Antibiotic resistance constitutes a significant public health challenge, with diverse reservoirs of resistant bacteria playing pivotal roles in their dissemination. Among these reservoirs, pets are carrying antibiotic-resistant strains. The objective of this study was to assess the resistance profiles of Escherichia coli, and the prevalence of extended-spectrum β-lactamase (ESBL) producing E. coli strains in dogs and cats from Tamaulipas, Mexico. A total of 300 stool samples (150 dogs and 150 cats) from healthy pets were subjected to analysis. Antibiotic susceptibility testing and the identification of ESBLs were carried out by disc diffusion method. The presence of resistance genes, class 1, 2, and 3 integrons (intI1, intI2, and intI3) and phylogroups was determined by PCR analysis. The findings reveal that 42.6% (128/300) of the strains exhibited resistance to at least one of the eight antibiotics assessed, and 18.6% (56/300) demonstrated multidrug resistance (MDR), that distributed across 69 distinct resistance patterns. Altogether 2.6% of E. coli strains (8/300) were confirmed as TEM and CTX-M type ESBL producers. These outcomes underscore the roles of dogs and cats in Tamaulipas as reservoirs for the dissemination of MDR and/or ESBL strains. The results underscore the necessity for conducting prevalence studies on ESBL-producing E. coli, forming a foundation for comprehending the present scenario and formulating strategies for the control and mitigation of this issue.
Miranda C, Silva V, Igrejas G, Poeta P. Impact of European pet antibiotic use on Enterococci and Staphylococci antimicrobial resistance and human health. Future Microbiol 2021; 16(3): 185–201.
Ghimpețeanu OM, Pogurschi EN, Popa DC, Dragomir N, Drăgotoiu T, Mihai OD, et al. Antibiotic use in livestock and residues in food—a public health threat: a review. Foods 2022; 11(10): 1430.
WHO. Global antimicrobial resistance and use surveillance system (GLASS) report. Geneva, Switzerland; 2022. Available from: https://www.who.int/publications/i/item/9789240062702, Accessed 10 November 2023.
Walsh TR, Gales AC, Laxminarayan R, Dodd PC. Antimicrobial resistance: addressing a global threat to humanity. Plos Med 2023; 20(7): e1004264.
Pormohammad A, Nasiri MJ, Azimi T. Prevalence of antibiotic resistance in Escherichia coli strains simultaneously isolated from humans, animals, food, and the environment: a systematic review and meta-analysis. Infect Drug Resist 2019; 12: 1181–1197.
Oh SS, Song J, Kim J, Shin J. Increasing prevalence of multidrug-resistant mcr-1-positive Escherichia coli isolates from fresh vegetables and healthy food animals in South Korea. Int J Infect Dis 2020; 92: 53–55.
Wang H, Qi JF, Qin R, Ding K, Graham DW, Zhu Y. Intensified livestock farming increases antibiotic resistance genotypes and phenotypes in animal feces. Commun Earth Environ 2023; 4(123).
Treskova M, Kuhlmann A, Freise F, Kreienbrock L, Brogden S. Occurrence of antimicrobial resistance in the environment in Germany, Austria, and Switzerland: a narrative review of existing evidence. Microorganisms 2022; 10(4): 728.
Xiao R, Huang D, Du L, Song B, Yin L, Chen Y, et al. Antibiotic resistance in soil-plant systems: a review of the source, dissemination, influence factors, and potential exposure risks. Sci Total Environ 2023; 869: 161855.
Wu J, Wang J, Li Z, Guo S, Li K, Xu P, et al. Antibiotics and antibiotic resistance genes in agricultural soils: a systematic analysis. Crit Rev Environ Sci Technol 2023; 57(7): 847–864.
Arsand JB, Hoff RB, Jank L, Bussamara R, Dallegrave A, Bento FM, et al. Presence of antibiotic resistance genes and its association with antibiotic occurrence in Dilúvio River in southern Brazil. Sci Total Environ 2020; 738: 139781.
Grenni P. Antimicrobial resistance in rivers: a review of the genes detected and new challenges. Environ Toxicol Chem 2022; 41(3): 687–714.
Morina JC, Franklin RB. Drivers of antibiotic resistance gene abundance in an urban river. Antibiotics (Bases) 2023; 12(8): 1270.
Ramadan H, Jackson CR, Frye JG, Hiott LM, Samir M, Awad A, et al. Antimicrobial resistance, genetic diversity and multilocus sequence typing of Escherichia coli from humans, retail chicken and ground beef in Egypt. Pathogens 2020; 9(5): 357.
Brunn A, Kadri-Alabi Z, Moodley A, Guardabassi L, Taylor P, Mateus A, et al. Characteristics and global occurrence of human pathogens harboring antimicrobial resistance in food crops: a scoping review. Front Sustain Food Syst 2022; 6: 824714.
Rega M, Andriani L, Poeta A, Bonardi S, Conter M, Bacci C. The pork food chain as a route of transmission of antimicrobial resistant Escherichia coli: a farm-to-fork perspective. Antibiotics (Basel) 2023; 12(2): 376.
Bhat AH. Bacterial zoonoses transmitted by household pets and as reservoirs of antimicrobial resistant bacteria. Microb Pathog 2021; 155: 104891.
Marchetti L, Buldain D, Gortari L, Buchamer A, Chirino M, Mestorino N. Pet and stray dogs as reservoirs of antimicrobial-resistant Escherichia coli. Int J Microbiol 2021: 6664557.
Dróżdż M, Małaszczuk M, Paluch E, Pawlak A. Zoonotic potential and prevalence of Salmonella serovars isolated from pets. Infect Ecol Epidemiol 2021; 11(1): 1975530.
Melo LC, Oresco C, Leigue L, Netto HM, Melville PA, Benites PA, et al. Prevalence and molecular features of ESBL/pAmpC-producing Enterobacteriaceae in healthy and diseased companion animals in Brazil. Vet Microbiol 2018; 221: 59–66.
Dupouy V, Abdelli M, Moyano G, Arpaillange N, Bibbal D, Cadiergues MC, et al. Prevalence of beta-lactam and quinolone/fluoroquinolone resistance in Enterobacteriaceae from dogs in France and Spain-characterization of ESBL/pAmpC isolates, genes, and conjugative plasmids. Front Vet Sci 2019; 6: 279.
Wang Y, Zhou J, Li X, Ma L, Cao X, Hu W, et al. Genetic diversity, antimicrobial resistance and extended-spectrum β-lactamase type of Escherichia coli isolates from chicken, dog, pig and yak in Gansu and Qinghai Provinces, China. J Glob Antimicrob Resist 2020; 22: 726–732.
Takagi H, Yamane K, Matsui M, Suzuki S, Ito K. Pathotypes and drug susceptibility of Escherichia coli isolated from companion dogs in Japan. Jpn J Infect Dis 2020; 73(3): 253–522.
Aurich S, Prenger-Berninghoff E, Ewers C. Prevalence and antimicrobial resistance of bacterial uropathogens isolated from dogs and cats. Antibiotics (Basel) 2022; 11(12): 1730.
Sun L, Meng N, Wang Z, Hong J, Dai Y, Wang Z, et al. Genomic characterization of ESBL/AmpC-producing Escherichia coli in stray dogs sheltered in Yangzhou, China. Infect Drug Resist 2022; 15: 7741–7750.
Haulisah NA, Hassan L, Jajere SM, Ahmad NI, Bejo SK. High prevalence of antimicrobial resistance and multidrug resistance among bacterial isolates from diseased pets: retrospective laboratory data (2015–2017). PLoS One 2022; 17(12): e0277664.
Fayez M, Elmoslemany A, Al Romaihi AA, Azzawi AY, Almubarak A, Elsohaby I. Prevalence and risk factors associated with multidrug resistance and extended-spectrum b-lactamase producing E. coli isolated from healthy and diseased cats. Antibiotics (Basel) 2023; 12(2): 229.
Yasugi M, Hatoya S, Motooka D, Kondo D, Akiyoshi H, Horie M, et al. Genetic and phenotypic analyses of mcr-harboring extended-spectrum β-lactamase-producing Escherichia coli isolates from companion dogs and cats in Japan. Vet Microbiol 2023; 280: 109695.
Ramos S, Silva V, Dapkevicius MLE, Caniça M, Tejedor-Junco MT, Igrejas G, et al. Escherichia coli as commensal and pathogenic bacteria among food-producing animals: health implications of extended spectrum β-lactamase (ESBL) production. Animals (Basel) 2020; 10(12): 2239.
Nyirabahizi E, Tyson GH, Dessai U, Zhao S, Kabera C, Crarey E, et al. Evaluation of Escherichia coli as an indicator for antimicrobial resistance in Salmonella recovered from the same food or animal ceca samples. Food Control 2020; 115: 107280.
Zhang H, Xu J, Xiao O, Wang Y, Wang J, Zhu M, et al. Carbapenem-sparing beta-lactam/beta-lactamase inhibitors versus carbapenems for bloodstream infections caused by extended-spectrum beta-lactamase-producing Enterobacteriaceae: a systematic review and meta-analysis. Int J Inf Dis 2023; 128: 194–204.
Ortega-Paredes D, Haro M, Leoro-Garzón P, Barba P, Loaiza K, Mora F, et al. Multidrug-resistant Escherichia coli isolated from canine faeces in a public park in Quito, Ecuador. J Glob Antimicrob Resist 2019; 18: 263–268.
Salgado-Caxito M, Benavides JA, Adell AD, Paes AC, Moreno-Switt AI. Global prevalence and molecular characterization of extended-spectrum β-lactamase producing-Escherichia coli in dogs and cats – a scoping review and meta-analysis. One Health 2021; 12: 100236.
Derakhshandeh A, Eraghi V, Boroojeni AM, Niaki MA, Zare S, Naziri Z. Virulence factors, antibiotic resistance genes and genetic relatedness of commensal Escherichia coli isolates from dogs and their owners. Microb Pathog 2018; 116: 241–245.
Rocha-Gracia RC, Cortés-Cortés G, Lozano-Zarain P, Bello F, Martínez-Laguna Y, Torres C. Faecal Escherichia coli isolates from healthy dogs harbour CTX-M-15 and CMY-2 β-lactamases. Vet J 2015; 203(3): 315–319.
Galindo M. Reservoirs of CTX-M extended spectrum β-lactamase-producing Enterobacteriaceae in Oaxaca, Mexico. J Microbiol Exp 2019; 7(1): 43–47.
Vogel RF, Entian KD, Mecke D. Cloning and sequence of the mdh structural gene of Escherichia coli coding for malate dehydrogenase. Arch Microbiol 1987; 149(1): 36–42.
Vázquez-Villanueva J, Vázquez K, Martínez-Vázquez AV, Wong A, Hernández J, Cabrero-Martínez O, et al. Molecular and antimicrobial susceptibility characterization of Escherichia coli isolates from bovine slaughterhouse process. Antibiotics (Basel, Switzerland) 2023; 12(2): 291.
CLSI. Performance standards for antimicrobial susceptibility testing, 31st ed. CLSI supplement M100. Clinical and Laboratory Standards Institute; 2021. Available from: https://www.standards-global.com/wp-content/uploads/pdfs/preview/2247002.
Ng LK, Martin I, Alfa M, Mulvey M. Multiplex PCR for the detection of tetracycline-resistant genes. Mol Cell Probes 2001; 15(4): 209–215.
Kozak GK, Boerlin P, Janecko N, Reid-Smith RJ, Jardine C. Antimicrobial resistance in Escherichia coli isolates from swine and wild small mammals in the proximity of swine farms and natural environments in Ontario, Canada. Appl Environ Microbiol 2009; 75(3): 559–66.
Kargar M, Mohammadalipour Z, Doosti A, Lorzadeh S, Japoni-Nejad A. High prevalence of class 1 to 3 integrons among multidrug-resistant diarrheagenic Escherichia coli in Sothwest of Iran. Osong Public Health Res Perspect 2014; 5(4): 193–198.
EUCAST. The European committee on antimicrobial susceptibility testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 11.0; 2021.
Clermont O, Bonacorsi S, Bingen E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 2000; 66(10): 4555–8.
Hong JS, Song W, Park HM, Oh JY, Chae JC, Jeong S, et al. Molecular characterization of fecal extended-spectrum β-lactamase- and AmpC β-lactamase-producing Escherichia coli from healthy companion animals and cohabiting humans in South Korea. Front Microbiol 2020; 11: 674.
Zhou Y, Ji X, Liang B, Jiang B, Li Y, Yuan T, et al. Antimicrobial resistance and prevalence of extended spectrum-lactamase-producing Escherichia coli from dogs and cats in northeastern China from 2012 to 2021. Antibiotics (Basel) 2022; 11(11): 1506.
Joosten P, Ceccarelli D, Odent E, Sarrazin S, Graveland H, Van Compel L, et al. Antimicrobial usage and resistance in companion animals: a cross-sectional study in three European countries. Antibiotics (Basel) 2020; 9(2): 1–16.
Flament-Simon SC, De Toro M, García V, Blanco JE, Blanco M, Alonso MP, et al. Molecular characteristics of extraintestinal pathogenic E. coli (ExPEC), uropathogenic E. coli (UPEC), and multidrug resistant Escherichia coli isolated from healthy dogs in Spain. Whole genome sequencing of canine ST372 isolates and comparison with human isolates causing extraintestinal infections. Microorganisms 2020; 8(11): 1712.
Rodríguez-González MJ, Jiménez-Pearson MA, Duarte F, Poklepovich T, Campos J, Araya LN, et al. Multidrug-resistant CTX-M and CMY-2 producing Escherichia coli isolated from healthy household dogs from the great metropolitan area, Costa Rica. Microb Drug Resist 2020; 26(11): 1421–1428.
Chen Y, Liu Z, Zhang Y, Zhang Z, Lei L, Xia Z. Increasing prevalence of ESBL-producing multidrug resistance Escherichia coli from diseased pets in Beijing, China from 2012 to 2017. Front Microbiol 2019; 10: 2852.
Hritcu OM, Schmidt VM, Salem SE, Maciuca IE, Moraru RF, Lipovan I, et al. Geographical variations in virulence factors and antimicrobial resistance amongst Staphylococci isolated from dogs from the United Kingdom and Romania. Front Vet Sci 2020; 7: 414.
Guardabassi L, Prescott JF. Antimicrobial stewardship in small animal veterinary practice. Vet Clin North Am Small Anim Pract 2015; 45(2): 361–vii.
Yudhanto S, Varga C. Knowledge and attitudes of small animal veterinarians on antimicrobial use practices impacting the selection of antimicrobial resistance in dogs and cats in Illinois, United States: a spatial epidemiological approach. Antibiotics (Basel) 2023; 12(13): 542.
Carvalho AC, Barbosa AV, Arais LR, Ribeiro PF, Carneiro VC, Cerqueira AMF. Resistance patterns, ESBL genes, and genetic relatedness of Escherichia coli from dogs and owners. Braz J Microbiol 2016; 47(1): 150–158.
de Menezes MP, Facin AC, Cardozo MV, Costa MT, Moraes PC. Evaluation of the resistance profile of bacteria obtained from infected sites of dogs in a veterinary teaching hospital in Brazil: a retrospective study. Top Companion Anim Med 2021; 42: 100489.
Jung WK, Shin S, Park YK, Noh SM, Shin SR, Yoo HS, et al. Distribution and antimicrobial resistance profiles of bacterial species in stray dogs, hospital-admitted dogs, and veterinary staff in South Korea. Prev Vet Med 2020; 184: 105151.
Hughes LA, Williams N, Clegg P, Callaby R, Nuttall T, Coyne K, et al. Cross-sectional survey of antimicrobial prescribing patterns in UK small animal veterinary practice. Prev Vet Med 2012; 104(3–4): 309–316.
Boehmer T, Vogler AJ, Thomas A, Sauer S, Hergenroether M, Straubinger RK, et al. Phenotypic characterization and whole genome analysis of extended-spectrum beta-lactamase-producing bacteria isolated from dogs in Germany. PLoS One 2018; 13(10): e0206252.
Carvalho I, Cunha R, Martins C, Martínez-Álvarez S, Safia N, Pimenta P, et al. Antimicrobial resistance genes and diversity of clones among faecal ESBL-producing Escherichia coli isolated from healthy and sick dogs living in Portugal. Antibiotics (Basel) 2021; 10(8): 1013.
de Oliveira PA, Moura RA, Rodrigues GV, Lopes KFC, Zaniolo MM, Rubio KAJ, et al. 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: 829.
Abreu-Salinas F, Díaz D, García I, Lumbreras P, López AM, Fidalgo LE, et al. High prevalence and diversity of cephalosporin-resistant Enterobacteriaceae including extraintestinal pathogenic E. coli CC648 lineage in rural and urban dogs in northwest Spain. Antibiotics (Basel, Switzerland) 2020; 9(8): 468.
Baede VO, Wagenaar JA, Broens EM, Duim B, Dohmen W, Nijsse R, et al. Longitudinal study of extended-spectrum lactamase and AmpC-producing Enterobacteriaceae in household dogs. Antimicrob Agents Chemother 2015; 59(6): 3117–3124.
Deepthi B, Srivani M, Ramani RN, Chaitanya Y. Detection of extended spectrum beta-lactamase (ESBL) producing Escherichia coli in companion dogs. Pharma Innov 2020; 9(9S): 189–194.
Gumus B, Celik B, Kahraman BB, Sigirci BD, Ak S. Determination of extended spectrum beta-lactamase (ESBL) and AmpC beta-lactamase producing Escherichia coli prevalence in faecal samples of healthy dogs and cats. Rev Med Vet 2017; 168: 46–52.
Abbas G, Khan I, Mohsin M, Sajjad-Ur-Rahman, Younas T, Ali S. High rates of CTX-M group-1 extended-spectrum β-lactamases producing Escherichia coli from pets and their owners is Faisalabad, Pakistan. Infect Drug Resist 2019; 12: 571–578.
Telling K, Brauer A, Laht M, Kalmus P, Toompere K, Kisand V, et al. Characteristics of extended-spectrum beta-lactamase-producing Enterobacteriaceae and contact to animals in Estonia. Microorganisms 2020; 8(8): 1130.
Ma L, Li AD, Yin XL, Zhang T. The Prevalence of integrons as the carrier of antibiotic resistance genes in natural and man-made environments. Environ Sci Technol 2017; 51(10): 5721–5728.
Toombs LJ, Benschopa J, Frencha NP, Biggsa PJ, Midwintera AC, Marshalla JC, et al. Carriage of extended-spectrum beta-lactamase-and AmpC beta-lactamase-producing Escherichia coli from humans and pets in the same households. Appl Environ Microbiol 2020; 86(24): e01613–20.
Nji E, Kazibwe J, Hambridge T, Joko CA, Larbi AA, Damptey LAO, et al. High prevalence of antibiotic resistance in commensal Escherichia coli from healthy human sources in community settings. Sci Rep 2021; 11(1): 3372.
Bourne JA, Chong WL, Gordon DM. Genetic structure, antimicrobial resistance, and frequency of human associated Escherichia coli sequence types among faecal isolates from healthy dogs and cats living in Canberra, Australia. PloS one 2019; 14(3): e0212867.
Majowicz SE, Scallan E, Jones-Bitton A, Sargeant JM, Stapleton J, Angulo FJ, et al. Global incidence of human shiga toxin–producing Escherichia coli infections and deaths: a systematic review and knowledge synthesis. Foodborne Pathog Dis 2014; 11(6): 447–455.
Vega-Manriquez XD, Ubiarco A, Verdugo A, Hernández U, Navarro A, Ahumada RE, et al. Pet dogs potential transmitters of pathogenic Escherichia coli with resistance to antimicrobials. Arch Microbiol 2020; 202(5): 1173–1179.