Carriage and acquisition rates of Clostridium difficile in hospitalized horses, including molecular characterization, multilocus sequence typing and antimicrobial susceptibility of bacterial isolates
[en] lostridium difficile has been identified as a significant agent of diarrhoea and enterocolitis in both foals and adult horses. Hospitalization, antibiotic therapy or changes in diet may contribute to the development of C. difficile infection. Horses admitted to a care unit are therefore at greater risk of being colonized. The aim of this study was to investigate the carriage of C. difficile in hospitalized horses and the possible influence of some risk factors in colonization. During a seven-month period, faecal samples and data relating the clinical history of horses admitted to a veterinary teaching hospital were collected. C. difficile isolates were characterized through toxin profiles, cytotoxicity activity, PCR-ribotyping, antimicrobial resistance and multilocus sequence typing (MLST). Ten isolates were obtained with a total of seven different PCR-ribotypes, including PCR-ribotype 014. Five of them were identified as toxinogenic. A high resistance to gentamicin, clindamycin and ceftiofur was found. MLST revealed four different sequencing types (ST), which included ST11, ST26, ST2 and ST15, and phylogenetic analysis showed that most of the isolates clustered in the same lineage. Clinical history suggests that horses frequently harbour toxigenic and non-toxigenic C. difficile and that in most cases they are colonized regardless of the reason for hospitalization; the development of diarrhoea is more unusual.
Disciplines :
Microbiology
Author, co-author :
Rodriguez Diaz, Cristina ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Technologie des denrées alimentaires
Taminiau, Bernard ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Brévers, Bastien; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Avesani, Véronique; Université Catholique de Louvain - UCL > Faculty of Medicine > Microbiology Unit
Van Broeck, Johan; Université Catholique de Louvain - UCL > Faculty of Medicine > Microbiology Unit
Leroux, Aurélia ; Université de Liège - ULiège > Dép. clinique des animaux de compagnie et des équidés (DCA) > Médecine interne des équidés
Amory, Hélène ; Université de Liège - ULiège > Dép. clinique des animaux de compagnie et des équidés (DCA) > Médecine interne des équidés
Delmée, Michel; Université Catholique de Louvain - UCL > Faculty of Medicine > Microbiology Unit
Daube, Georges ; Université de Liège - ULiège > Département de sciences des denrées alimentaires (DDA) > Microbiologie des denrées alimentaires
Language :
English
Title :
Carriage and acquisition rates of Clostridium difficile in hospitalized horses, including molecular characterization, multilocus sequence typing and antimicrobial susceptibility of bacterial isolates
Publication date :
06 August 2014
Journal title :
Veterinary Microbiology
ISSN :
0378-1135
eISSN :
1873-2542
Publisher :
Elsevier Science, Amsterdam, Netherlands
Volume :
172
Pages :
309-317
Peer reviewed :
Peer Reviewed verified by ORBi
Name of the research project :
Contract RF09/6226
Funders :
FPS Health Federal Public Service Health, Food Chain Safety and Environment
Arroyo, L.G., Henry, R., Stampfli, H.R., Weese, J.S., Potential role of Clostridium difficile as a cause of duodenitis-proximal jejunitis in horses (2006) J. Med. Microbiol., 55, pp. 605-608
Barbut, F., Petit, J.C., Epidemiology of Clostridium difficile-associated infections (2001) Clin. Microbiol. Infect., 7, pp. 405-410
Barbut, F., Mastrantonio, P., Delmée, M., Brazier, J., Kuijper, E., Poxton, I., Prospective study of Clostridium difficile infections in Europe with phenotypic and genotypic characterisation of the isolates (2007) Clin. Microbiol. Infect., 13, pp. 1048-1057. , European Study Group of Clostridium difficile (ESGCD)
Barr, B.S., Waldrige, B.M., Morresey, P.R., Reed, S.M., Clark, C., Belgrave, R., Donecker, J.M., Weigel, D.J., Antimicrobial-associated diarrhoea in three equine referral practices (2013) Equine Vet. J., 45, pp. 154-158
Baverud, V., Clostridium difficile diarrhea: infection control in horses (2004) Vet. Clin. Equine, 20, pp. 615-630
Baverud, V., Gustafsson, A., Franklin, A., Aspan, A., Gunnarsson, A., Clostridium difficile: prevalence in horses and environment and antimicrobial susceptibility (2003) Equine Vet. J., 35, pp. 465-471
Bengualid, V., Umesh, K.C., Alapati, J., Berger, J., Clostridium difficile at a community hospital in the Bronx, New York: incidence, prevalence and risk factors from 2006 to 2008 (2011) Am. J. Infect. Control, 39, pp. 183-187
Bidet, P., Barbut, F., Lalande, V., Burghoffer, B., Petit, J.C., Development of a new PCR-ribotyping method based on ribosomal RNA gene sequencing (1999) FEMS Microbiol. Lett., 175, pp. 261-266
Cattoir, V., Ould-Hocine, Z.F., Legrand, P., Antimicrobial susceptibility of Clostridium difficile clinical isolates collected from 2001 to 2007 in a French university hospital (2008) Pathol. Biol., 56, pp. 7-8
Clabots, C.R., Johnson, S., Olson, M.M., Peterson, L.R., Gerding, D.N., Acquisition of Clostridium difficile by hospitalized patients: evidence for colonized new admissions as a source of infection (1992) J. Infect. Dis., 166, pp. 561-567
(2010) 20th Informational Supplement, 30 (1). , Clinical and Laboratory Standards Institute, Wayne, PA. USA, M100-S20, CLSI
Delmée, M., Vandercam, B., Avesani, V., Michaux, J.L., Epidemiology and prevention of Clostridium difficile in a leukaemia unit (1987) Eur. J. Clin. Microbiol., 6, pp. 623-627
Delmée, M., Avesani, V., Correlation between serogroup and susceptibility to chloramphenicol clindamycin, erythromycin, rifampicin and tetracycline among 308 isolates of Clostridium difficile (1988) J. Antimicrob. Chemother., 22, pp. 325-331
Deshpande, A., Pasupuleti, V., Thota, P., Pant, C., Rolston, D.D., Sferra, T.J., Hernandez, A.V., Donskey, C.J., Community-associated Clostridium difficile infection and antibiotics: a meta-analysis (2013) J. Antimicrob. Chemother., 68, pp. 1951-1961
Diab, S.S., Songer, G., Uzal, F.A., Clostridium difficile infection in horses: a review (2013) Vet. Microbiol., 167, pp. 42-49
Dingle, K.E., Griffiths, D., Didelot, X., Evans, J., Vaughan, A., Kachrimaidau, M., Stoesser, N., Crook, D.W., Clinical Clostridium difficile: clonality and pathogenicity locus diversity (2011) Plos One, 6, pp. e19993
Donaldson, M.M., Palmer, J.E., Prevalence of Clostridium perfringens enterotoxin and Clostridium difficile toxin A in feces of horses with diarrhea and colic (1999) J. Am. Vet. Med. Assoc., 215, pp. 358-361
Drummond, A.J., Ahston, B., Buxton, S., Cheung, M., Heled, J., Kearse, M., Moir, R., Wilson, A., (2013) Geneious v4.8, , http://www.geneious.com, Available from
Erikstrup, L.T., Danielsen, T.K.L., Hall, V., Olsen, K.E.P., Kristensen, B., Kahlmeter, G., Fuursted, K., Justesen, U.S., Antimicrobial susceptibility testing of Clostridium difficile using EUCAST epidemiological cut-off values and disk diffusion correlates (2012) Clin. Microbiol. Infect., 18, pp. 266-272
http://www.eucast.org/clinical_breakpoints, European Committee on Antimicrobial Susceptibility testing clinical break-points (EUCAST)
Griffiths, D., Fawley, W., Kachrimanidou, M., Bowden, R., Crook, D.W., Fung, R., Golubchik, T., Dingle, K.E., Multilocus sequence typing of Clostridium difficile (2010) J. Clin. Microbiol., 48, pp. 370-378
Keel, M.K., Songer, J.G., The comparative pathology of Clostridium difficile-associated disease (2006) Vet. Pathol., 43, pp. 225-240
Knetsch, C.W., Terveer, E.M., Lauber, C., Gorbalenya, A.E., Harmanus, C., Kuijper Ed, J., Corver, J., van Leeuwen, H.C., Comparative analysis of an expanded Clostridium difficile reference strain collection (2012) Infect. Genet. Evol., 12, pp. 1577-1585
Magdesian, K.G., Leutenegger, C.M., Real-time PCR and typing of Clostridium difficile isolates colonizing mare-foal pairs (2011) Vet. J., 190, pp. 119-123
Marie, J., Morvan, H., Berthelot-Hérault, F., Sanders, P., Kempf, I., Gautier-Bouchardon, A.V., Jouy, E., Kobisch, M., Antimicrobial susceptibility of Streptococcus suis isolated from swine in France and from humans in different countries between 1996 and 2000 (2000) J. Antimicrob. Chemother., 50, pp. 201-209
Medina-Torres, C.E., Weese, J.S., Staempfli, H.R., Prevalence of Clostridium difficile in horses (2011) Vet. Microbiol., 152, pp. 212-215
Niwa, H., Kato, H., Hobo, S., Kinoshita, Y., Ueno, T., Katayama, Y., Hariu, K., Nakai, K., Postoperative Clostridium difficile infection with PCR ribotype 078 strain identified at necropsy in five thoroughbred racehorses (2013) Vet. Rec., 173, p. 607
Lemée, L., Dhalluin, A., Pestel-Caron, M., Lemeland, J.F., Pons, J.L., Multilocus sequence typing of humans and animal Clostridium difficile isolates of various toxigenic types (2004) J. Clin. Microbiol., 42, pp. 2609-2617
Lemée, L., Pons, J.L., Multilocus sequence typing for Clostridium difficile (2010) Methods Mol. Biol., 646, pp. 77-90
Ozaqui, E., Kato, H., Kita, H., Karasawa, T., Maegawa, T., Koino, Y., Matsumoto, K., Nakamura, S., Clostridium difficile colonization in healthy adults: transient colonization and correlation with enterococcal colonization (2004) J. Med. Microbiol., 53, pp. 167-172
Pituch, H., Obuch-Woszczatyriski, P., Wultanska, D., Meisel-Mikolajczyk, F., Luczak, M., A survey of metronidazole and vancomycin resistance in strains of Clostridium difficile isolated in Warsaw, Poland (2005) Anaerobe, 11, pp. 197-199
Pelaez, T., Alcala, L., Blanco, J.L., Alvarez-Perez, S., Marin, M., Martin-Lopez, A., Catalan, P., Bouza, E., Characterization of swine isolates of Clostridium difficile in Spain: a potential source of epidemic multidrug resistant strains? (2013) Anaerobe, 22, pp. 45-49
Pirs, T., Avbersek, J., Zdovc, I., Krt, B., Andlovic, A., Lejko-Zupanc, T., Rupnik, M., Ocepek, M., Antimicrobial susceptibility of animal and human isolates of Clostridium difficile by broth microdilution (2013) J. Med. Microbiol., 62, pp. 1478-1485
Rodriguez, C., Taminiau, B., Van Broeck, J., Avesani, V., Delmée, M., Daube, G., Clostridium difficile in young farm animals and slaughter animals in Belgium (2012) Anaerobe, 18, pp. 621-625
Rodriguez, C., Avesani, V., Van Broeck, J., Taminiau, B., Delmée, M., Daube, G., Presence of Clostridium difficile pigs and cattle intestinal contents and carcass contamination at slaughterhouse in Belgium (2013) Int. J. Food Microbiol., 166, pp. 256-262
Rodriguez-Palacios, A., Pickworth, C., Loerch, S., Lejeune, J.T., Transient fecal sheeding and limited animal-to-animal transmission of Clostridium difficile by naturally infected finishing feedlot cattle (2011) Appl. Environ. Microbiol., 77, pp. 3391-3397
Rodriguez-Palacios, A., Borgmann, S., Kline, T.R., Lejeune, J.T., Clostridium difficile in foods and animals: history and measures to reduce exposure (2013) Anim. Health Res. Rev., 14, pp. 11-29
Schoster, A., Staempfli, H.R., Arroyo, L.G., Reid-Smith, R.J., Janecko, N., Shewen, P.E., Weese, J.S., Longitudinal study of Clostridium difficile and antimicrobial susceptibility of Escherichia coli in healthy horses in a community setting (2012) Vet. Microbiol., 159, pp. 364-370
Schoster, A., Arroyo, L.G., Staempfli, H.R., Shewen, P.E., Weese, J.S., Presence and molecular characterization of Clostridium difficile and Clostridium perfringens in intestinal compartments of healthy horses (2012) BMC Vet. Res., 8, p. 94
Slimings, C., Riley, T.V., Antibiotics and hospital aquired Clostridium difficile infection: update of systematic review and meta-analysis (2014) J. Antimicrob. Chemother., 69, pp. 881-891
Stabler, R.A., Dawson, L.F., Valiente, E., Cairns, M.D., Martin, M.J., Donahue, E.H., Riley, T.V., Wren, B.W., Macro and micro diversity of Clostridium difficile isolates from diverse sources and geographical locations (2012) PLoS One, 7, pp. e31559
Thean, S., Elliott, B., Riley, T.V., Clostridium difficile in horses in Australia-a preliminary study (2011) J. Med. Microbiol., 60, pp. 1188-1192
Uzal, F.A., Diab, S.S., Blanchard, P., Moore, J., Anthenill, L., Shahriar, F., Garcia, J.P., Songer, J.G., Clostridium perfringens type C and Clostridium difficile co-infection in foals (2012) Vet. Microbiol., 156, pp. 395-402
Weber, I., Riera, E., Déniz, C., Pérez, J.L., Oliver, A., Mena, A., Molecular epidemiology and resistance profiles of Clostridium difficile in a tertiary care hospital in Spain (2013) Int. J. Med. Microbiol., 303, pp. 128-133
Weese, J.S., Toxopeux, L., Arroyo, L., Clostridium difficile associated diarrhoea in horses within the community: predictors clinical presentation and outcome (2006) Equine Vet. J., 38, pp. 185-188
Zidaric, V., Pardon, B., Dos Vultos, T., Deprez, P., Brouwer, M.S.M., Roberts, A.P., Henriques, A.O., Rupnik, M., Different antibiotic resistance and sporulation properties within multiclonal Clostridium difficile PCR Ribotypes 078 126 and 033 in a single calf farm (2012) Appl. Environ. Microbiol., 78, pp. 8515-8522
