Clinical, pathological and microbiological profiles of spontaneous enteropathies in growing rabbits

P. Badagliacca, A. Letizia, L. Candeloro, A. Di Provvido, A. Di Gennaro, S. Scattolini, G. Pompei, R. Pedicone, M. Scacchia


In a rabbit production facility, health monitoring for enteropathies was performed in 15 production cycles for 20 mo. For each cycle, up to a hundred 35 d old rabbits weaned the same day were randomly selected, reared in the same fattening unit, but separately from the source batch and fed with the same feed except for antimicrobial supplementation. Clinical symptoms and enteric lesions of the selected group were recorded, using two checklists with binomial response (yes/no answer to a list of 54 clinical and enteric variables). The day after weaning, one week later, at the beginning of the enteric symptoms and 4-5 d after the start of the symptoms, inocula from the small intestine and caecum of selected animals were subjected to microbiological, C. spiroforme, Eimeria oocyst and rotavirus antigen detection tests. Representative samples of E. coli and C. perfringens isolates were tested, respectively, for serotype, biotype, eae, afr/2 genes and for a, b1, b2, e, i and enterotoxin toxin genes. The answers to the clinical-pathological variables were subjected to statistical analysis with a cluster analysis programme in order to obtain homogeneous, statistically significant groups of diseased animals (clusters). Then, the clusters were statistically associated with the laboratory outcomes. The cluster to which the enterotyphlitis lesions significantly contributed was associated with E. coli detection, E. coli O103 serotype detection and C. spiroforme (“several elements” variable). C. spiroforme (“rare elements” variable) was significantly associated with a cluster, characterised by a pathological profile consisting of bloating/rumbling noise and liquid content in stomach and caecum, without enteric inflammation. C. perfringens was significantly associated with a cluster, characterised by a pathological profile consisting of dilation/liquid content of small intestine, caecal impaction and mucoid content in the colon. Eighteen out of twenty-fi ve C. perfringens strains, examined for their toxin genotypes, proved to be toxin type A, while 7 out of 25 strains showed the a and b2 toxin genes in combination. The rotavirus antigen and Eimeria oocysts were detected from healthy rabbits (specimens of the day after weaning and one week later) in about 15% of specimens examined, but their presence in the sick animals was not significantly associated with any cluster.



Clostridium; Cluster analysis; Enteropathy; Escherichia coli; Rabbit

Full Text:



Alberti S. 2006. L’Enteropatia Enzootica del Coniglio. Riv. Zoot. Vet. 34: 5-6.

Anderberg M.R. 1973. Cluster analysis for applications. Ed. Academic Press, New York, USA.

Agnoletti F., Favretti M., Deotto S., Passera A, Tisato E., Bano L., Mazzolini E. 2004. Report of enteropathogenic Escherichia coli (EPEC) isolated from enteric outbreaks in italian intensive rabbit herds. In Proc.: 8th World Rabbit Congress, 7-10 September, 2004. Puebla, Mexico. 416-421.

Agnoletti F., Bano L., Cocchi M., Mazzolini E. 2006. Aggiornamenti sulle enteriti batteriche del coniglio. Riv. Zoot. Vet. 34: 29-38.

Baums C.G., Scotte U., Amtsberg G., Goethe R. 2004. Diagnostic multiplex PCR for toxin genotyping of Clostridium perfringens isolates. Vet. Microbiol., 100: 11-16.

Blanco J.E., Blanco M., Blanco J., Mora A., Balaguer L., Mourino M., Juarez A., Jansen W.H. 1996. O serogroups, biotypes and eae genes in Escherichia coli strains isolated from diarrheic and healthy rabbits. J. Clin. Microbiol., 34: 3101-3107.

Boisot P., Licois D. and Gidenne T. 2003. Une restriction alimentaire réduit l’impact sanitaire d’une reproduction expérimentale de l’entérophatie épizootique (EEL) chez le lapin en croissance. In Proc.: 10èmes Journées de la Recherche Cunicole. 19-20 November 2003, Paris. 267-270.

Camguilhem R., Milon A., 1989. Biotypes and O serogroups of Escherichia coli involved in intestinal infections of weaned rabbits: clues to diagnosis of pathogenic strains. J. Clin. Microbiol. 27: 743747.

China B., Pirson V., Mainil J. 1996. Typing of bovine attaching and effacing Escherichia coli by multiplex in vitro amplification of virulence-associated genes. Appl. Environ. Microbiol., 62: 34623465.

Cocchi M., Agnoletti F., Bacchin C., Bano L., Guolo A., Drigo I. 2007. Tossinotipizzazione di Clostridium perfringens isolati dal coniglio. In proc: Atti delle Giornate ASIC di Coniglicoltura. 26-27 Settembre, Forlì, Italia. 2007; 67-69.

Council Directive 86/609/EEC of 24 November 1986 on the approximation of laws, regulations and administrative provisions of the Member States regarding the protection of animals used for experimental and other scientific purposes. European Official Journal L 358 , 18/12/1986; 1-28.

Dewrée R., Meulemans L., Lassence C., Desmecht D., Ducatelle R., Mast J., Licois D., Vindevogel H., Marlier D. 2007. Experimentally induced epizootic rabbit enteropathy: clinical, histopathological, ultrastructural, bacteriological and haematological findings. World Rabbit Sci., 15: 91-102.

Fortun-Lamonthe L., Bouillier S. 2007. A review on the interactions between gut microflora and digestive mucosal immunity. Possible ways to improve the health of rabbits. Livest. Sci., 107: 1-18.

Gallazzi D.,1998. Enterocolite, una malattia da conoscere. Rivista di Coniglicoltura. 3; 21-23.

Grilli G., Ferrazzi V., Agnoletti F., Piccirillo A., Pisoni A.M., Gallazzi D. 2006. La patologia enterica nel coniglio da carne allevato in Italia. Riv. Zoot. Vet., 34: 51-56.

Holmes H.T., Sonn R.J., Patton N.M., 1988. Isolation of Clostridium spiroforme from rabbits. Lab. Anim. Sci., 38: 167-168.

Huybens N., Houeix J., Licois D., Mainil J., Marlier D. 2009. Inoculation and bacterial analyses of fractions obtained from the reference inoculum TEC4 which experimentally reproduces epizootic rabbit enteropathy. World Rabbit Sci., 17: 185-193.

Le Normand B., Le Guenec J., Moalic P.Y. 2003. Contribution à l’étude toxinotypique de souches de Clostridium perfringens isolées dans l’entéropathie épizootique du lapin (EEL). 10èmes Journées de la Recherche cunicole, 19-20 novembre 2003. Paris.

Licois D. 2004. Domestic rabbit enteropathies. In Proc.: 8th World Rabbit Congress, 7-10 September, 2004. Puebla, Mexico. 385-403.

Licois D., Marlier D. 2008. Pathologies infectieuses du lapin en élevage rationnel. INRA Prod. Anim., 21: 257-268.

Licois D., Wyers M., Coudert P. 2005. Epizootic rabbit enteropathy: experimental transmission and clinical characterization. Vet. Res., 36: 601-613.

Marlier D., Dewrée R., Lassence C., Licois D., Mainil J., Coudert P., Meulemans L., Ducatelle R., Vindevogel H. 2006. Infectious agents associated with epizootic rabbit enteropathy: isolation and attempts to reproduce the syndrome. Vet. J., 172: 493-500.

Milon A., Oswald E. De Rycke J. 1999. Rabbit EPEC: a model for the study of enteropathogenic Escherichia coli. Vet. Res. 30: 203-219.

Nouaille L., 2006. Enterocolite del coniglio in Francia. Riv. Zoot. Vet., 34: 45-50.

Penteado A.S., Ugrinovich L.A., Blanco J., Blanco M., Blanco J.E., Mora A., Andrade J.R.C., Corrêa S.S., Pestana de Castro A.F. 2002. Serobiotypes and virulence genes of Escherichia coli isolated from diarrheic and healthy rabbits in Brazil. Vet. Microbiol., 89: 41-51.

Peeters J.E. 1987. Troubles digestifs chez le lapin de chair: causes et prévention. Revue de l’Agriculture, 40: 1240-1254.

Peréz de Rozas A.M., Carabaño R., Garcìa J., Rosell J., Diaz J.V., Barbé J., Pascual J.J., Badiola I., 2005. Etiopatogenia de la Enteropatia Epizootica del conejo. In Proc.: XXX Symposium de ASESCU. 1820 May, 2005. Valladolid, Spain. 167-174.

Rosell J.M. 2000. Enfermedades del conejo. Tomo II, Enfermedades. Ed. Mundi-Prensa, Madrid, España.

Rosell J.M. 2006. Enterocolite del coniglio in Spagna e in Portogallo. Riv. Zoot. Vet. 34: 39-44.

Rosell J.M., de la Fuente L.F., Badiola J.I., Fernández de Luco D., Casal J., Saco M. 2009. Study of urgent visits to commercial rabbit farms in Spain and Portugal during 1997-2007. World Rabbit Sci., 17: 127-136. SPSS. 2006. Statistical Package for Social Science for Windows, 15.0 version.

SPSS Inc., 1989-2006, Chicago, USA.

Szalo I.M., Lassence C., Licois D., Coudert P., Poulipoulis A., Vindevogel H., Marlier D. 2007. Fractionation of the reference inoculum of epizootic rabbit enteropathy in discontinuous sucrose gradient indentifies aetiological agents in high density fractions. Vet. J., 173: 652-657.

Yoo H. S., Lee S. U., Park K. Y., Park Y. H., 1997. Molecular typing and epidemiological survey of prevalence of Clostridium perfringens types by multiplex PCR. J. Clin. Microbiol., 35: 228-232.

Abstract Views

Metrics Loading ...

Metrics powered by PLOS ALM


Cited-By (articles included in Crossref)

This journal is a Crossref Cited-by Linking member. This list shows the references that citing the article automatically, if there are. For more information about the system please visit Crossref site

1. Molecular methods in detection and epidemiologic studies of rabbit and hare viruses: a review
Ewa Kwit, Artur Rzeżutka
Journal of Veterinary Diagnostic Investigation  vol: 31  issue: 4  first page: 497  year: 2019  
doi: 10.1177/1040638719852374


 Universitat Politècnica de València


Official journal of the World Rabbit Science Association (WRSA)


e-ISSN: 1989-8886     ISSN: 1257-5011