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Abstract
The most common cause of urinary tract infection in dogs is uropathogenic Escherichia coli (UPEC). This condition often presents with vaginal discharge, dribbling of urine, straining or vocalization while urinating due to pain. Furthermore, the following signs are also noticeable: hematuria, lethargy, proteinuria, dysuria, cystitis, and oliguria. The aim of this research was to investigate the genes of ampicillin resistance in E. coli isolates from dogs with urinary tract infections. Out of 103 urine samples cultured (Blood agar, MacConkey’s lactose agar and Eosin methylene blue agar), 24.3% were positive for uropathogenic Escherichia coli. The positive isolates were further subjected to antimicrobial sensitivity test and PCR analysis. All the uropathogenic Escherichia coli isolates were resistant to ampicillin while 96% were resistant to Cloxacillin and Oxytetracycline. Susceptibility to Meropenem, Gentamicin and Amikacin were 64 %, 44 % and 40% respectively. All the 25 strains of the E. coli were identified to be resistant to two or more antibiotics. The PCR result showed the presence of blaAMPC in all the samples and 60 % had blaTEM genes responsible for ampicillin resistance. However, none of the isolates were positive for the blaSHV gene.The presence of the blaAMPC and blaTEM genes in the dogs studied resulted in ampicillin resistance, with blaAMPC being the most commonly detected ampicillin gene in Escherichia coli in the study area. Meropenem was also found to be a good choice for treating uropathogenic E. coli infection in dogs.
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References
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- Bauer, A.W., Kirby, W.M.M, Sherris, J.C. and Turck, M. (1966). Antibiotic susceptibility testing by standardized single disk method. American. Journal of Clinical Pathology, 45,493-496.PMID: 5325707
- Bradford, P.A. (2001). Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clinical Microbiology Reviews, 14, 933-951.DOI: 10.1128/CMR.14.4
- Brinas, L., Lanteo, M., DeDiego, I., Alvarez. M., Zarazag, M. and Torres. C. (2005). Mechanisms of resistance to expanded spectrum cephalosporins in E. coli isolates recovered in a Spanish hospital Journal of Antimicrobial Chemotherapy, 56, 1107-1110. DOI: 10.1093/jac/dki370
- Brinas, L., Zarazaga, M., Saenz, Y., Ruiz-Larrea, F. and Torres. C. (2002). Beta-lactamases in ampicillin-resistant Escherichia coli isolates from foods, humans and healthy animals. Antimicrobial Agent and Chemotherapy, 46, 3156 3163. DOI: 10.1128/aac.39.6.1211.
- Bush, K. and Jacoby, G.A. (1997). Nomenclature of TEM β lactamases. Journal Antimicrobial and Chemotherapy. 39:13
- Bush, K., Jacoby, G.A. and Medeiros, A.A (1995). A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimicrobial Agents Chemotherapy. 39,1211-1233.DOI: 10.1128/aac.39.6.1211
- Calva, J.J., Sifuentes-Osornio, J. and Céron, C. (1996). Antimicrobial resistance in fecal flora: longitudinal community-based surveillance of children from urban Mexico. Antimicrobial Agents Chemotherapy. 40, 1699-1702. DOI: 10.1128/AAC.40.7.1699
- Caroff, N., Espaze, E., Berard, I., Richet, H. and Reynaud, A. (1999). Mutations in the ampC promoter of Escherichia coli isolates resistant to oxyiminocephalosporins without extended spectrum β-lactamase production. FEMS Microbiology letters 173,459 465. DOI: 10.1111/j.1574-6968.1999.tb13539.x
- Carvalho, A.C., Barbosa, A.V., Arais, L.R., Ribeiro, P.F., Carneiro, V.C. and Cerqueira, A.M.F. (2016). Resistance patterns, ESBL genes, and genetic relatedness of Escherichia coli from dogs and owners. Brazilian Journal Microbiology. 47,150-158. DOI.org/10.1016/j.bjm.11.005
- Chang, S.K., Lo, D.Y., Wei, H.W. and Kuo, H.C. (2015). Antimicrobial resistance of Escherichia coli isolates from canine urinary tract infections. Journal of Veterinary and Medical Sciences, 77, 59-65. DOI: 10.1292/jvms.13-0281
- Cummings, K.J., Aprea, V.A. and Altier, C. (2015). Antimicrobial resistance trends among canine Escherichia coli isolates obtained from clinical samples in the northeastern USA, 2004–2011. Canadian Veterinary Journal,56,393-398.PMCID: PMC4357913
- Cummings, K.J., Warnick, L.D., Davis, M.A., Eckmann, K, Gröhn, Y.T., Hoelzer, K., MacDonald, K., Root, T.P., Siler, J.D., McGuir,e S.M. and Wiedmann, M. (2012). Farm animal contact as risk factor for transmission of bovine-associated Salmonella subtypes. Emerging Infectious Diseases.18, 1929-1936. DOI: 10.3201/eid1812.110831
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- Kuan, N.L., Chang, C.W., Lee, C.A. and Yeh, K.S. (2016). Extended-Spectrum Beta-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 Veterinary Journal, 42, 143-148.DOI.org/10.1142/S1682648515500274
- Lei, T., Tian, W., He, L., Huang, X.H., Sun, Y.X., Deng, Y.T., Sun, Y., Lv, D.H., Wu, C.M., Huang, L.Z. and Shen, J.Z. (2010). Antimicrobial resistance in Escherichia coli isolates from food animals, animal food products and companion animals in China. Veterinary Microbiology, 146, 85-89. DOI: 10.1016/j.vetmic.2010.04.025
- Levy, S.B. (1997). January. Antibiotic resistance: an ecological imbalance. In Ciba Found Symposium 207, 1-9.DOI: 10.1002/9780470515358.ch1
- Liu, X., Liu, H., Li, Y. and Hao, C. (2017). Association between virulence profile and fluoroquinolone resistance in Escherichia coli isolated from dogs and cats in China. Journal of Infection in Developing. Countries. 11,306-313. DOI: 10.3855/jidc.8583
- Livermore, D.M. (1995). beta-Lactamases in laboratory and clinical resistance. Clinical Microbiology Reviews,8, 557-584.DOI: 10.1128/CMR.8.4.557
- M., Chakraborty, T. and Mshana, S.E. (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. Frontiers in Microbiology 7,142. DOI: 10.3389/fmicb.2016.00142
- Moyaert, H., Morrissey, I., de Jong, A., El Garch, F., Klein, U., Ludwig, C., Thiry, J. and Youala, M. (2017). Antimicrobial susceptibility monitoring of bacterial pathogens isolated from urinary tract infections in dogs and cats across Europe: ComPath results. Microbial Drug Resistance, 23,391-403. DOI: 10.1089/mdr.2016.0110
- Muhammad, M., Parveen, G., Vinay, K., Divya, A., Tarun, K. and Sushila, M. (2019). Isolation of uropathogenic Escherichia coli from dogs and molecular detection of chloramphenicol resistance genes. Haryana Veterinarian 58, 66-69.
- O'BrienO’Brien, T.F. (1997). The global epidemic nature of antimicrobial resistance and the need to monitor and manage it locally. Clinical Infectious Disease, 24, S2-S8. DOI: 10.1093/clinids/24.supplement1.s2
- Onanuga, A., Oyi, A.R. and Onaolapo, J.A. (2005). Prevalence and susceptibility pattern of methicillinresistant Staphylococcus aureus isolates among healthy women in Zaria, Nigeria. African Journal of Biotechnology 4, 1321 1324. DOI: 10.1093/jac/dkm269
- Pedersen, K., Pedersen, K., Jensen, H., Finster, K., Jensen, V.F. and Heuer, O.E. (2007). Occurrence of antimicrobial resistance in bacteria from diagnostic samples from dogs. Journal of Antimicrobial Chemotherapy, 60,775 781. DOI: 10.1093/jac/dkm269
- Pinto, L., Radhouani, H., Coelho, C., da Costa, P.M., Simões, R., Brandão, R.M., Torres, C., Igrejas, G. and Poeta, P. (2010). Genetic detection of extended-spectrum β-lactamase-containing Escherichia coli isolates from birds of prey from Serra da Estrela natural reserve in Portugal. Applied and Environmental Microbiology, 76, 4118-4120. DOI: 10.1128/AEM.02761-09
- Pitout, J.D. and Laupland, K.B. (2008). Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infectious Disease. 8,159-166. DOI: 10.1016/S1473-3099(08)70041-0
- Pitout, J.D.D., Thomson, K.S., Hanson, N.D., Ehrhardt, A.F., Moland, E.S. and Sanders, C.C. (1998). β-Lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiellapneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrobial Agents and Chemotherapy. 42, 1350-1354. DOI: 10.1128/AAC.42.6.1350
- Poeta, P., Costa, D., Rodrigues, J. and Torres, C. (2005). Study of faecal colonization by vanA-containing Enterococcus strains in healthy humans, pets, poultry and wild animals in Portugal. Journal of Antimicrobial Chemotherapy. 55,278-280. DOI: 10.1093/jac/dkh549
- Saenz ,Y., Brinas, L., Domínguez, E., Ruiz, J., Zarazaga, M., Vila, J. and Torres. C. (2004). Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origins. Antimicrobial Agents and Chemotherapy. 48, 3996-4001. DOI: 10.1128/AAC.48.10.3996-4001.2004
- Seguin, M.A., Vaden A.C., Stone, E. and Levine, J.F. (2003). Persistent urinary tract infections and reinfections in 100 dogs (1989–1999). Journal of Veterinary Internal Medicine. 17, 622 631. DOI: 10.1111/j.1939-1676.2003.tb02492.x
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- Simjee, S., White, D.G., McDermott, P.F., Wagner, D.D., Zervos, M.J., Donabedian, S.M., English, L.L., Hayes, J.R. and Walker, R.D. (2002). Characterization of Tn1546 in vancomycin-resistant Enterococcus faecium isolated from canine urinary tract infections: evidence of gene exchange between human and animal enterococci. Journal of Clinical Microbiology. 40, 4659-4665.DOI: 10.1128/JCM.40.12.4659-4665.2002
- Sodha, S.V., Lynch, M., Wannemuehler, K., Leeper, M., Malavet, M., Schaffzin, J., Chen, T., Langer, A., Glenshaw, M., Hoefer, D. and Dumas, N. (2011). Multistate outbreak of Escherichia coli O157: H7 infections associated with a national fast-food chain, 2006: a study incorporating epidemiological and food source traceback results. Epidemiology and Infection, 139,309 316. DOI: 10.1017/S0950268810000920
- Sørum, H. and Sunde. M. (2001). Resistance to antibiotics in the normal flora of animals. Veterinary Research, 32, 227-241. DOI: 10.1051/vetres:2001121
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- Von Baum, H. and Marre, R. (2005). Antimicrobial resistance of Escherichia coli and therapeutic implications. International Journal of Medical Microbiology, 295,503511. DOI: 10.1016/j.ijmm.2005.07.002
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References
Ball, K.R., Rubin, J.E., Chirino-Trejo M. and Dowling, P.M. (2008). Antimicrobial resistance and prevalence of canine uropathogens at the Western College of Veterinary Medicine Veterinary Teaching Hospital, 2002–2007. Canadian Veterinary Journal. 49,985-990. PMID: 19119366
Bauer, A.W., Kirby, W.M.M, Sherris, J.C. and Turck, M. (1966). Antibiotic susceptibility testing by standardized single disk method. American. Journal of Clinical Pathology, 45,493-496.PMID: 5325707
Bradford, P.A. (2001). Extended-spectrum β-lactamases in the 21st century: characterization, epidemiology, and detection of this important resistance threat. Clinical Microbiology Reviews, 14, 933-951.DOI: 10.1128/CMR.14.4
Brinas, L., Lanteo, M., DeDiego, I., Alvarez. M., Zarazag, M. and Torres. C. (2005). Mechanisms of resistance to expanded spectrum cephalosporins in E. coli isolates recovered in a Spanish hospital Journal of Antimicrobial Chemotherapy, 56, 1107-1110. DOI: 10.1093/jac/dki370
Brinas, L., Zarazaga, M., Saenz, Y., Ruiz-Larrea, F. and Torres. C. (2002). Beta-lactamases in ampicillin-resistant Escherichia coli isolates from foods, humans and healthy animals. Antimicrobial Agent and Chemotherapy, 46, 3156 3163. DOI: 10.1128/aac.39.6.1211.
Bush, K. and Jacoby, G.A. (1997). Nomenclature of TEM β lactamases. Journal Antimicrobial and Chemotherapy. 39:13
Bush, K., Jacoby, G.A. and Medeiros, A.A (1995). A functional classification scheme for beta-lactamases and its correlation with molecular structure. Antimicrobial Agents Chemotherapy. 39,1211-1233.DOI: 10.1128/aac.39.6.1211
Calva, J.J., Sifuentes-Osornio, J. and Céron, C. (1996). Antimicrobial resistance in fecal flora: longitudinal community-based surveillance of children from urban Mexico. Antimicrobial Agents Chemotherapy. 40, 1699-1702. DOI: 10.1128/AAC.40.7.1699
Caroff, N., Espaze, E., Berard, I., Richet, H. and Reynaud, A. (1999). Mutations in the ampC promoter of Escherichia coli isolates resistant to oxyiminocephalosporins without extended spectrum β-lactamase production. FEMS Microbiology letters 173,459 465. DOI: 10.1111/j.1574-6968.1999.tb13539.x
Carvalho, A.C., Barbosa, A.V., Arais, L.R., Ribeiro, P.F., Carneiro, V.C. and Cerqueira, A.M.F. (2016). Resistance patterns, ESBL genes, and genetic relatedness of Escherichia coli from dogs and owners. Brazilian Journal Microbiology. 47,150-158. DOI.org/10.1016/j.bjm.11.005
Chang, S.K., Lo, D.Y., Wei, H.W. and Kuo, H.C. (2015). Antimicrobial resistance of Escherichia coli isolates from canine urinary tract infections. Journal of Veterinary and Medical Sciences, 77, 59-65. DOI: 10.1292/jvms.13-0281
Cummings, K.J., Aprea, V.A. and Altier, C. (2015). Antimicrobial resistance trends among canine Escherichia coli isolates obtained from clinical samples in the northeastern USA, 2004–2011. Canadian Veterinary Journal,56,393-398.PMCID: PMC4357913
Cummings, K.J., Warnick, L.D., Davis, M.A., Eckmann, K, Gröhn, Y.T., Hoelzer, K., MacDonald, K., Root, T.P., Siler, J.D., McGuir,e S.M. and Wiedmann, M. (2012). Farm animal contact as risk factor for transmission of bovine-associated Salmonella subtypes. Emerging Infectious Diseases.18, 1929-1936. DOI: 10.3201/eid1812.110831
Gibson, J.S., Morton, J.M., Cobbold, R.N., Sidjabat, H.E., Filippich, L.J. and Trott, D.J. (2008). Multidrug‐resistant E. coli and Enterobacter extraintestinal infection in 37 dogs. Journal of Veterinary Internal Medicine, 22, 844-850. DOI: 10.1111/j.1939-1676.00124.x
Hoge, C.W., Gambel, J.M., Srijan, A., Pitarangsi, C. and Echeverria, P. (1998). Trends in antibiotic resistance among diarrheal pathogens isolated in Thailand over 15 years. Clinical Infectious Disease,26, 341-345. DOI: 10.1086/516303
Johnson, A. P. (2015). Surveillance of antibiotic resistance. Philosophical Transactions of the Royal Society B: Biological Sciences, 370(1670), 20140080.DOI: 10.1098/rstb.0080
Johnson, T.J., Kariyawasam, S., Wannemuehler, Y., Mangiamele, P., Johnson, S.J., Doetkott, C., Skyberg, J.A., Lynne, A.M., Johnson, J.R. and Nolan, L.K. (2007). The genome sequence of avian pathogenic Escherichia coli strain O1: K1: H7 shares strong similarities with human extraintestinal pathogenic E. coli genomes. Journal of Bacteriology.189, 3228-3236. DOI: 10.1128/JB.01726-06
Kang, S., Lee, D., Shin, S., Ahn, J. and Yoo. H. (2005). Changes in patterns of antimicrobial susceptibility and class 1 integron carriage among Escherichia coli isolates. Journal of Veterinary Sciences, 6,201-205.PMID: 16131822
Kuan, N.L., Chang, C.W., Lee, C.A. and Yeh, K.S. (2016). Extended-Spectrum Beta-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 Veterinary Journal, 42, 143-148.DOI.org/10.1142/S1682648515500274
Lei, T., Tian, W., He, L., Huang, X.H., Sun, Y.X., Deng, Y.T., Sun, Y., Lv, D.H., Wu, C.M., Huang, L.Z. and Shen, J.Z. (2010). Antimicrobial resistance in Escherichia coli isolates from food animals, animal food products and companion animals in China. Veterinary Microbiology, 146, 85-89. DOI: 10.1016/j.vetmic.2010.04.025
Levy, S.B. (1997). January. Antibiotic resistance: an ecological imbalance. In Ciba Found Symposium 207, 1-9.DOI: 10.1002/9780470515358.ch1
Liu, X., Liu, H., Li, Y. and Hao, C. (2017). Association between virulence profile and fluoroquinolone resistance in Escherichia coli isolated from dogs and cats in China. Journal of Infection in Developing. Countries. 11,306-313. DOI: 10.3855/jidc.8583
Livermore, D.M. (1995). beta-Lactamases in laboratory and clinical resistance. Clinical Microbiology Reviews,8, 557-584.DOI: 10.1128/CMR.8.4.557
M., Chakraborty, T. and Mshana, S.E. (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. Frontiers in Microbiology 7,142. DOI: 10.3389/fmicb.2016.00142
Moyaert, H., Morrissey, I., de Jong, A., El Garch, F., Klein, U., Ludwig, C., Thiry, J. and Youala, M. (2017). Antimicrobial susceptibility monitoring of bacterial pathogens isolated from urinary tract infections in dogs and cats across Europe: ComPath results. Microbial Drug Resistance, 23,391-403. DOI: 10.1089/mdr.2016.0110
Muhammad, M., Parveen, G., Vinay, K., Divya, A., Tarun, K. and Sushila, M. (2019). Isolation of uropathogenic Escherichia coli from dogs and molecular detection of chloramphenicol resistance genes. Haryana Veterinarian 58, 66-69.
O'BrienO’Brien, T.F. (1997). The global epidemic nature of antimicrobial resistance and the need to monitor and manage it locally. Clinical Infectious Disease, 24, S2-S8. DOI: 10.1093/clinids/24.supplement1.s2
Onanuga, A., Oyi, A.R. and Onaolapo, J.A. (2005). Prevalence and susceptibility pattern of methicillinresistant Staphylococcus aureus isolates among healthy women in Zaria, Nigeria. African Journal of Biotechnology 4, 1321 1324. DOI: 10.1093/jac/dkm269
Pedersen, K., Pedersen, K., Jensen, H., Finster, K., Jensen, V.F. and Heuer, O.E. (2007). Occurrence of antimicrobial resistance in bacteria from diagnostic samples from dogs. Journal of Antimicrobial Chemotherapy, 60,775 781. DOI: 10.1093/jac/dkm269
Pinto, L., Radhouani, H., Coelho, C., da Costa, P.M., Simões, R., Brandão, R.M., Torres, C., Igrejas, G. and Poeta, P. (2010). Genetic detection of extended-spectrum β-lactamase-containing Escherichia coli isolates from birds of prey from Serra da Estrela natural reserve in Portugal. Applied and Environmental Microbiology, 76, 4118-4120. DOI: 10.1128/AEM.02761-09
Pitout, J.D. and Laupland, K.B. (2008). Extended-spectrum β-lactamase-producing Enterobacteriaceae: an emerging public-health concern. Lancet Infectious Disease. 8,159-166. DOI: 10.1016/S1473-3099(08)70041-0
Pitout, J.D.D., Thomson, K.S., Hanson, N.D., Ehrhardt, A.F., Moland, E.S. and Sanders, C.C. (1998). β-Lactamases responsible for resistance to expanded-spectrum cephalosporins in Klebsiellapneumoniae, Escherichia coli, and Proteus mirabilis isolates recovered in South Africa. Antimicrobial Agents and Chemotherapy. 42, 1350-1354. DOI: 10.1128/AAC.42.6.1350
Poeta, P., Costa, D., Rodrigues, J. and Torres, C. (2005). Study of faecal colonization by vanA-containing Enterococcus strains in healthy humans, pets, poultry and wild animals in Portugal. Journal of Antimicrobial Chemotherapy. 55,278-280. DOI: 10.1093/jac/dkh549
Saenz ,Y., Brinas, L., Domínguez, E., Ruiz, J., Zarazaga, M., Vila, J. and Torres. C. (2004). Mechanisms of resistance in multiple-antibiotic-resistant Escherichia coli strains of human, animal, and food origins. Antimicrobial Agents and Chemotherapy. 48, 3996-4001. DOI: 10.1128/AAC.48.10.3996-4001.2004
Seguin, M.A., Vaden A.C., Stone, E. and Levine, J.F. (2003). Persistent urinary tract infections and reinfections in 100 dogs (1989–1999). Journal of Veterinary Internal Medicine. 17, 622 631. DOI: 10.1111/j.1939-1676.2003.tb02492.x
Rweyemamu, M., Chakraborty, T., Mshana, S.E. (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, Frontiers in Microbiology, 11, 142.DOI: 10.3389/fmicb.2016.00142
Simjee, S., White, D.G., McDermott, P.F., Wagner, D.D., Zervos, M.J., Donabedian, S.M., English, L.L., Hayes, J.R. and Walker, R.D. (2002). Characterization of Tn1546 in vancomycin-resistant Enterococcus faecium isolated from canine urinary tract infections: evidence of gene exchange between human and animal enterococci. Journal of Clinical Microbiology. 40, 4659-4665.DOI: 10.1128/JCM.40.12.4659-4665.2002
Sodha, S.V., Lynch, M., Wannemuehler, K., Leeper, M., Malavet, M., Schaffzin, J., Chen, T., Langer, A., Glenshaw, M., Hoefer, D. and Dumas, N. (2011). Multistate outbreak of Escherichia coli O157: H7 infections associated with a national fast-food chain, 2006: a study incorporating epidemiological and food source traceback results. Epidemiology and Infection, 139,309 316. DOI: 10.1017/S0950268810000920
Sørum, H. and Sunde. M. (2001). Resistance to antibiotics in the normal flora of animals. Veterinary Research, 32, 227-241. DOI: 10.1051/vetres:2001121
Sow, A.G., Wane, A.A., Diallo, M.H., Boye, C.S.B. and Aïdara-Kane, A. (2007). Genotypic characterization of antibiotic-resistant Salmonella enteritidis isolates in Dakar, Senegal. Journal of Infection in Developing Countries,1,284-288.PMID: 19734606
Stokholm, J., Schjørring, S., Pedersen, L., Bischoff, A.L., Følsgaard, N., Carson, C.G., Chawes, B., Bønnelykke, K., Mølgaard, A., Krogfelt, K.A. and Bisgaard, H. (2012). Living with cat and dog increases vaginal colonization with E. coli in pregnant women. PLoS One. 7, 1-7. DOI.org/10.1371/journal.pone.0046226
Rubab, M. and Oh, D. H. (2021). Molecular Detection of Antibiotic Resistance Genes in Shiga Toxin-Producing E. coli Isolated from Different Sources. Antibiotics, 10(4), 344. DOI.org/10.3390/antibiotics10040344
Tramuta, C., Robino, P., Nucera, D., Salvarani, S., Banche, G., Malabaila, A. and Nebbia, P. (2014). Molecular characterization and antimicrobial resistance of faecal and urinary Escherichia coli isolated from dogs and humans in Italy. Veterinary Italia, 50,23-30. DOI: 10.12834/VetIt.1304.09
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