahuja A, Bhattacharjee U, Das S, Pradhan NR, Puro K, Jana C, Dey TK, Prashantkumar KL, Das A, Shakuntala I, Biswas U, Jana PS: Detection of New Delhi Metallo-β-lactamase and extended-spectrum β-lactamase genes in Escherichia coli isolated from mastitic milk samples. Transbound Emerg Dis 2013, 60: 385-389.10.1111/tbed.1211923870003 Search in Google Scholar

12. Timofte D, Maciuca IE, Evans NJ, Williams H, Wattret A, Fick JC, Willams NJ: Detection and molecular characterisation of Escherichia coli CTX-M-15 and Klebsiella pneumoniae SHV-12 β lactamases from bovine mastitis isolates in the United Kingdom. Antimicrob Agents Chemother 2014, 58 (2): 789-794.10.1128/AAC.00752-13391087324247146 Search in Google Scholar

13. Eisenberger D, Carl A, Balsliemke J, Kampf P, Nickel S, Schulze G, Valenza G: Molecular characterisation of extended-spectrum β-lactamase-producing Escherichia coli isolates from milk samples of dairy cows with mastitis in Bavaria, Germany. Microb Drug Resist 2018, 24 (4): 505-510.10.1089/mdr.2017.018228953418 Search in Google Scholar

14. Pehlivanoglu F, Turutoglu H, Ozturk D: CTX-M-15-type extended-spectrum β-lactamase-producing Escherichia coli as causative agent of bovine mastitis. Foodborne Pathog Dis 2016, 13 (9): 477-482.10.1089/fpd.2015.211427182838 Search in Google Scholar

15. Locatelli C, Scaccabarozzi L, Pisoni G, Moroni P: CTX-M1 ESBL-producing Klebsiella pneumoniae subsp. pneumoniae isolated from cases of bovine mastitis. J Clin Microbiol 2010, 48: 3822-3823.10.1128/JCM.00941-10295311520720020 Search in Google Scholar

16. Wagner S, Gally DL, Argyle SA: Multidrug-resistant Escherichia coli from canine urinary tract infections tend to have commensal phylotypes, lower prevalence of virulence determinants and ampC-replicons. Vet Microbiol 2014, 169 (3-4) :171-178.10.1016/j.vetmic.2014.01.003396958324485933 Search in Google Scholar

17. Valat C, Drapeau A, Beurlet S, Bachy V, Boulouis H-J, Pin R, Cazeau G, Madec J-Y, Haenni M: Pathogenic Escherichia coli in dogs reveals the predominance of ST372 and the human-associated ST73 extra-intestinal lineages. Front in Microbiol 2020, 11: 580.10.3389/fmicb.2020.00580718635832373083 Search in Google Scholar

18. Pehlivanoglu F, Sababoglu E, Ozturk D, Turutoglu H: Characterisation of extended-spectrum β-lactamase genes of Klebsiella pneumoniae isolated from urinary tract infection of a dog. In: Proceedings of the 12th National Congress of Veterinary Microbiology; Kapadokya, Nevşehir, Türkiye; 2016. Pp. 19-20. Search in Google Scholar

19. Huber H, Zweifel C, Wittenbrink WW, Stephan R: ESBL-producing uropathogenic Escherichia coli from dog and cats in Switzerland. Vet Microbiol 2013, 162 (2-4): 992-996.10.1016/j.vetmic.2012.10.02923177909 Search in Google Scholar

20. Kuan NL, Chang CW, Lee CA, Yeh KS: Extended-spectrum β-lactamase producing Escherichia coli and Klebsiella pneumoniae isolates from the urine of dogs and cats suspected of urinary tract infection in a Veterinary teaching hospital. Taiwan Vet J 2016, 42 (3): 143-148.10.1142/S1682648515500274 Search in Google Scholar

21. Marques C, Belas A, Franco A, Aboim C, Gama LT, Pomba C: Increase in antimicrobial resistance and emergence of major international high-risk clonal lineages in dogs and cats with urinary tract infection: 16 year retrospective study. J Antimicrob Chemother 2018, 73 (2): 377-384.10.1093/jac/dkx401589075329136156 Search in Google Scholar

22. CLSI: Performans standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 5th edition. CLSI document Vet01S. Wayne, PA: Clinical and Laboratory Standards Institute; 2020. Search in Google Scholar

23. Winn W, Allen S, Janda W, Koneman E, Procop G, Schreckenberger P, Woods G: Koneman’s Color Atlas and Textbook of Diagnostic Microbiology. 6th edition, Philadelphia, USA: Lippincott Williams and Wilkins; 2006. Search in Google Scholar

24. Weisburg WG, Barns SM, Pelletier DA, Lane DJ: 16S ribosoma DNA amplification for phylogenetic study. J Bacteriol 1991, 173 (2): 697-703.10.1128/jb.173.2.697-703.19912070611987160 Search in Google Scholar

25. Laudy AE, Róg P, Smolińska-Król K, Ćmiel M, Słoczyńska A, Patzer J, Dzieerzanowska D, Wolinowska R, Starosciak B, Tyski S: Prevalence of ESBL-producing Pseudomonas aeruginosa isolates in Warsaw, Poland, detected by various phenotypic and genotypic methods. Plos One 2017, 12 (6): e0180121.10.1371/journal.pone.0180121548919228658322 Search in Google Scholar

26. Weldhagen GF, Poirel L, Nordmann P: Ambler class A extended-spectrum β-lactamases in Pseudomonas aeruginosa: novel development and clinical impact. Antimicrob Agents Chemother 2003, 47 (8): 2385-2392.10.1128/AAC.47.8.2385-2392.200316605612878494 Search in Google Scholar

27. Polsfuss S, Bloemberg GV, Giger J, Meyer V, Böttger EC, Hombach M: Practical approach for reliable detection of AmpC β-lactamase producing Enterobactericeae. J Clin Microbiol 2011, 49 (8): 2798-2803.10.1128/JCM.00404-11314773521632895 Search in Google Scholar

28. CLSI: Performance standards for antimicrobial susceptibility testing, 30th edition. CLSI Supplement M100. Wayne, PA: Clinical and Laboratory Standards Institute; 2020. Search in Google Scholar

29. Coudron PE: Inhibitor based methods for detecti on of plasmid mediated AmpC β-lactamases in Klebsiella spp., Escherichia coli, and Proteus mira bilis J Clin Microbiol 2005, 43 (8): 4163-4167.10.1128/JCM.43.8.4163-4167.2005123391316081966 Search in Google Scholar

30. Heffernan HM, Woodhouse RE, Pope CE, Blackmore TK: Prevalence and types of extended-spectrum β-lactamases among urinary Escherichia coli and Klebsiella spp. in New Zealand. Int J Antimicrob Agents 2009, 34: 544-549.10.1016/j.ijantimicag.2009.07.01419748232 Search in Google Scholar

31. Jeong SH, Bae IK, Kwon SB, Lee JH, Song JS, Jung HI, Sung KH, Jang SJ, Lee SH: Dissemination of transferable CTX-M-type extended-spectrum β-lactamase-producing E. coli in Korea. J Appl Microbiol 2005, 98: 921–927.10.1111/j.1365-2672.2004.02526.x15752339 Search in Google Scholar

32. Pehlivanoglu F, Turutoglu H, Ozturk D, Yardimci H: Molecular characterisation of ESBL-producing Escherichia coli isolated from healthy cattle and sheep. Acta Vet- Beograd 2016, 66 (4): 520-533.10.1515/acve-2016-0045 Search in Google Scholar

33. Rodrigues-Martines JM, Poirel L, Nordmann P: Extended-spectrum cephalosporinases in P. aeruginosa. Antimicrob Agents Chemother 2009; 53 (5): 1766-1771. Search in Google Scholar

34. CLSI: Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 4th edition. CLSI document VET01-A4 and VET01-S2, Wayne, PA: Clinical and Laboratory Standards Institute; 2013. Search in Google Scholar

35. WHO (World Health Organisation): Global priority list of antibiotic-resistant bacteria to guide research, discovery, and development of new antibiotics. https://www.who.int/publications Search in Google Scholar

36. Tark D-S, Moon DC, Kang HY, Kim S-R, Nam H-M, Lee H-S, Jung S-C, Lim S-K: Antimicrobial susceptibility and characterization of extended-spectrum β-lactamases in Escherichia coli isolated from bovine mastitic milk in South Korea from 2012 to 2015. J Dairy Sci 2017, 100 (5): 3463-3469.10.3168/jds.2016-1227628318579 Search in Google Scholar

37. Ali T, ur Rahman S, Zhang L, Shahid M, Han D, Gao J, Zhang S, Ruegg PL, Saddique U, Han B: Characteristics and genetic diversity of multi-drug resistant extended-spectrum β-lactamase (ESBL)-producing Escherichia coli isolated from bovine mastitis. Oncotarget 2017, 8 (52): 90144-90163.10.18632/oncotarget.21496568573829163817 Search in Google Scholar

38. Singh F, Sonawane GG, Kumar J, Dixit SK, Meena RK, Tripathi BN: Antimicrobial resistance and phenotypic and molecular detection of extended-spectrum ß-lactamases among extraintestinal Escherichia coli isolated from pneumonic and septicemic sheep and goats in Rajasthan, India. Turk J Vet Anim Sci 2019, 43: 754-760.10.3906/vet-1905-1 Search in Google Scholar

39. Chia JH, Siu LK, Su LH, Lin HS, Kuo AJ, Lee MH, Wu TL: Emergence of carbapenem-resistant Escherichia coli in Taiwan: Resistance due to combined CMY-2 production and porin deficiency. J Chemother 2009, 21(6): 621-626.10.1179/joc.2009.21.6.62120071284 Search in Google Scholar

40. Lister PD, Wolter DJ, Hanson ND: Antibacterial-resistant Pseudomonas aeruginosa: Clinical impact and complex regulation of chromosomally encoded resistance mechanismis. Clin Microbiol Rev 2009, 22: 582-610.10.1128/CMR.00040-09277236219822890 Search in Google Scholar

41. Naas T, Oueslati S, Bonnin RA, Dabos ML, Zavala A, Dortet L, Retailleau P, Iorga BI: Β-lactamase database (BLDB)-structure and function. J Enzyme Inhib Med Chem 2017, 32 (1): 917-919.10.1080/14756366.2017.1344235644532828719998 Search in Google Scholar

42. Palmeira JD, Ferreira HMN: Extended-spectrum β-lactamase (ESBL)- producing Enterobactericeae in cattle production- a threat around the world. Heliyon 2020, 6 (1): e03206.10.1016/j.heliyon.2020.e03206700283832042963 Search in Google Scholar

43. Schwaber MJ, Carmeli Y: Mortality and delay in effective therapy associated with extended-spectrum β-lactamase production in Enterobacteriaceae bacteraemia: a systematic review and meta-analysis. J Antimicrob Chemother 2007, 60 (5): 913-920.10.1093/jac/dkm31817848376 Search in Google Scholar

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