Characterization of Staphylococcus aureus ST3320 clone causing fatal respiratory infection in rabbits
DOI:
https://doi.org/10.4995/wrs.2021.14280Keywords:
Staphylococcus aureus, rabbit, fatal respiratory infection, virulence gene, multi-locus sequencing typingAbstract
Staphylococcus aureus is a well-known pathogen that infects humans and animals. However, information on the fatal respiratory infection in rabbits caused by S. aureus is still limited. In the present study, a S. aureus isolate designated ND01 was recovered from lung samples of rabbits that died of fatal respiratory infection, and the ND01 was characterised by intranasal infection of rabbits, multi-locus sequencing typing, screening virulence genes and testing antimicrobial susceptibility. Clinical signs of matted forepaws and pathological lesions of haemorrhagic tracheitis and necrotising haemorrhagic pneumonia were observed in the ND01 infected rabbits, which were identical to those of naturally infected ones. The sequence type of the ND01 was defined as ST3320 and the ND01 was further grouped into the clonal complex 398. Notably, the ND01 was pvl-positive S. aureus and carried the human-associated scn gene. Moreover, the ND01 was methicillin-susceptible S. aureus and was susceptible to 6 of 10 tested antibiotics. This study described the characteristics of the ND01 causing fatal respiratory infection in rabbits. The results are helpful to further the understanding of the pathogenicity of S. aureus ST3320 clone in rabbits. The results also highlighted that operators must be on the alert for the colonisation of pvl-positive S. aureus in rabbits and potential transmission events between rabbits and humans.Downloads
References
Agnoletti F., Mazzolini E., Bacchin C., Bano L., Berto G., Rigoli R., Muffato G., Goato P., Tonon E., Drigo I. 2014. First reporting of methicillin-resistant Staphylococcus aureus (MRSA) ST398 in an industrial rabbit holding and in farm-related people. Vet. Microbiol., 170: 172-177. https://doi.org/10.1016/j.vetmic.2014.01.035
Algammal A.M., Hetta H.F., Elkelish A., Alkhalifah D.H.H., Hozzein W.H., Batiha G.E., EI Nahhas N., Mabrok M.A. 2020. Methicillin-resistant Staphylococcus aureus (MRSA): One health perspective approach to the bacterium epidemiology, virulence factors, antibiotic-resistant, and zoonotic impact. Infect. Drug Resist., 13: 3255-3265. https://doi.org/10.2147/IDR.S272733
Brakstad O.G., Aasbakk K., Maeland J.A. 1992. Detection of Staphylococcus aureus by polymerase chain reaction amplification of the nuc gene. J. Clin. Microbiol., 30: 1654-1660. https://doi.org/10.1128/JCM.30.7.1654-1660.1992
Chroboczek T., Boisset S., Rasigade J., Tristan A., Bes M., Meugnier H., Vandenesch F., Etienne J., Laurent F. 2013. Clonal complex 398 methicillin susceptible Staphylococcus aureus: a frequent unspecialized human pathogen with specific phenotypic and genotypic characteristics. PLoS One, 8: e68462. https://doi.org/10.1371/journal.pone.0068462
CLSI (Clinical and Laboratory Standards Institute). 2018. Performance standards for antimicrobial susceptibility testing, 28th edition, CLSI supplement M100. Wayne, PA, USA.
Corpa J.M., Hermans K., Haesebrouck F. 2009. Main pathologies associated with Staphylococcus aureus infections in rabbits: a review. World Rabbit Sci., 17: 115-125. https://doi.org/10.4995/wrs.2009.651
Davies P.R., Wagstrom E.A., Bender J.B. 2011. Lethal necrotizing pneumonia caused by an ST398 Staphylococcus aureus strain. Emerg. Infect. Dis., 17: 1152-1153. https://doi.org/10.3201/eid1706.101394
Ferreira A., Monteiro J.M., Vieira-pinto M. 2014. The importance of subcutaneous abscess infection by Pasteurella spp. and Staphylococcus aureus as a cause of meat condemnation in slaughtered commercial rabbits. World Rabbit Sci., 22: 311-317. https://doi.org/10.4995/wrs.2014.2238
Gillet Y., Issartel B., Vanhems P., Fournet J., Lina G., Bes M., Vandenesch F., Piémont Y., Brousse N., Floret D., Etienne J. 2002. Association between Staphylococcus aureus strains carrying gene for Panton-Valentine leukocidin and highly lethal necrotising pneumonia in young immunocompetent patients. Lancet, 359: 753-759. https://doi.org/10.1016/S0140-6736(02)07877-7
Giulieri S.G., Tong S.Y.C., Williamson D.A. 2020. Using genomics to understand meticillin- and vancomycin-resistant Staphylococcus aureus infections. Microb. Genom., 6: e000324. https://doi.org/10.1099/mgen.0.000324
Huang J., Zhang T., Zou X., Wu S., Zhu J. 2020. Panton-Valentine leukocidin carrying Staphylococcus aureus causing necrotizing pneumonia inactivates the JAK/STAT signaling pathway and increases the expression of inflammatory cytokines. Infect. Genet. Evol., 86: 104582. https://doi.org/10.1016/j.meegid.2020.104582
Jarraud S., Mougel C., Thioulouse J., Lina G., Meugnier H., Forey F., Nesme X., Etienne J., Vandenesch F. 2002. Relationships between Staphylococcus aureus genetic background, virulence factors, agr groups (alleles), and human disease. Infect. Immun., 70: 631-641. https://doi.org/10.1128/IAI.70.2.631-641.2002
Jenul C., Horswill A.R. 2019. Regulation of Staphylococcus aureus virulence. Microbiol. Spectr., 7: GPP3-0031-2018. https://doi.org/10.1128/microbiolspec.GPP3-0031-2018
Liu Y., Li W., Dong Q., Liu Y., Ye X. 2021. Livestock-associated and non-livestock-associated Staphylococcus aureus carriage in humans is associated with pig exposure in a dose-response manner. Infect. Drug Resist., 14: 173-184. https://doi.org/10.2147/IDR.S290655
Lozano C., Gharsa H., Slama K.B., Zarazaga M., Torres C. 2016. Staphylococcus aureus in animals and food: methicillin resistance, prevalence and population structure. A review in the African continent. Microorganisms, 4: 12. https://doi.org/10.3390/microorganisms4010012
Mongodin E., Bajolet O., Cutrona J., Bonnet N., Dupuit F., Puchelle E., de Bentzmann S. 2002. Fibronectin-binding proteins of Staphylococcus aureus are involved in adherence to human airway epithelium. Infect. Immun., 70: 620-630. https://doi.org/10.1128/iai.70.2.620-630.2002
Moreno-Grúa E., Pérez-Fuentes S., Muñoz-Silvestre A., Viana D., Fernández-Ros A.B., Celia Sanz-Tejero C., Corpa J.M., Selva L. 2018. Characterization of livestockassociated methicillin-resistant Staphylococcus aureus isolates obtained from commercial rabbitries located in the Iberian Peninsula. Front. Microbiol., 9: 1812. https://doi.org/10.3389/fmicb.2018.01812
Murakami K., Minamide W., Wada K., Nakamura E., Teraoka H., Watanabe S. 1991. Identification of methicillinresistant strains of staphylococci by polymerase chain reaction. J. Clin. Microbiol., 29: 2240-2244. https://doi.org/10.1128/jcm.29.10.2240-2244.1991
Paterson G.K., Larsen A.R., Robb A., Edwards G.E., Pennycott T.W., Foster G., Mot D., Hermans K., Baert K., Peacock S.J., Parkhill J., Zadoks R.N., Holmes M.A. 2012. The newly described mecA homologue, mecALGA251, is present in methicillinresistant Staphylococcus aureus isolates from a diverse range of host species. J. Antimicrob. Chemother., 67: 2809-2813. https://doi.org/10.1093/jac/dks329
Rowe S.E., Wagner N.J., Li L., Beam J.E., Wilkinson A.D., Radlinski L.C., Zhang Q., Miao E.A., Conlon B.P. 2020. Reactive oxygen species induce antibiotic tolerance during systemic Staphylococcus aureus infection. Nat. Microbiol., 5: 282-290. https://doi.org/10.1038/s41564-019-0627-y
Selva L., Viana D., Corpa J.M. 2015. Staphylococcus aureus nasal carriage could be a risk for development of clinical infections in rabbits. World Rabbit Sci., 23: 181-184. https://doi.org/10.4995/wrs.2015.3960
Sicot N., Khanafer N., Meyssonnier V., Dumitrescu O., Tristan A., Bes M., Lina G., Vandenesch F., Vanhems P., Etienne J., Gillet Y. 2013. Methicillin resistance is not a predictor of severity in community acquired Staphylococcus aureus necrotizing pneumonia-results of a prospective observational study. Clin. Microbiol. Infect., 19: E142-148. https://doi.org/10.1111/1469-0691.12022
Silva V., de Sousa T., Gómez P., Sabença C., Vieira-Pinto M., Capita R., Alonso-Calleja C., Torres C., Capelo J.L., Igrejas G., Poeta P. 2020. Livestock-associated methicillinresistant Staphylococcus aureus (MRSA) in purulent subcutaneous lesions of farm rabbits. Foods, 9: 439. https://doi.org/10.3390/foods9040439
Speziale P., Pietrocola G. 2020. The multivalent role of fibronectin-binding proteins A and B (FnBPA and FnBPB) of Staphylococcus aureus in host infections. Front. Microbiol., 11: 2054. https://doi.org/10.3389/fmicb.2020.02054
Srinivasan V., Sawant A.A., Gillespie B.E., Headrick S.J., Ceasaris L., Oliver S.P. 2006. Prevalence of enterotoxin and toxic shock syndrome toxin genes in Staphylococcus aureus isolated from milk of cows with mastitis. Foodborne Pathog. Dis., 3: 274-283. https://doi.org/10.1089/fpd.2006.3.274
Stegger M., Liu C.M., Larsen J., Soldanova K., Aziz M., Contente-Cuomo T., Petersen A., Vandendriessche S., Jiménez J.N., Mammina C., van Belkum A., Salmenlinna S., Laurent F., Skov R.L., Larsen A.R., Andersen P.S., Price L.B. 2013. Rapid differentiation between livestock-associated and livestockindependent Staphylococcus aureus CC398 clades. PLoS One, 8: e79645. https://doi.org/10.1371/journal.pone.0079645
van Wamel W.J.B., Rooijakkers S.H.M., Ruyken M., van Kessel K.P.M., van Strijp J.A.G. 2006. The innate immune modulators staphylococcal complement inhibitor and chemotaxis inhibitory protein of Staphylococcus aureus are located on beta-hemolysin-converting bacteriophages. J. Bacteriol., 188: 1310-1315. https://doi.org/10.1128/JB.188.4.1310-1315.2006
Viana D., Selva L., Penadés M., Corpa J.M. 2015. Screening of virulence genes in Staphylococcus aureus isolates from rabbits. World Rabbit Sci., 23: 185-195. https://doi.org/10.4995/wrs.2015.3961
Wang J., Sang L., Sun S., Chen Y., Chen D., Xie X. 2019a. Characterisation of Staphylococcus aureus isolated from rabbits in Fujian, China. Epidemiology and Infection, e256: 1-5. https://doi.org/10.1017/S0950268819001468
Wang J., Sang L., Chen Y., Sun S., Chen D., Xie X. 2019b. Characterisation of Staphylococcus aureus strain causing severe respiratory disease in rabbits. World Rabbit Sci., 27: 41-48. https://doi.org/10.4995/wrs.2019.10454
Warsa U.C., Nonoyama M. Ida T., Okamoto R., Okubo T., Shimauchi C., Kuga A., Inoue M. 1996. Detection of tet(K) and tet(M) in Staphylococcus aureus of Asian countries by the polymerase chain reaction. J. Antibiot. (Tokyo), 49: 1127-1132. https://doi.org/10.7164/antibiotics.49.1127
Weisburg W.G., Barns S.M., Pelletier D.A., Lane D.J. 1991. 16S ribosomal DNA amplification for phylogenetic study. J. Bacteriol., 173: 697-703. https://doi.org/10.1128/jb.173.2.697-703.1991
Xie Y., He Y., Gehring A, Hu Y, Li Q., Tu SI., Shi X. 2011. Genotypes and toxin gene profiles of Staphylococcus aureus clinical isolates from China. PLoS One, 6: e28276. https://doi.org/10.1371/journal.pone.0028276
Downloads
Published
Issue
Section
License
This journal is licensed under a "Attribution-NonCommercial-ShareAlike 4.0 International (CC BY-NC-SA 4.0)".
