Multidrug-resistant bacteria recovered from the respiratory and reproductive tracts of horses from Mayabeque, Cuba
Article Sidebar
Main Article Content
Abstract
Antimicrobial resistance in bacteria isolated from horses represents a threat to global health due to the close relationship of these animals with humans. This study aimed to elucidate the antimicrobial susceptibility profiles of bacteria with pathogenic and zoonotic potential, isolated from the respiratory and genital tracts of horses in Mayabeque, Cuba. Nasal and genital exudates were collected from twenty-three horses, and the isolates obtained were identified using the analytical profile index and mass spectrometry. The minimum inhibitory concentration (MIC) of thirteen antibiotics was determined for the isolates. Twenty-three bacterial isolates, including one Streptococcus uberis, sixteen Enterococcus spp., three Staphylococcus sciuri, one Morganella morganii, and two Stenotrophomonas maltophilia, were obtained. S. uberis showed resistance to gentamicin, enrofloxacin, and doxycycline, while enterococci isolates displayed resistance to doxycycline (n=16), rifampicin (n=8), erythromycin (n=7), enrofloxacin (n=3), and chloramphenicol (n=1). All S. sciuri isolates were resistant to at least six antibiotics, including methicillin, with high MIC values for erythromycin (>8192 µg/ml), doxycycline (128 µg/ml), and gentamicin (64 µg/ml). M. morganii isolate was resistant to three antibiotics, with MICs of 128 μg/ml and 256 μg/ml for cefquinome and doxycycline, respectively. S. maltophilia isolates exhibited resistance to cefquinome, with MIC values of 512 μg/ml and 128 μg/ml, respectively. The 91.3% of the isolates were multiresistant to antimicrobials, which represents the first detection in Cuba of bacteria with multiresistance phenotypes, isolated from samples of the nasal and genital mucosa of horses.
Article Details
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.
National Center for Animal and Plant Health (CENSA)References
Orand JP, Moulin G, Vindel EE. Combatting antimicrobial resistance through a One Health approach: actions and OIE strategy. 84th General Session Paris, France: World Organization of Animal Health (WOAH); 2016. p. 10.
World Health Organization (WHO). Global action plan on antimicrobial resistance. Organization WH, editor. Geneva, Switzerland: World Health Organization; 2015.
Pinto Jimenez CE, Keestra S, Tandon P, Cumming O, Pickering AJ, Moodley A, et al. Biosecurity and water, sanitation, and hygiene (WASH) interventions in animal agricultural settings for reducing infection burden, antibiotic use, and antibiotic resistance: a One Health systematic review. Lancet Planet Health. 2023;7 (5):e418-e434. DOI: 10.1016/S2542-5196(23)00049-9
van Duijkeren E, Ten Horn L, Wagenaar JA, de Bruijn M, Laarhoven L, Verstappen K, et al. Suspected horse-to-human transmission of MRSA ST398. Emerg Infect Dis. 2011;17(6): 1137-1139. DOI: 10.3201/eid1706.101330
Sack A, Oladunni FS, Gonchigoo B, Chambers TM, Gray GC. Zoonotic diseases from horses: a systematic review. Vector Borne Zoonotic Dis. 2020;20(7):484-495. DOI: 10.1089/vbz.2019.2541
Clark C, Greenwood S, Boison JO, ChirinoTrejo M, Dowling PM. Bacterial isolates from equine infections in western Canada (19982003). Can Vet J. 2008;49(2):153-160.
Fonseca JD, Mavrides DE, Morgan AL, Na JG, Graham PA, McHugh TD. Antibiotic resistance in bacteria associated with equine respiratory disease in the United Kingdom. Vet Record. 2020;187(5):1-6. DOI: 10.1136/vr.105842
Al-Kass Z, Eriksson E, Bagge E, Wallgren M, Morrell JM. Bacteria detected in the genital tract, semen or pre-ejaculatory fluid of Swedish stallions from 2007 to 2017. Acta Vet Scand. 2019;61(1):1-6. DOI: 10.1186/s13028-019-0459-z
Paudel R, Dogra P, Montgomery-Yates AA, Coz Yataco A. Procalcitonin: a promising tool or just another overhyped test? Int J Med Sci. 2020; 17(3):332-337. DOI: 10.7150/ijms.39367
Martins L, Gonçalves JL, Leite RF, Tomazi T, Rall VLM, Santos MV. Association between antimicrobial use and antimicrobial resistance of Streptococcus uberis causing clinical mastitis. J Dairy Sci. 2021;104(11):12030-12041. DOI: 10. 3168/jds.2021-20177
Uchida-Fujii E, Niwa H, Kinoshita Y, Nukada T. Matrix-Assisted Laser Desorption IonizationTime of Flight Mass Spectrometry (MALDITOF MS) for identification of bacterial isolates from horses. J Equine Vet Sci. 2020;95:103276. DOI: 10.1016/j.jevs.2020.103276
Salam MA, Al-Amin MY, Pawar JS, Akhter N, Lucy IB. Conventional methods and future trends in antimicrobial susceptibility testing. Saudi J Biol Sci. 2023;30(3):103582. DOI: 10.10 16/j.sjbs.2023.103582
Fouché N, Gerber V, Thomann A, Perreten V. Antimicrobial susceptibility patterns of blood culture isolates from foals in Switzerland. Schweiz Arch Tierheilkd. 2018;160(11): 665671. DOI: 10.17236/sat00184
Díaz-Sánchez AA, Corona-González B, Chilton NB, Lobo-Rivero E, Vega-Cañizares E, YrurzunEstrada C, et al. Molecular detection and identification of tick-borne pathogens in Equus caballus and ticks from western Cuba. Biotecnol Apl. 2022;39(2):2501-2505.
Ramón-Martínez A, Pupo-Batista F, RoblejoArias L, Díaz Sánchez A, Miranda-Cabrera I, Corona González B, et al. Detection of microorganisms of the class Mollicutes associated to the respiratory-reproductive complex in horses from Mayabeque, Cuba. Rev Salud Anim. 2019;41(3):1-11.
Salas-Romero J, Gómez-Cabrera KA, Salas JE, Vázquez R, Arenal A, Nielsen MK. First report of anthelmintic resistance of equine cyathostomins in Cuba. Vet Parasitol Reg Stud Reports. 2018;13:220-223. DOI: 10.1016/j.vprsr. 2018.07.005
Rasmussen CD, Haugaard MM, Petersen MR, Nielsen JM, Pedersen HG, Bojesen AM. Streptococcus equi subsp. zooepidemicus isolates from equine infectious endometritis belong to a distinct genetic group. Vet Res. 2013;44:26. DOI: 10.1186/1297-9716-44-26
Clinical and Laboratory Standards Institute (CLSI). VET08 Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 4th ed. Wayne, USA: Clinical and Laboratory Standards Institute; 2018. 200 p.
European Committee on Antimicrobial Susceptibility Testing (EUCAST). Breakpoint tables for interpretation of MICs and zone diameters. Version 13.0 ed. Available online: http://www.eucast.org: EUCAST; 2023. 110 p.
Clinical and Laboratory Standards Institute (CLSI). M100 Performance standards for antimicrobial susceptibility testing. 28th ed. Wayne, USA: Clinical and Laboratory Standards Institute; 2018. 296 p.
Sweeney MT, Lubbers BV, Schwarz S, Watts JL. Applying definitions for multidrug resistance, extensive drug resistance and pandrug resistance to clinically significant livestock and companion animal bacterial pathogens. J Antimicrob Chemother. 2018;73(6):1460-1463. DOI: 10.109 3/jac/dky043
Sukmawinata E, Sato W, Uemura R, Kanda T, Kusano K, Kambayashi Y, et al. Antimicrobialresistant Enterococcus faecium and Enterococcus faecalis isolated from healthy thoroughbred racehorses in Japan. J Equine Vet Sci. 2020;94: 103232. DOI: 10.1016/j.jevs.2020.103232
Nielsen SS, Bicout DJ, Calistri P, Canali E, Drewe JA, Garin-Bastuji B, et al. Assessment of animal diseases caused by bacteria resistant to antimicrobials: horses. EFSA J. 2021;19(12): 7112. DOI: 10.2903/j.efsa.2021.7112
Sherwin VE, Egan SA, Green MJ, Leigh JA. Survival of Streptococcus uberis on bedding substrates. Vet J. 2021;276:105731. DOI: 10.10 16/j.tvjl.2021.105731
Rosa NM, Duprè I, Azara E, Longheu CM, Tola S. Molecular typing and antimicrobial susceptibility profiles of Streptococcus uberis isolated from sheep milk. Pathogens (Basel, Switzerland). 2021;10:1489. DOI: 10.3390/patho gens10111489
Hayes K, O'Halloran F, Cotter L. A review of antibiotic resistance in Group B Streptococcus: the story so far. Crit Rev Microbiol. 2020;46(3): 253-269. DOI: 10.1080/1040841X.2020.1758626
Nocera FP, D'Eletto E, Ambrosio M, Fiorito F, Pagnini U, De Martino L. Occurrence and antimicrobial susceptibility profiles of Streptococcus equi subsp. zooepidemicus strains isolated from mares with fertility problems. Antibiotics. 2022;11(25):1-11. DOI: 10.3390/anti biotics11010025
Zhang T, Niu G, Boonyayatra S, Pichpol D. Antimicrobial resistance profiles and genes in Streptococcus uberis associated with bovine mastitis in Thailand. Front Vet Sci. 2021;8: 705338. DOI: 10.3389/fvets.2021.705338
Ahasan MS, Picard J, Elliott L, Kinobe R, Owens L, Ariel E. Evidence of antibiotic resistance in Enterobacteriales isolated from green sea turtles, Chelonia mydas on the Great Barrier Reef. Mar Pollut Bull. 2017;120 (12):18-27. DOI: 10.1016/j.marpolbul.2017.04.046
Yoshino Y. Enterococcus casseliflavus infection: a review of clinical features and treatment. Infect Drug Resist. 2023;16:363-368. DOI: 10.2147/ IDR.S398739
Stefanetti V, Beccati F, Passamonti F, Sgariglia E, Coletti M, Vuerich M, et al. Detection and DNA quantification of Enterococcus casseliflavus in a foal with septic meningitis. J Am Vet Med Assoc. 2016;249(1):96-100. DOI: 10.2460/javma.249.1.96
Nocera FP, Papulino C, Del Prete C, Palumbo V, Pasolini MP, De Martino L. Endometritis associated with Enterococcus casseliflavus in a mare: a case report. Asian Pac J Trop Biomed. 2017;7(8):760-762. DOI: 10.1016/j.apjtb.2017. 07.016
Malaluang P, Wilén E, Frosth S. Vaginal bacteria in mares and the occurrence of antimicrobial resistance. Microorganisms. 2022;10:2204. DOI: 10.3390/microorganisms10112204
Anyanwu MU, Okorie-Kanu OJ, Ogugua AJ, Ezenduka EV, Anidebe CO. Occurrence, antibiogram and vancomycin resistance of generic enterococci in horses in Nigeria. Revue Méd Vét. 2019;170(1-3):46-52.
Kim DH, Chung YS, Park YK, Yang SJ, Lim SK, Park YH, et al. Antimicrobial resistance and virulence profiles of Enterococcus spp. isolated from horses in Korea. Comp Immunol Microbiol Infect Dis. 2016;48:6-13. DOI: 10.1016/j.cim id .2016.07.001
Deshpande LM, Fritsche TR, Moet GJ, Biedenbach DJ, Jones RN. Antimicrobial resistance and molecular epidemiology of vancomycin-resistant enterococci from North America and Europe: a report from the SENTRY antimicrobial surveillance program. Diagn Microbiol Infect Dis. 2007;58(2):163-170. DOI: 10.1016/j.diagmicrobio.2006.12.022
Torres C, Alonso CA, Ruiz-Ripa L, LeónSampedro R, Del Campo R, Coque TM. Antimicrobial Resistance in Enterococcus spp. of animal origin. Microbiol Spectr. 2018;6(4): ARBA-0032-2018. DOI: 10.1128/microbiolspec. ARBA-0032-2018
Fungwithaya P, Boonchuay K, Narinthorn R, Sontigun N, Sansamur C, Petcharat Y, et al. First study on diversity and antimicrobial-resistant profile of staphylococci in sports animals of Southern Thailand. Vet World. 2022;15(3): 765-774. DOI: 10.14202/vetworld.2022.765-774
Mama OM, Gómez P, Ruiz-Ripa L, Gómez-Sanz E, Zarazaga M, Torres C. Antimicrobial resistance, virulence, and genetic lineages of staphylococci from horses destined for human consumption: high detection of S. aureus isolates of lineage ST1640 and those carrying the lukPQ gene. Animals. 2019;9:900. DOI: 10.3390/ani91 10900
Miklasińska-Majdanik M. Mechanisms of resistance to macrolide antibiotics among Staphylococcus aureus. Antibiotics. 2021;10 (11):1-23. DOI: 10.3390/antibiotics10111406
Urban-Chmiel R, Marek A, Stępień-Pyśniak D, Wieczorek K, Dec M, Nowaczek A, et al. Antibiotic resistance in bacteria - a review. Antibiotics. 2022;11(8):1079. DOI: 10.3390/anti biotics11081079
Garcia-Aroca T, Souza SSR, Ikhimiukor OO, Marcovici MM, Smith JT, Amador S, et al. Genome sequencing of methicillin-resistant and methicillin-susceptible Mammaliicoccus sciuri from diseased animals. Microbiol Resour Announc. 2022;11(10):e0071422. DOI: 10.1128/ mra.00714-22
Hurni JI, Kaiser-Thom S, Gerber V, Keller JE, Collaud A, Fernandez J, et al. Prevalence and whole genome-based phylogenetic, virulence and antibiotic resistance characteristics of nasal Staphylococcus aureus in healthy Swiss horses. Schweiz Arch Tierheilkd. 2022;164(7):499-512. DOI: 10.17236/sat00360
Hou Z, Liu L, Wei J, Xu B. Progress in the prevalence, classification and drug resistance mechanisms of methicillin-resistant Staphylococcus aureus. Infect Drug Resist. 2023;16:3271-3292. DOI: 10.2147/IDR.S412308
Hassanzadeh S, Ganjloo S, Pourmand MR, Mashhadi R, Ghazvini K. Epidemiology of efflux pumps genes mediating resistance among Staphylococcus aureus: a systematic review. Microb Pathog. 2020;139:103850. DOI: 10.101 6/j.micpath.2019.103850
Zaric RZ, Jankovic S, Zaric M, Milosavljevic M, Stojadinovic M, Pejcic A. Antimicrobial treatment of Morganella morganii invasive infections: systematic review. Indian J Med Microbiol. 2021;39(4):404-412. DOI: 10.1016/j.i jmmb.2021.06.005
Bandy A. Ringing bells: Morganella morganii fights for recognition. Public Health. 2020; 182:45-50. DOI: 10.1016/j.puhe. 2020.01.016
Khusro A, Aarti C, Buendía-Rodriguez G, Arasu MV, Al-Dhabi NA, Barbabosa-Pliego A. Adverse effect of antibiotics administration on horse health: An overview. J Equine Vet Sci. 2021;97:103339. DOI: 10.1016/j.jevs.2020.103 339
World Health Organization (WHO) & WHO Advisory Group on Integrated Surveillance of Antimicrobial Resistance (AGISAR). Critically important antimicrobials for human medicine: Ranking of antimicrobial agents for risk management of antimicrobial resistance due to non-human use. 6th ed. Geneva, Switzerland: World Health Organization; 2019. 52 p.
Pimenta J, Pinto AR, Saavedra MJ, Cotovio M. Equine Gram-negative oral microbiota: an antimicrobial resistances watcher? Antibiotics. 2023;12 (4) :792. DOI: 10.3390/antibiotics12040792
Palmieri N, Hess C, Hess M, Alispahic M. Sequencing of five poultry strains elucidates phylogenetic relationships and divergence in virulence genes in Morganella morganii. BMC Genom. 2020;21:1-13. DOI: 10.1186/s12864 -020-07001-2
Tamma PD, Aitken SL, Bonomo RA, Mathers AJ, van Duin D, Clancy CJ. Infectious Diseases Society of America guidance on the treatment of AmpC β-lactamase-producing Enterobacterales, carbapenem-resistant Acinetobacter baumannii, and Stenotrophomonas maltophilia infections. Clin Infect Dis. 2022;74(12):2089-2114. DOI: 10.1093/cid/ciab1013
Winther L, Andersen RM, Baptiste KE, Aalbæk B, Guardabassi L. Association of Stenotrophomonas maltophilia infection with lower airway disease in the horse: a retrospective case series. Vet J. 2010;186(3):358-363. DOI: 10.1016/j.tvjl.2009.08.026
Blanco P, Corona F, Martínez JL. Involvement of the RND efflux pump transporter SmeH in the acquisition of resistance to ceftazidime in Stenotrophomonas maltophilia. Nature. 2019;9 (1):4917. DOI: 10.1038/s41598-019-4130 8-9
Chang YT, Lin CY, Chen YH, Hsueh PR. Update on infections caused by Stenotrophomonas maltophilia with particular attention to resistance mechanisms and therapeutic options. Front Microbiol. 2015;6:893. DOI: 10.3389/fmicb.2015.00893