Hamdy, M., Mohammed, S., Farghali, H., Aboul-Ella, H., Marouf, S. (2025). Monitoring the Burden of the Antibiotic Resistance and Virulence Genes in Pet Animals Suffering from Bacterial Otitis. Journal of Applied Veterinary Sciences, 10(3), 62-77. doi: 10.21608/javs.2025.374908.1584
Mayson Hamdy; Soliman Mohammed; Haithem Farghali; Hassan Aboul-Ella; Sherif Marouf. "Monitoring the Burden of the Antibiotic Resistance and Virulence Genes in Pet Animals Suffering from Bacterial Otitis". Journal of Applied Veterinary Sciences, 10, 3, 2025, 62-77. doi: 10.21608/javs.2025.374908.1584
Hamdy, M., Mohammed, S., Farghali, H., Aboul-Ella, H., Marouf, S. (2025). 'Monitoring the Burden of the Antibiotic Resistance and Virulence Genes in Pet Animals Suffering from Bacterial Otitis', Journal of Applied Veterinary Sciences, 10(3), pp. 62-77. doi: 10.21608/javs.2025.374908.1584
Hamdy, M., Mohammed, S., Farghali, H., Aboul-Ella, H., Marouf, S. Monitoring the Burden of the Antibiotic Resistance and Virulence Genes in Pet Animals Suffering from Bacterial Otitis. Journal of Applied Veterinary Sciences, 2025; 10(3): 62-77. doi: 10.21608/javs.2025.374908.1584
Monitoring the Burden of the Antibiotic Resistance and Virulence Genes in Pet Animals Suffering from Bacterial Otitis
1Department of Microbiology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt
2Department of Internal Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt
3Department of Surgery, Anesthesiology, and Radiology, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt
Receive Date: 12 April 2025,
Revise Date: 22 May 2025,
Accept Date: 28 May 2025
Abstract
The etiology of otitis in dogs and cats is multifactorial and complex, involving bacterial and fungal pathogens. This study aimed to describe microbiological features and susceptibility profiles of bacterial pathogens associated with 212 cases of external otitis, comprising 118 dogs and 94 cats. Ear swabs were processed to identify bacterial etiologies following standard microbiological methods, followed by antibiotic sensitivity profiling of each obtained isolate and PCR screening for a list of virulence and resistance genes. The overall resistance incidence for the obtained isolates against amoxicillin was 3.8%, amoxicillin/clavulanic acid was 55.4%, ceftriaxone was 26.6%, ceftazidime was 27.5%, cefoperazone (22.9%), enrofloxacin (1.6%), gentamicin (9.9%), amikacin (7.2%), linezolid (92.8%), tylosin was 76%. PCR screening of isolated bacteria revealed that E. coli and K. pneumoniae harbored ESBL genes like blaTEM, blaCTX-M, and other resistance genes aadB and qnrB. Likewise, the other Gram-negative isolates of P. aeruginosa and P. mirabilis were also positive for the same resistance genes. Gram-positive S. aureus harbored blaZ and norA resistance genes. Current work provides priceless surveillance value in monitoring resistant bacteria in pet animals as Customized monitoring programs can help identify certain AMR frameworks, aid clinicians in making logical treatment choices, and restrict the selection and spread of AMR within the population.
ABOUL-ELLA, H., MOSALLAM, T., SAMIR, O., Ali, A., QASIM, A., MAHMOUD, H.E., and SAMIR, A., 2025. Emergence of Rhodotorula mucilaginosaamong pet animals: a possible public health risk on the move. BMC Microbiology 25: 273. https://doi.org/10.1186/s12866-025-03894-9
ALCANTAR-CURIEL M.D., LEDEZMA-ESCALANTE C.A., JARILLO-QUIJADA M.D., GAYSSO-VAZQUEZ C., MORFIN-OTERO R., RODRIGUEZ-NORIEGA E., CEDILLO-RAMIREZ M.L., SANTOS-PRECIADO J.I., and GIRON J.A., 2018. Association of Antibiotic Resistance, Cell Adherence, and Biofilm Production with the Endemicity of Nosocomial Klebsiella pneumoniae. BioMed Research International : 7012958. https://doi.org/10.1155/2018/7012958
ANGUS, J.C. 2004. Otic cytology in health and disease. Veterinary Clinics of North America: Small Animal Practice 34(2): 411-424. https://doi.org/10.1016/j.cvsm.2003.10.005
ARCHAMBAULT, M., PETROV, P., HENDRIKSEN, R.S., ASSEVA, G., BANGTRAKULNONTH, A., HASMAN, H., and AARESTUP, F.M., 2006. Molecular characterization and occurrence of extended-spectrum beta-lactamase resistance genes among Salmonella enterica serovar Corvallis from Thailand, Bulgaria, and Denmark. Microbial Drug Resistance 12(3): 192-198. https://doi.org/10.1089/mdr.2006.12.192
ATAYA, H.A., SOLIMAN, M.S., KAYAF, K.A.H., MAROUF, S., and AL-AMRY, K., 2023. Incidence, Bacterial causes and Antibiotic Resistance Patterns of Urinary Tract Infection in Pet Animals. Journal of Applied Veterinary Sciences 8(2): 35-43. https://dx.doi.org/10.21608/javs.2023.179690.1199
BAGCIL, A.F., TAPONEN, S., KOORT, J., BENGTSSON, B., MYLLYNIEMI, A.L., and PYORALA, S., 2012. Genetic basis of penicillin resistance of S. aureus isolated in bovine mastitis. Acta Veterinaria Scandinavica 54(1): 69. https://doi.org/10.1186/1751-0147-54-69
BAHT, S., MUTHUNATARAJAN, S., MULKI, S.S., ARCHANA, B.K., and KOTIAN, K.H., 2021. Bacterial Infection among Cancer Patients: Analysis of Isolates and Antibiotic Sensitivity Pattern. International Journal of Microbiology: 8883700. https://doi.org/10.1155/2021/8883700
BAHTI, T., NATHAWAT, P., SHARMA, S.K., YADAV, R., BISHOI, J., and KATARIA, A.K., 2016. Polymorphism in spa gene of Staphylococcus aureus from bovine subclinical mastitis. Veterinary World 9(4): 421-424. https://doi.org/10.14202/vetworld.2016.421-424
BAJWA, J. 2019. Canine otitis externa - Treatment and complications. The Canadian Veterinary Journal 60(1): 97-99.
BARUA A., BORUAH, D., PHUKAN, A., BAISHYA, B.C., DUTTA J.B., and BARMAN D., 2021. A study on the prevalence of otitis in dogs in Guwahati, Assam. Journal of Entomology and Zoology Studies 9(5): 214.
BORRIELLO, G., PARADISO, R., CATOZZI, C., BRUNETTI, R., ROCCABIANCA, P., RICCARDI, M.G., CECERE, B., LECCHI, C., FUSCO, G., CECILIANI, F., and GALIERO, G., 2020. Cerumen microbial community shifts between healthy and otitis affected dogs. PLoS ONE 15(11): e0241447. https://doi.org/10.1371/journal.pone.0241447
BROGAN, D.M., and MOSSIALOS, E., 2016. A critical analysis of the review on antimicrobial resistance report and the infectious disease financing facility. Global Health 12: 8. https://doi.org/10.1186/s12992-016-0147-y
BRUYETTE, D.S. 2020. Clinical Small Animal Internal Medicine Volume I, First Edition. John Wiley & Sons, Inc.
BUSH, K., and JACOBY, G.A., 2010. Updated functional classification of beta-lactamases. Antimicrobial Agents and Chemotherapy 54(3): 969-976. https://doi.org/10.1128/AAC.01009-09
CANDELLONE, A., BADINO, P., GIROLAMI, F., ALA, U., MINA, F., and ODORE, R., 2023. Dog Owners' Attitude toward Veterinary Antibiotic Use and Antibiotic Resistance with a Focus on Canine Diarrhea Management. Animals (Basel) 13(6): 1061. https://doi.org/10.3390/ani13061061
CANESCHI, A., BARDHI, A., BARBARISSA, A., and ZAGHINI, A., 2023. The Use of Antibiotics and Antimicrobial Resistance in Veterinary Medicine, a Complex Phenomenon: A Narrative Review. Antibiotics (Basel) 12(3): 487. https://doi.org/10.3390/antibiotics12030487
CHIPANGURA, J.K., EAGAR, H., KGOETE, M., ABERNETHY, D., and NAIDOO, V., 2017. An investigation of antimicrobial usage patterns by small animal veterinarians in South Africa. Preventive Veterinary Medicine 136: 29-38. https://doi.org/10.1016/j.prevetmed.2016.11.017
CHOI, N., EDGINTON, H.D., GRIFFIN, C.E., and ANGUS, J.C., 2018. Comparison of two ear cytological collection techniques in dogs with otitis externa. Veterinary Dermatology 29(5): 413-e136. https://doi.org/10.1111/vde.12664
CIFTCI, A., FINDIK, A., ONUK, E.E., and SAVASAN, S., 2009. Detection of methicillin resistance and slime factor production of Staphylococcus aureus in bovine mastitis. Brazilian Journal of Microbiology 40(2): 254-61. https://doi.org/10.1590/S1517-83822009000200009
CLSI (Clinical and Laboratory Standards Institute), 2022. Performance standards for antimicrobial susceptibility testing. 31st ed. CLSI supplement M100. USA
COLOM, K., PEREZ, J., ALONSO, R., FERNANDEZ-ARANGUIZ, A., LARINO, E., and CISTERNA, R., 2003. Simple and reliable multiplex PCR assay for detection of blaTEM, bla(SHV) and blaOXA-1 genes in Enterobacteriaceae. FEMS Microbiology Letters 223(2): 147-151. https://doi.org/10.1016/S0378-1097(03)00306-9
DELICATO, E.R., DE BRITO, B.G., GAZIRI L.C., and VIDOTTO, M.C., 2003. Virulence-associated genes in Escherichia coli isolates from poultry with colibacillosis. Veterinary Microbiology 94(2): 97-103. https://doi.org/10.1016/s0378-1135(03)00076-2
FATHI, M.M., SAMIR, A., MAROUF, S., ALI, A.R., and AL-AMRY, K., 2022. Phenotypic and Genotypic Characteristics of Antimicrobial Resistance of Gram-negative Bacteria isolated From Pet Animal. Journal of Advanced Veterinary Research 12(5): 597-604. Retrieved from https://www.advetresearch.com/index.php/AVR/article/view/1073
FERNANDEZ, G., BARBOZA, G., VILLALOBOS, A., PARRA, O., and RAMIREZ, G.F.R.A., 2006. Isolation and Identification of Microorganisms Present in 53 Dogs suffering otitis externa. Revista Científica 16(1): 23-30.
FRANA, T.S., CARLSON, S.A., and GRIFFITH, R.W., 2001. Relative distribution and conservation of genes encoding aminoglycosidemodifying enzymes in Salmonella enterica serotype Typhimurium phage type DT104. Applied and Environmental Microbiology 67(1): 445-448. https://doi.org/10.1128/AEM.67.1.445- 448.2001
HASSANIEN, H.A., SAYED, R.H., and ELYAZEED, H.S.A., 2021. Cross-sectional study on dermatological affections of companion animals caused by dermatophytes and other keratinophilic fungi in greater cairo area, Egypt. Advances in Animal Veterinary Sciences 9(4): 615-622. http://dx.doi.org/10.17582/journal.aavs/2021/9.4.615.622
HATA, A., FUJITANI, N., ONO, F., and YOSHIKAWA, Y., 2022. Surveillance of antimicrobial-resistant Escherichia coli in Sheltered dogs in the Kanto Region of Japan. Scientific Reports 12(1): 773. https://doi.org/10.1038/s41598-021-04435-w
HU, Q., TU, J., HAN, X., ZHU, Y., DING, C., and YU, S., 2011. Development of multiplex PCR assay for rapid detection of Riemerella anatipestifer, Escherichia coli, and Salmonella enterica simultaneously from ducks. Journal of Microbiological Methods 87(1): 64-69. https://doi.org/10.1016/j.mimet.2011.07.007
HUANG, J.T., ABRAMS, M., TLOUGAN, B., RADEMAKER, A., and PALLER, A.S., 2009. Treatment of Staphylococcus aureus colonization in atopic dermatitis decreases disease severity. Pediatrics 123(5): e808-14. https://doi.org/10.1542/peds.2008-2217
KAO, C.Y., UDVAL, U., HUANG, Y.T., WU, H.M., HUANG, A.H., BOLORMAA, E., YAN, J.J., URANGO, Z., BATBAATAR, G., KHOSBAYAR, T., and WU, J.J., 2016. Molecular characterization of extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella spp. isolates in Mongolia. Journal of Microbiology, Immunology, and Infection 49(5): 692-700. https://doi.org/10.1016/j.jmii.2015.05.009
KHALIFA, S.M., ABD EL-AZIZ, A.M., HASSAN, R., and ABDELMEGEED, E.S., 2021. β-lactam resistance associated with β-lactamase production and porin alteration in clinical isolates of E. coli and K. pneumoniae. PLoS One 16(5): e0251594. https://doi.org/10.1371/journal.pone.0251594
KUMAR, S., HUSSAIN, K., SHARMA, R., CHHIBBER, S., and SHARMA, N., 2014. Prevalence of Canine Otitis Externa in Jammu. Journal of Animal Research 4(1): 121-129. https://doi.org/10.5958/2277-940X.2014.00083.7
LEE, S., AN, J.U., GUK, J.H., SONG, H., YI, S., KIM, W.H., and CHO, S., 2021. Prevalence, Characteristics and Clonal Distribution of Extended-Spectrum β-Lactamase- and AmpC β-Lactamase-Producing Escherichia coli Following the Swine Production Stages, and Potential Risks to Humans. Frontiers in Microbiology 12: 710747. https://doi.org/10.3389/fmicb.2021.710747
LEFKADITIS, M.A., KOUKERI, S.E., and MIHALCA, A.D., 2009. Prevalence and intensity of Otodectes cynotis in kittens from Thessaloniki area, Greece. Veterinary Parasitology 63: 374-375.
LYSKOVA, P., VYDRZALOVA, M., and MAZUROVA, J., 2007. Identification and antimicrobial susceptibility of bacteria and yeasts isolated from healthy dogs and dogs with otitis externa. Journal of veterinary medicine. A, Physiology, pathology, clinical medicine 54(10): 559-563. https://doi.org/10.1111/j.1439-0442.2007.00996.x
MARQUES, C., BELAS, A., ABOIM, C., CAVACO-SILVA, P., TRIGUEIRO, G., GAMA, L.T., and POMBA, C., 2019. Evidence of Sharing of Klebsiella pneumoniae Strains between Healthy Companion Animals and Cohabiting Humans. Journal of Clinical Microbiology 57(6): e01537-18. https://doi.org/10.1128/JCM.01537-18
MARTIN, R.M., CAO, J., BRISSE, S., PASSET, V., WU, W., ZHA, L., MALANI, P.N., RAO, K., and BACHMAN, M.A., 2016. Molecular Epidemiology of Colonizing and Infecting Isolates of Klebsiella pneumoniae. mSphere 1(5): e00261-16. https://doi.org/10.1128/mSphere.00261-16
MARUVE, S.A., and ESSACK, S.Y., 2022. Knowledge, attitudes, and practices of veterinarians on antibiotic use and resistance and its containment in South Africa. Journal of the South African Veterinary Association 93(2): 99-108. https://doi.org/10.36303/JSAVA.164
MATAR, G.M., RAMLAWI, F., HIJAZI, N., KHNEISSER, I., and ABDELNOOR, A.M., 2002. Transcription levels of Pseudomonas aeruginosa exotoxin a gene and severity of symptoms in patients with otitis externa. Current Microbiology 45(5): 350-354. https://doi.org/10.1007/s00284-002-3703-z
MOUSSA, I.M., ELJAKEE, G., BEDER, M., ABDELAZIZ, K., MUBARAK, A.S., DAWOUD, T.M., HEMEG, H.A., ALSUBKI, R.A., KABLI, A.A., and MAROUF, S., 2021. Zoonotic risk and public health hazards of companion animals in the transmission of Helicobacter species, Journal of King Saud University – Science 33(6). https://doi.org/10.1016/j.jksus.2021.101494
NOLI, C., MINAFO, G., and GALZERANO, M., 2011. Quality of life of dogs with skin diseases and their owners. Part 1: development and validation of a questionnaire. Veterinary Dermatology. 22(4): 335-343. https://doi.org/10.1111/j.1365-3164.2010.00954.x
NUTTALL, T. 2023. Managing recurrent otitis externa in dogs: what have we learned and what can we do better? AVMA - Journal of the American Veterinary Medical Association 261(1): 10-22. https://doi.org/10.2460/javma.23.01.0002
O'NEILL, A.M., WORTHING, K.A., KULKARNI, N., LI, F., NAKATSUJI, T., MCGROSSO, D., MILLS, R.H., KALLA, G., CHENG, J.Y., NORRIS, J.M., POGLIANO, K., POGLIANO, J., GONZALEZ, D.J., and GALLO, R.L., 2021. Antimicrobials from a feline commensal bacterium inhibit skin infection by drug-resistant S. pseudintermedius. Elife :10:e66793. https://doi.org/10.7554/eLife.66793
PATERSON, S., and MATYSKIEWICZ, W.A., 2018. A study to evaluate the primary causes associated with Pseudomonas otitis in 60 dogs. Journal of Small Animal Practice 59(4): 238-242. https://doi.org/10.1111/jsap.12813
PATHIRANA, H.N.K.S., DE SILVA, B.C.J., WIMALASENA, S.H.M.P., and HOSSAIN, S., HEO, G.J., 2018. Comparison of virulence genes in Proteus species isolated from human and pet turtle. Iranian Journal of Veterinary Research 19(1): 48-52.
PESAVENTO, P.A., and MURPHY, B.G., 2014. Common and emerging infectious diseases in the animal shelter. Veterinary Pathology 51(2): 478-491. https://doi.org/10.1177/0300985813511129
POURMAND, M.R., YOUSEFI, M., SALAMI, S.A., and AMINI, M., 2014. Evaluation of expression of NorA efflux pump in ciprofloxacin resistant Staphylococcus aureus against hexahydroquinoline derivative by real-time PCR. Acta Medica Iranica 52(6): 424-429.
PYE, C. 2018.Pseudomonas otitis externa in dogs. The Canadian Veterinary Journal 59(11): 1231-1234.
ROBICSEK, A., JACOBY, G.A., and HOOPER, D.C., 2006. The worldwide emergence of plasmid-mediated quinolone resistance. The Lancet Infectious Diseases 6(10): 629-640. https://doi.org/10.1016/S1473-3099(06)70599-0
SEVILLA-NAVARRO, S., CATALA-GREGORI, P., TORRES-BONCOMPTE, J., ORENGA, M.T., GARCIA-LORENS, J., and CORTES, V., 2022. Antimicrobial Resistance Trends of Escherichia coli Isolates: A Three-Year Prospective Study of Poultry Production in Spain. Antibiotics (Basel) 11(8): 1064. https://doi.org/10.3390/antibiotics11081064
SMITH, D.R.M., DOLK, F.C.K., POUWELS, K.B., CHRISTIE, M., ROBOTHAM, J.V., and SMIESZEK, T., 2018. Defining the appropriateness and inappropriateness of antibiotic prescribing in primary care, Journal of Antimicrobial Chemotherapy 73: 11-18. https://doi.org/10.1093/jac/dkx503
SPILKER, T., COENYE, T., VANDAMME, P., and LIPUMA, J.J., 2004. PCR-based assay for differentiation of Pseudomonas aeruginosa from other Pseudomonas species recovered from cystic fibrosis patients. Journal of Clinical Microbiology 42(5): 2074-2079. https://doi.org/10.1128/JCM.42.5.2074-2079.2004
SUMMERS, J.F., O'NEILL, D.G., CHURCH, D., COLLINS, L., SARGAN, D., and BRODBELT, D.C., 2019. Health-related welfare prioritisation of canine disorders using electronic health records in primary care practice in the UK. BMC Veterinary Research 15(1): 163. https://doi.org/10.1186/s12917-019-1902-0
TOPALA, R., BURTAN, I., FANTANARU, M., CIOBANU, S., and BURTAN, L.C., 2007. Epidemiological studies of otitis externa at carnivores. Lucrari Stiinlifice Medicina Veterinara 40: 647-651.
TURTON, J.F., PERRY C., ELGOHARI S., and HAMPTON C.V., 2010. PCR characterization and typing of Klebsiella pneumoniae using capsular type-specific, variable number tandem repeat and virulence gene targets. Journal of Medical Microbiology 59(5): 541-547. https://doi.org/10.1099/jmm.0.015198-0
VON WINTERSDORFF, C.J., PENDERS, J., VAN NIEKERK J.M., MILLS, N.D., MAJUMDER, S., VAN ALPHEN, L.B., SAVELKOUL, P.H., and WOLFFS, P.F., 2016. Dissemination of Antimicrobial Resistance in Microbial Ecosystems through Horizontal Gene Transfer. Frontiers in Microbiology 7: 173. https://doi.org/10.3389/fmicb.2016.00173
WALY, N.E., and SAYED, R.K., 2013. Demography of Small Animal Cases in Assiut between Years 2007-2010: A Retrospective Study of 312 Cases. Assiut Veterinary Medical Journal 59(136): 81-87. https://doi.org/10.21608/avmj.2013.171067
YAGUCHI, K., OGITANI, T., OSAWA, R., KAWANO, M., KOKUMAI, N., KANESHIGE, T., NORO, T., MASUBUCHI, K., and SHIMIZU, Y., 2007. Virulence factors of avian pathogenic Escherichia coli strains isolated from chickens with colisepticemia in Japan. Avian Diseases 51(3): 656-662. https://doi.org/10.1637/0005-2086(2007)51
YEH, K.M., KURUP, A., SIU, L.K., KOH, Y.L., FUNG, C.P., LIN, J.C., CHEN, T.L., CHANG, F.Y., and KOH, T.H., 2007. Capsular serotype K1 or K2, rather than magA and rmpA, is a major virulence determinant for Klebsiella pneumoniae liver abscess in Singapore and Taiwan. Journal of Clinical Microbiology 45(2): 466-471. https://doi.org/10.1128/JCM.01150-06
ZHANG, H.L., GONTIES, K.J., HAN, J.H., ALBY, K., LAPP, Z., SNITKIN, E., GOLDSTEIN, E.J.C., MULDOON, S., TOLOMEO, P., and LAUTENBACH, E., 2023. Characterization of resistance to newer antimicrobials among carbapenem-resistant Klebsiella pneumoniae in the post-acute-care setting. Infection Control and Hospital Epidemiology 44(7): 1159-1162. https://doi.org/10.1017/ice.2022.185
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