Beta-Lactam Antibiotic Resistance among Enterobacter spp. Isolated from Infection in Animals


Nosocomial infections are frequent complications of hospitalization, caused by opportunistic pathogens that gain access to hosts undergoing invasive procedures, such as surgery, intubation, and placement of deep vein lines. Nosocomial infections in animal hospitals can infect other animals, as well as be transmitted to human personnel. Enterobacter is a genus of common gram-negative bacteria, which can be associated with antibiotic resistant hospital infections. Because of an outbreak in antibiotic resistance in the genus, we decided to investigate five years of Enterobacter infections in the Large Animal Services of the Lois Bates Acheson Veterinary Teaching Hospital (LBAVTH) at Oregon State University. The demographics from 37 Enterobacter-infected patients of the LBAVTH were obtained from charts and analyzed. The identified clusters of infections suggested possible patient-environment sources of infection. The environment of the hospital was sampled in an attempt to determine the source of infection. Although Enterobacter was not isolated, three of the collected samples contained bacteria with resistance to third-generation cephalosporins. Enterobacter isolates from six of the 37 patients were further analyzed for presence of specific ESBL resistance genes. All six of the isolates harbored multiple extended-spectrum beta-lactamase genes, i.e., CTX-M-15, TEM-80, SHV-2 and AmpC. In summary, Enterobacter infection in the veterinary hospital was caused by beta-lactam-resistant strains, carrying ESBL-resistant genes. Veterinary hospital personnel should be aware of the potential for transmission, to both humans and animals, of ESBL-gene-containing bacteria.

Share and Cite:

S. Wilberger, M. , E. Anthony, K. , Rose, S. , McClain, M. and E. Bermudez, L. (2012) Beta-Lactam Antibiotic Resistance among Enterobacter spp. Isolated from Infection in Animals. Advances in Microbiology, 2, 129-137. doi: 10.4236/aim.2012.22018.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] C. Arpin, C. Coze, A. M. Rogues, J. P. Gachie, C. Bebear and C. Quentin, “Epidemiological Study of an Outbreak Due to Multidrug-Resistant Enterobacter aerogenes in a Medical Intensive Care Unit,” Journal of Clinical Microbiology, Vol. 34, No. 9, 1996, pp. 2163-2169.
[2] S. E. Cosgrove, K. S. Kaye, G. M. Eliopoulous and Y. Carmeli, “Health and Economic Outcomes of the Emergence of Third-Generation Cephalosporin Resistance in Enterobacter Species,” Archives of Internal Medicine, Vol. 162, No. 2, 2002, pp. 185-190. doi:10.1001/archinte.162.2.185
[3] S. Jalaluddin, J. M. Devaster, R. Scheen, M. Gerard and J. P. Butzler, “Molecular Epidemiological Study of Nosocomial Enterobacter aerogenes Isolates in a Belgian Hospital,” Journal of Clinical Microbiology, Vol. 36, No. 7, 1998, pp. 1846-1852.
[4] W. E. Sanders Jr. and C. C. Sanders, “Enterobacter spp.: Pathogens Poised to Flourish at the Turn of the Century,” Clinical Microbiology Reviews, Vol. 10, No. 2, 1997, pp. 220-241.
[5] P. E. Coudron, E. S. Moland and C. C. Sanders, “Occurrence and Detection of Extended-Spectrum Beta-Lactamases in Members of the Family Enterobacteriaceae at a Veterans Medical Center: Seek and You May Find,” Journal of Clinical Microbiology, Vol. 35, No. 10, 1997, pp. 2593-2597.
[6] L. B. Rice, S. H. Willey, G. A. Papanicolaou, A. A. Medeiros, G. M. Eliopoulos, R. C. Moellering Jr. and G. A. Jacoby, “Outbreak of Ceftazidime Resistance Caused by Extended-Spectrum Beta-Lactamases at a Massachusetts Chronic-Care Facility,” Antimicrobial Agents and Chemotherapy, Vol. 34, No. 11, 1990, pp. 2193-2199.
[7] L. A. Minarini, E. C. Clímaco, D. B. Guimar?es, J. C. Ferreira, I. C. Palazzo, R. Martinez and A. L. Darini, “Clonal Transmission of ESBL-Producing Klebsiella spp. at a University Hospital in Brazil,” Current Microbiology, Vol. 56, No. 6, 2008, pp. 587-591. doi:10.1007/s00284-008-9129-5
[8] N. D. Hanson, “AmpC Beta-Lactamases: What Do We Need to Know for the Future?” Journal of Antimicrobial Consumption, Vol. 52, No. 1, 2003, pp. 2-4. doi:10.1093/jac/dkg284
[9] R. Bonnet, “Growing Group of Extended-Spectrum Beta-Lactamases: The CTX-M Enzymes,” Antimicrobial Agents and Chemotherapy, Vol. 48, No. 1, 2004, pp. 1-14. doi:10.1128/AAC.48.1.1-14.2004
[10] J. S. Weese, “Investigation of Enterobacter cloacae Infections at a Small Animal Veterinary Teaching Hospital,” Veterinary Microbiology, Vol. 130, No. 3-4, 2008, pp. 426-428. doi:10.1016/j.vetmic.2008.02.009
[11] L. Bret, C. Chanal-Claris, D. Sirot, E. B. Chaibi, R. Labia and J. Sirot, “Chromosomally Encoded AmpC-Type Beta-Lactamase in a Clinical Isolate of Proteus mirabilis,” Antimicrobial Agents and Chemotherapy, Vol. 42, No. 5, 1998, pp. 1110-1114.
[12] C. Dutour, R. Bonnet, H. Marchandin, M. Boyer, C. Chanal, D. Sirot and J. Sirot, “CTX-M-1, CTX-M-3, and CTX-M-14 Beta-Lactamases from Enterobacteriaceae Isolated in France,” Antimicrobial Agents and Chemotherapy, Vol. 46, No. 2, 2002, pp. 534-537. doi:10.1128/AAC.46.2.534-537.2002
[13] M. Quinteros, M. Radice, N. Gardella, M. M. Rodriguez, N. Costa, D. Korbenfeld, E. Couto and G. Gutkind, “Extended-Spectrum Beta-Lactamases in Enterobacteriaceae in Buenos Aires, Argentina, Public Hospitals,” Antimicrobial Agents and Chemotherapy, Vol. 47, No. 9, 2003, pp. 2864-2867. doi:10.1128/AAC.47.9.2864-2867.2003
[14] J. Schlesinger, S. Navon-Venezia, I. Chmelnitsky, O. Hammer-Munz, A. Leavitt, H. S. Gold, M. J. Schwaber and Y. Carmeli, “Extended-Spectrum Beta-Lactamases among Enterobacter Isolates Obtained in Tel Aviv, Israel,” Antimicrobial Agents and Chemotherapy, Vol. 49, No. 3, 2005, pp. 1150-1156. doi:10.1128/AAC.49.3.1150-1156.2005
[15] J. D. Pitout, D. B. Gregson, D. L. Church, S. Elsayed and K. B. Laupland, “Community-Wide Outbreaks of Clonally Related CTX-M-14 Beta-Lactamase-Producing Escherichia coli Strains in the Calgary Health Region,” Journal of Clinical Microbiology, Vol. 43, No. 6, 2005, pp. 2844-2849. doi:10.1128/JCM.43.6.2844-2849.2005
[16] X. Bertrand, D. Hocquet, K. Boisson, E. Siebor and P. Plesiat, D. Talon, “Molecular Epidemiology of Enterobacteriaceae Producing Extended-Spectrum Beta-Lactamase in a French University-Affiliated Hospital,” The International Journal of Antimicrobial Agents, Vol. 22, No. 2, 2003, pp. 128-133. doi:10.1016/S0924-8579(03)00098-0
[17] C. Neuwirth, E. Siebor, J. Lopez, A. Pechinot and A. Kazmierczak, “Outbreak of TEM-24-Producing Enterobacter aerogenes in an Intensive Care Unit and Dissemination of the Extended-Spectrum Beta-Lactamase to Other Members of the Family Enterobacteriaceae,” Journal of Clinical Microbiology, Vol. 34, No. 1, 1996, pp. 76-79.
[18] O. Lesens, Y. Hansmann, P. Riegel, R. Heller, M. Benaissa-Djellouli, M. Martinot, H. Petit and D. Christmann, “Bacteremia and Endocarditis Caused by a Gordonia Species in a Patient with a Central Venous Catheter,” Emerging Infectious Diseases, Vol. 6, No. 4, 2000, pp. 382-385. doi:10.3201/eid0604.000410
[19] J. Duchon, P. Graham III, P. Della-Latta, S. Whittier, D. Carp, D. Bateman and L. Saiman, “Epidemiology of Enterococci in a Neonatal Intensive Care Unit,” Infection Control & Hospital Epidemiology, Vol. 29, No. 4, 2008, pp. 374-376. doi:10.1086/533544
[20] E. Tzelepi, P. Giakkoupi, D. Sofianou, V. Loukova, A. Kemeroglou and A. Tsakris, “Detection of Extended-Spectrum Beta-Lactamases in Clinical Isolates of Enterobacter cloacae and Enterobacter aerogenes,” Journal of Clinical Microbiology, Vol. 38, No. 2, 2000, pp. 542-546.
[21] A. Y. Peleg and D. C. Hooper, “Hospital-Acquired Infections Due to Gram-Negative Bacteria,” The New England Journal of Medicine, Vol. 362, No. 19, 2010, pp. 1804-1813. doi:10.1056/NEJMra0904124

Copyright © 2024 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.