Detection of beta-lactamase-producing Enterobacteriaceae in a veterinary hospital environment




TEM, CTX-M, Antimicrobial resistance, Nosocomial infection


Due to the strong selective pressure resulting from the misuse of antibiotics, the natural process of bacterial resistance has been accelerated, leading to the increasingly constant appearance of multiresistant isolates. The high number of multiresistant bacteria is a one health problem. Enterobacteriaceae are usually commensal bacteria of the gastrointestinal tract. However, they can cause infections, and the most important resistance characteristic among them is the production of β-lactamases. This study aimed to identify ESBL-producing Enterobacteriaceae of types of TEM, SHV, and the CTX-M groups. To isolate the enterobacteria, swabs were collected by swiping objects that had contact with the patients and professionals, and the water of the hospital environment. Ten collections were carried out, yielding 306 samples, from which 118 enterobacteria were identified: Escherichia coli, Enterobacter spp., Klebsiella spp., Proteus mirabilis, Serratia spp., and Citrobacter spp. Isolates. The genes TEM and CTX-M, for the production of β lactamases, were detected in 12.7% of the 118 enterobacterial isolates. It is very important to know the bacterial population circulating in the veterinary hospital environment and its resistance to  antimicrobials so that professionals can take appropriate measures to minimize the risks of transmission, especially from cages and consultation tables. In addition, the correct control of the microbiological quality of the supply water, as well as environmental cleaning procedures, are essential to prevent the transmission of these microorganisms.


Download data is not yet available.

Author Biography

Jefferson Fernando Naves Pinto, Universidade Federal de Jataí, Laboratório de Recursos Genéticos e Melhoramento Vegetal

Laboratório de recursos genéticos e melhoramento vegetal, Universidade Federal de Jataí UFJ.


Agência Nacional de Vigilância Sanitária - Anvisa. Boletim de segurança do paciente e qualidade em serviços de saúde n°16: avaliação dos indicadores nacionais das infecções relacionadas à assistência à saúde (IRAS) e resistência microbiana do anos de 2016 (revisado). Brasília: Anvisa; 2017.

Ambler RP. The structure of β-lactamases. Philos Trans R Soc Lond B Biol Sci. 1980;289(1036):321-31. PMid:6109327.

Bajpai T, Pandey M, Varma M, Bhatambare GS. Prevalence of TEM, SHV and CTX-M beta- lactamase genes in the urinary iolates of a tertiary care hospital. Avicenna J Med. 2017;7(1):12-6. PMid:28182026.

Bevan ER, Jones AM, Hawkey PM. Global epidemiology of CTX-M β lacamases: temporal and geographical shifts in genotype. J Antimicrob Chemother. 2017;72(8):2145- 55. PMid:28541467.

Blair JMA, Webber MA, Baylay J, Ogbolu DO, Piddock LJV. Molecular mechanisms of antibiotic resistance. Nat Rev Microbiol. 2015;13(1):42-51. PMid:25435309.

Bogaerts P, Huang TD, Bouchahrouf W, Bauraing C, Berhin C, El Garch F, Glupczynski Y. Characterization of ESBL- and AmpC-Producing Enterobacteriaceae from diseased companion animals in Europe. Microb Drug Resist. 2015;21(6):643-50. PMid:26098354.

Bonnet R. Growing group of Extended-Spectrum B-Lactamases: the CTX-M Enzymes. Antimicrob Agents Chemother. 2004;48(1):1-14. AAC.48.1.1-14.2004. PMid:14693512.

Bush K, Jacoby GA. Updated functional classification of beta-lactamases. Antimicrob Agentes Chemother. 2010;54(3):969-76. PMid:19995920.

Carvalho MV, Spinola T, Tavolari F, Irino K, Oliveira RM, Ramos MCC. Infecções do trato urinário (ITU) de cães e gatos: etiologia e resistência aos antimicrobianos. Pesq Vet Bras. 2014;34(1):62-70.

Clinical and Laboratory Standards Institute - CLSI. Performance standards for antimicrobial susceptibility testing. 28th ed. Pennsylvania: National Committee for Clinical Laboratory Standards; 2018.

Dropa M, Lincopan N, Balsalobre LC, Oliveira DE, Moura RA, Fernandes MR, Silva QS, Matté GR, Sato MIZ, Matté MH. Genetic background of novel sequence types of CTX-M-8 and a CTX-M-15- producing Escherichia coli and Klebsiella pneumoniae from public wasterwater treatment plants in São Paulo, Brazil. Environ Sci Pollut Res Int. 2016;23(5):4953-8. PMid:26782324.

Guzmán-Blanco M, Labarca JA, Villegas MV, Gotuzzo E. Extended spectrum - lactamase producers among nosocomial Enterobacteriaceae in Latin America. Braz J Infect Dis. 2014;18(4):421-33. PMid:24389277.

Johard S, Borjesson S, Thowald-Wigh G, Fernstrom L, Nicol C, Bergstrom A. Extended spectrum Beta-Lactamase/7/8 Braz J Vet Res Anim Sci. 2022;59:e191724 AmpC-producing E.coli in dogs treated with antimicrobial in surgical wards. Int J Appl Res Vet Med. 2015;13(1):80-8. Available from:

Kanamori H, Rutala WA, Weber DJ. The role of patient care items as a fomite in healthcare-associated outbreaks and infection prevention. Clin Infect Dis. 2017;65(8):1412- 9. PMid:28520859.

Koneman E, Winn W Jr, Allen S, Janda W, Procop G, Schreckenberber P, Woods G. Diagnóstico microbiológico: texto e atlas colorido. Rio de Janeiro: Guanabara Koogan; 2012.

Livermore DM. Current epidemiology and growing resistance of gram-negative pathogens. Korean J Intern Med. 2012;27(2):128-42. PMid:22707882.

López-Cerero L. Papel del ambiente hospitalario y los equipamientos en la transmisión de las infecciones nosocomiales. Enferm Infecc Microbiol Clin. 2014;32(7):459-64. PMid:24315300.

Loureiro RJ, Roque F, Rodrigues AT, Herdeiro MT, Ramalheira E. O uso de antibióticos e as resistências bacterianas: breves notas sobre a sua evolução. Rev Port Saude Publica. 2016;34(1):77-84.

Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, Harbarth S, Hindler JF, Kahlmeter G, Olsson Liljequist B, Paterson DL, Rice LB, Stelling J, Struelens MJ, Vatopoulos A, Weber JT, Monnet DL. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268-81. PMid:21793988.

Mendelson M, Matsoso MP. The World Health Organization global action plan for antimicrobial resistance. SAMJ: S Afr Med J. 2015;105(5):325. PMid:26242647.

Milton AAP, Priya GB, Aravind M, Parthasarathyl S, Saminathan M, Jeevan K, Agarwal RK. Nosocomial Infections and their Surveillance in Veterinary. Adv Anim Vet Sci. 2014;3(2s):1-24.

Moyaert H, Morrissey I, de Jong A, El Garch F, Klein U, Ludwig C, Thiry J, Youala M. Antimicrobial susceptibility monitoring of bacterial pathogens isolated from urinary tract infections in dogs and cats across Europe: ComPath results. Microb Drug Resist. 2017;23(3):391-403. PMid:28384093.

Munita JM, Arias CA. Mechanisms of antibiotic resistance. Microbiol Spectr. 2016;4(2):4215. PMid:27227291.

Nordmann P, Poirel L. Rapid diagnostic tests for detecting emerging antibiotic resistance are mostly available and should be used now. Infectious Diseases Hub. 2017;2(13):11199.

Oliveira DV, Nunes LS, Barth AL, Van Der Sandi ST. Genetic background of β-lactamses in Enterobacteriaceae isolates from environmental samples. Microb Ecol. 2017;74(3):599-607. PMid:28378066.

Oliveira PA, Moura RA, Rodrigues GV, Lopes KFC, Zaniolo MM, Rubio KAJ, Dias EH, Oliveira LA, Chideroli RT, Gonçalves DD. Detection of extended spectrum beta-lactamases and resistance in members of the Enterobacteriaceae family isolated from healthy sheep and dogs in Umuarama, Paraná, Brazil. Semina: Ciênc Agrár. 2016;37(2):829-40.

Poirel L, Bonnin RA, Nordmann P. Genetic support and diversity of acquired extended-spectrum b-lactamases in Gram-negative rods. Infect Genet Evol. 2012;12(5):883- 93. PMid:22414916.

Poirel L, Fernandez J, Nordemann P. Comparison of three biochemical test for rapid detection of Extenderd-Spectrum Lactamase-Producing Enterobacteriaceae. J Clin Microbiol. 2016;54(2):423-7. PMid:26659217.

Rocha FR, Pinto VPT, Barbosa FCB. The spread of CTX M-type extended-spectrum β-lactamases in Brazil: a systematic review. Microb Drug Resist. 2016;22(4):301-11. PMid:26669767.

Rocha FR. Análise molecular da prevalência dos genes Beta lactamases blaCTX-M, blaSHV e blaTEM em Klebsiella pneumoniae isoladas de pacientes com diagnóstico de infecção hospitalar na Santa Casa de Misericórdia de Sobral, Ceará [dissertação de mestrado]. Sobral: Universidade do Ceará; 2015 [cited 2021 Oct 23]. 63 p. Available from:

Rubin JE, Pitout JD. Extended-spectrum β-lactamase, carbapenemase and AmpC producing Enterobacteriaceae in companion animals. Vet Microbiol. 2014;170(1-2):10-8. http:// PMid:24576841.

Sfaciotte RAP, Parussolo L, Melo FD, Wildemann P, Bordignon G, Israel ND, Leitzke M, Wosiacki SR, Salbego FZ, Costa UM, Ferraz SM. Identification and characterization of multidrug-resistant extended-spectrum beta-lactamase producing bacteria from healthy and diseased dogs and cats admitted to a veterinary hospital in Brazil. Microb Drug Resist. 2021;27(6):855-64. PMid:33185513.

Shaikh S, Fatima J, Shakil S, Rizvi SMD, Kamal MA. Antibiotic resistance and extended spectrum beta lactamases: types, epidemiology and treatment. Saudi J Biol Sci. 2015;22(1):90-101. PMid:25561890.

Stull JW, Weese JS. Hospital-associated infections in small animal practice. Vet Clin North Am Small Anim Pract. 2015;45(2):217-33. PMid:25559054.

van den Berg RWA, Claahsen HL, Niessen M, Muytjens HL, Liem K, Voss A. Enterobacter cloacae outbreak in the NICU related to disinfected thermometers. J Hosp Infect. 2000;45(1):29-34. PMid:10917779.

Walther B, Tedin K, Lübke-Becker A. Multidrug-resistant opportunistic pathogens challenging veterinary infection control. Vet Microbiol. 2017;200:71-8. PMid:27291944.

Wieler LH, Walther B, Vincze S, Guenther S, Lübke-Becker A. Infections with multidrug-resistant bacteria: has the post-antibiotic era arrived in companion animals? In Sing A, editor. Zoonoses-infections affecting humans and animals. Dordrecht: Springer; 2015. p. 433-52.

Woerther PL, Lepeule R, Burdet C, Decousser JW, Ruppé É, Barbier F. Carbapenems and alternative β-lactams for the treatment of infections due to extended-spectrum β-lactamase-producing Enterobacteriaceae: what impact on intestinal colonisation resistance? Int J Antimicrob Agents. 2018;52(6):762-70. PMid:30176355.

Wong C, Epstein SE, Westropp JL. Antimicrobial susceptibility patterns in urinary tract infections in dogs (2010-2013). J Vet Intern Med. 2015;29(4):1045-52. PMid:26133165.

Woodford N, Fagan EJ, Ellington MJ. Multiplex PCR for rapid detection of genes encoding CTX-M extended-spectrum β-lactamases. J Antimicrob Chemother. 2006;57(1):154- 5. PMid:16284100.

Zogg AL, Simmen S, Zurfluh K, Stephan R, Schmitt SN, Nüesch-Inderbinen M. High prevalence of extended spectrum β-lactamase producing enterobacteriaceae among clinical isolates from cats and dogs admitted to a veterinary hospital in Switzerland. Front Vet Sci. 2018;5:62. PMid:29662886.




How to Cite

Oliveira, A. F. de ., Arrais, B. R., Bannwart, P. F. ., Pinto, J. F. N. ., & Stella, A. E. (2022). Detection of beta-lactamase-producing Enterobacteriaceae in a veterinary hospital environment. Brazilian Journal of Veterinary Research and Animal Science, 59, e191724.