Pastern dermatitis outbreak associated with toxigenic and non-toxigenic Corynebacterium diphtheriae and non-toxigenic Corynebacterium ulcerans at a horse stable in Finland, 2021.
diphtheria
diphtheria toxin
epidemiology
horses
zoonosis
Journal
Zoonoses and public health
ISSN: 1863-2378
Titre abrégé: Zoonoses Public Health
Pays: Germany
ID NLM: 101300786
Informations de publication
Date de publication:
05 Nov 2023
05 Nov 2023
Historique:
revised:
13
10
2023
received:
19
06
2023
accepted:
21
10
2023
medline:
6
11
2023
pubmed:
6
11
2023
entrez:
5
11
2023
Statut:
aheadofprint
Résumé
Corynebacterium diphtheriae and Corynebacterium ulcerans, when producing toxin, are the cause of diphtheria, a potentially life-threatening illness in humans. Horses (Equus ferus caballus) are known to be susceptible to infection that may manifest clinically on rare occasions. In late 2021 and early 2022, specimens from five horses suffering from pastern dermatitis were cultured at the Laboratory of Clinical Microbiology at the Faculty of Veterinary Medicine, University of Helsinki, Finland. C. diphtheriae and/or C. ulcerans were recovered from all of these. This study aimed to (1) analyse the bacterial isolates and (2) describe the outbreak and identify possible sources of the infection and infection routes in the stable. Susceptibility testing, PCR for the tox gene, and Elek test for toxin production in PCR-positive isolates were performed. Whole genome sequencing was also conducted to achieve high-resolution strain typing. An epidemiological survey was done by means of a semi-structured interview of horses' caretaker, and contact tracing was done among people at the stable. Two tox gene-positive, toxin-producing C. diphtheriae belonged to sequence type (ST) 822. Other C. diphtheriae (n = 2, ST828) and C. ulcerans (n = 2, ST325 and ST838) isolates did not carry the tox gene. The epidemiological investigation explored numerous possible routes of transmission, but the definite source of infection was not identified. All established human contacts tested negative for diphtheriae. All horses recovered after antimicrobial treatment. Our study shows that C. diphtheriae and C. ulcerans may readily spread among horses at the same stable and complicate pastern dermatitis infections. These potentially zoonotic bacteria can cause outbreaks even in a country with a very low prevalence. Caretakers should be encouraged to wear gloves and practice good hand hygiene when treating infected skin lesions in horses.
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Informations de copyright
© 2023 The Authors. Zoonoses and Public Health published by Wiley-VCH GmbH.
Références
Abbott, Y., Efstratiou, A., Brennan, G., Hallanan, S., Leggett, B., Leonard, F. C., Markey, B. K., Tuite, C., & Fry, N. K. (2020). Toxigenic Corynebacterium ulcerans associated with upper respiratory infections in cats and dogs. The Journal of Small Animal Practice, 61, 554-560.
Airas, N., Hautaniemi, M., Syrjä, P., Knuuttila, A., Putkuri, N., Coulter, L., McInnes, C. J., Vapalahti, O., Huovilainen, A., & Kinnunen, P. M. (2016). Infection with possible novel Parapoxvirus in horse, Finland, 2013. Emerging Infectious Diseases, 22, 1242-1245.
Antunes, L. C. S., Visca, P., & Towner, K. J. (2014). Acinetobacter baumannii: Evolution of a global pathogen. Pathogens and Disease, 71, 292-301.
Baraúna, R. A., Ramos, R. T. J., Veras, A. A. O., de Sá, P. H. C. G., Guimarães, L. C., das Graças, D. A., Carneiro, A. R., Edman, J. M., Spier, S. J., Azevedo, V., & Silva, A. (2017). Genomic analysis of four strains of Corynebacterium pseudotuberculosis bv. Equi isolated from horses showing distinct signs of infection. Standards in Genomic Sciences, 12, 16.
Berbers, G., van Gageldonk, P., Kassteele, J. V., Wiedermann, U., Desombere, I., Dalby, T., Toubiana, J., Tsiodras, S., Ferencz, I. P., Mullan, K., Griskevicius, A., Kolupajeva, T., Vestrheim, D. F., Palminha, P., Popovici, O., Wehlin, L., Kastrin, T., Maďarová, L., Campbell, H., … S. S. Team. (2021). Circulation of pertussis and poor protection against diphtheria among middle-aged adults in 18 European countries. Nature Communications, 12, 2871.
Berger, A., Boschert, V., Konrad, R., Schmidt-Wieland, T., Hörmansdorfer, S., Eddicks, M., & Sing, A. (2013). Two cases of cutaneous diphtheria associated with occupational pig contact in Germany. Zoonoses and Public Health, 60, 539-542.
Bonmarin, I., Guiso, N., Le Flèche-Matéos, A., Patey, O., Patrick, A. D., & Levy-Bruhl, D. (2009). Diphtheria: A zoonotic disease in France? Vaccine, 27, 4196-4200.
Carfora, V., Scarampella, F., Iurescia, M., Donati, V., Stravino, F., Lorenzetti, S., Menichini, E., Franco, A., Caprioli, A., & Battisti, A. (2018). Non-toxigenic Corynebacterium ulcerans sequence types 325 and 339 isolated from two dogs with ulcerative lesions in Italy. Journal of Veterinary Diagnostic Investigation, 30, 447-450.
Clausen, P. T. L. C., Aarestrup, F. M., & Lund, O. (2018). Rapid and precise alignment of raw reads against redundant databases with KMA. BMC Bioinformatics, 19, 307.
CLSI. (2018). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. Clinical and Laboratory Standards Institute.
CLSI. (2020). Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals: Second informational supplement VET01S2. Clinical and Laboratory Standards Institute.
Cobbett, L. (1900). Diphtheria in the horse. Lancet, 156, 1-574.
Colman, G., Weaver, E., & Efstratiou, A. (1992). Screening tests for pathogenic corynebacteria. Journal of Clinical Pathology, 45, 46-48.
Corboz, L., Thoma, R., Braun, U., & Zbinden, R. (1996). Isolation of Corynebacterium diphtheriae subsp. belfanti from a cow with chronic active dermatitis. Schweizer Archiv für Tierheilkunde, 138, 596-599.
Dangel, A., Berger, A., Konrad, R., Bischoff, H., & Sing, A. (2018). Geographically diverse clusters of nontoxigenic Corynebacterium diphtheriae infection, Germany, 2016-2017. Emerging Infectious Diseases, 24, 1239-1245.
Eisenberg, T., Kutzer, P., Peters, M., Sing, A., Contzen, M., & Rau, J. (2014). Nontoxigenic tox-bearing Corynebacterium ulcerans infection among game animals, Germany. Emerging Infectious Diseases, 20, 448-452.
Eisenberg, T., Mauder, N., Contzen, M., Rau, J., Ewers, C., Schlez, K., Althoff, G., Schauerte, N., Geiger, C., Margos, G., Konrad, R., & Sing, A. (2015). Outbreak with clonally related isolates of Corynebacterium ulcerans in a group of water rats. BMC Microbiology, 15, 42.
Elsinga, J., van Meijeren, D., & Reubsaet, F. (2023). Surveillance of diphtheria in The Netherlands between 2000-2021: Cutaneous diphtheria supersedes the respiratory form. BMC Infectious Diseases, 23, 420.
Engler, K. H., Glushkevich, T., Mazurova, I. K., George, R. C., & Efstratiou, A. (1997). A modified Elek test for detection of toxigenic corynebacteria in the diagnostic laboratory. Journal of Clinical Microbiology, 35, 495-498.
Erol, E., Locke, S. J., Donahoe, J. K., Mackin, M. A., & Carter, C. N. (2012). Beta-hemolytic Streptococcus spp. from horses: A retrospective study (2000-2010). Journal of Veterinary Diagnostic Investigation, 24, 142-147.
Freeman, K., Woods, E., Welsby, S., Percival, S. L., & Cochrane, C. A. (2009). Biofilm evidence and the microbial diversity of horse wounds. Canadian Journal of Microbiology, 55, 197-202.
Fuursted, K., Søes, L. M., Crewe, B. T., Stegger, M., Andersen, P. S., & Christensen, J. J. (2015). Non-toxigenic tox gene-bearing Corynebacterium ulcerans in a traumatic ulcer from a human case and his asymptomatic dog. Microbes and Infection, 17, 717-719.
Gerber, V., Kaiser-Thom, S., & Oesch, S. (2023). Equine pastern dermatitis: A narrative review on clinical presentation, diagnosis, risk factors, prevention, and therapeutic approaches. Journal of the American Veterinary Medical Association, 261, S58-S65.
Hasman, H., Saputra, D., Sicheritz-Ponten, T., Lund, O., Svendsen, C. A., Frimodt-Møller, N., & Aarestrup, F. M. (2014). Rapid whole-genome sequencing for detection and characterization of microorganisms directly from clinical samples. Journal of Clinical Microbiology, 52, 139-146.
Henricson, B., Segarra, M., Garvin, J., Burns, J., Jenkins, S., Kim, C., Popovic, T., Golaz, A., & Akey, B. (2000). Toxigenic Corynebacterium diphtheriae associated with an equine wound infection. Journal of Veterinary Diagnostic Investigation, 12, 253-257.
Jünemann, S., Sedlazeck, F. J., Prior, K., Albersmeier, A., John, U., Kalinowski, J., Mellmann, A., Goesmann, A., von Haeseler, A., Stoye, J., & Harmsen, D. (2013). Updating benchtop sequencing performance comparison. Nature Biotechnology, 31, 294-296.
Katsukawa, C., Komiya, T., Yamagishi, H., Ishii, A., Nishino, S., Nagahama, S., Iwaki, M., Yamamoto, A., & Takahashi, M. (2012). Prevalence of Corynebacterium ulcerans in dogs in Osaka, Japan. Journal of Medical Microbiology, 61, 266-273.
Katsukawa, C., Umeda, K., Inamori, I., Kosono, Y., Tanigawa, T., Komiya, T., Iwaki, M., Yamamoto, A., & Nakatsu, S. (2016). Toxigenic Corynebacterium ulcerans isolated from a wild bird (ural owl) and its feed (shrew-moles): Comparison of molecular types with human isolates. BMC Research Notes, 9, 181.
König, C., Meinel, D. M., Margos, G., Konrad, R., & Sing, A. (2014). Multilocus sequence typing of Corynebacterium ulcerans provides evidence for zoonotic transmission and for the increased prevalence of certain sequence types among toxigenic strains. Journal of Clinical Microbiology, 52, 4318-4324.
Larsen, M. V., Cosentino, S., Lukjancenko, O., Saputra, D., Rasmussen, S., Hasman, H., Sicheritz-Pontén, T., Aarestrup, F. M., Ussery, D. W., & Lund, O. (2014). Benchmarking of methods for genomic taxonomy. Journal of Clinical Microbiology, 52, 1529-1539.
Larsen, M. V., Cosentino, S., Rasmussen, S., Friis, C., Hasman, H., Marvig, R. L., Jelsbak, L., Sicheritz-Pontén, T., Ussery, D. W., Aarestrup, F. M., & Lund, O. (2012). Multilocus sequence typing of total-genome-sequenced bacteria. Journal of Clinical Microbiology, 50, 1355-1361.
Layman, Q. D., Rezabek, G. B., Ramachandran, A., Love, B. C., & Confer, A. W. (2014). A retrospective study of equine actinobacillosis cases: 1999-2011. Journal of Veterinary Diagnostic Investigation, 26, 365-375.
Leggett, B. A., De Zoysa, A., Abbott, Y. E., Leonard, N., Markey, B., & Efstratiou, A. (2010). Toxigenic Corynebacterium diphtheriae isolated from a wound in a horse. The Veterinary Record, 166, 656-657.
Mathewson, A. A., Morse, D., Dreisig, J., Crawford, S., Bassette, N., Campbell, C., Gibson, R., Gao, G., Cassidy, P., Tiwari, T. S. P., Chan, B. P., & Talbot, E. (2018). Toxigenic Corynebacterium diphtheriae in a horse with respiratory illness, New Hampshire, 2017. In Council of State and territorial epidemiologists annual conference. West Palm Beach, Florida, USA.
Minett, F. C. (1920). Diphtheria bacilli in the horse. Journal of Comparative Pathology and Therapeutics, 33, 267-293.
Mothershed, E. A., Cassiday, P. K., Pierson, K., Mayer, L. W., & Popovic, T. (2002). Development of a real-time fluorescence PCR assay for rapid detection of the diphtheria toxin gene. Journal of Clinical Microbiology, 40, 4713-4719.
Muscat, M., Gebrie, B., Efstratiou, A., Datta, S. S., & Daniels, D. (2022). Diphtheria in the WHO European region, 2010 to 2019. Euro Surveillance, 27(8), 2100058. https://doi.org/10.2807/1560-7917.ES.2022.27.8.2100058
Museux, K., Arcari, G., Rodrigo, G., Hennart, M., Badell, E., Toubiana, J., & Brisse, S. (2023). Corynebacteria of the diphtheriae species complex in companion animals: Clinical and microbiological characterization of 64 cases from France. Microbiology Spectrum, 11, e0000623.
Oliveira, M., Barroco, C., Mottola, C., Santos, R., Lemsaddek, A., Tavares, L., & Semedo-Lemsaddek, T. (2014). First report of Corynebacterium pseudotuberculosis from caseous lymphadenitis lesions in Black Alentejano pig (Sus scrofa domesticus). BMC Veterinary Research, 10, 218.
Rückert, C., Kriete, M., Jaenicke, S., Winkler, A., & Tauch, A. (2015). Virulence factor genes detected in the complete genome sequence of Corynebacterium uterequi DSM 45634, Isolated from the Uterus of a Maiden Mare. Genome Announcements, 30, e00783-15.
Saeki, J., Katsukawa, C., Matsubayashi, M., Nakanishi, H., Furuya, M., Tani, H., & Sasai, K. (2015). The detection of toxigenic Corynebacterium ulcerans from cats with nasal inflammation in Japan. Epidemiology and Infection, 143, 2660-2665.
Sangal, V., & Hoskisson, P. A. (2016). Evolution, epidemiology and diversity of Corynebacterium diphtheriae: New perspectives on an old foe. Infection, Genetics and Evolution, 43, 364-370.
Schlez, K., Eisenberg, T., Rau, J., Dubielzig, S., Kornmayer, M., Wolf, G., Berger, A., Dangel, A., Hoffmann, C., Ewers, C., & Sing, A. (2021). Corynebacterium rouxii, a recently described member of the C. diphtheriae group isolated from three dogs with ulcerative skin lesions. Antonie Van Leeuwenhoek, 114, 1361-1371.
Schuhegger, R., Schoerner, C., Dlugaiczyk, J., Lichtenfeld, I., Trouillier, A., Zeller-Peronnet, V., Busch, U., Berger, A., Kugler, R., Hörmansdorfer, S., & Sing, A. (2009). Pigs as source for toxigenic Corynebacterium ulcerans. Emerging Infectious Diseases, 15, 1314-1315.
Sharma, N. C., Efstratiou, A., Mokrousov, I., Mutreja, A., Das, B., & Ramamurthy, T. (2019). Diphtheria. Nature Reviews Disease Primers, 5, 81.
Sing, A., Konrad, R., Meinel, D. M., Mauder, N., Schwabe, I., & Sting, R. (2016). Corynebacterium diphtheriae in a free-roaming red fox: Case report and historical review on diphtheria in animals. Infection, 44, 441-445.
THL. (2021). Diphtheria (in Finnish). Finnish Institute of Health and Welfare.
Virtanen, J., Hautala, K., Utriainen, M., Dutra, L., Eskola, K., Airas, N., Uusitalo, R., Ahvenainen, E., Smura, T., Sironen, T., Vapalahti, O., Kant, R., Virtala, A.-M. K., & Kinnunen, P. M. (2023). Equine dermatitis outbreak associated with parapoxvirus. bioRxiv. https://doi.org/10.1101/2023.09.01.555671
Virtanen, J., Hautaniemi, M., Dutra, L., Plyusnin, I., Hautala, K., Smura, T., Vapalahti, O., Sironen, T., Kant, R., & Kinnunen, P. M. (2023). Partial genome characterization of novel parapoxvirus in horse, Finland. Emerging Infectious Diseases, 29, 1941-1944.
Vu, M. L. D., & Rajnik, M. (2022). Arcanobacterium Haemolyticum. In StatPearls. StatPearls Publishing LLC.
Wagner, K. S., White, J. M., Crowcroft, N. S., De Martin, S., Mann, G., & Efstratiou, A. (2010). Diphtheria in the United Kingdom, 1986-2008: The increasing role of Corynebacterium ulcerans. Epidemiology and Infection, 138, 1519-1530.
Westgate, S. J., Percival, S. L., Knottenbelt, D. C., Clegg, P. D., & Cochrane, C. A. (2011). Microbiology of equine wounds and evidence of bacterial biofilms. Veterinary Microbiology, 150, 152-159.
Zasada, A. A., & Rzeczkowska, M. (2019). Nontoxigenic Corynebacterium diphtheriae infections, Europe. Emerging Infectious Diseases, 25, 1437-1438.
Zendri, F., Isgren, C. M., Sinovich, M., Richards-Rios, P., Hopkins, K. L., Russell, K., Groves, N., Litt, D., Fry, N. K., & Timofte, D. (2021). Case report: Toxigenic Corynebacterium ulcerans diphtheria-like infection in a horse in the United Kingdom. Frontiers in Veterinary Science, 8, 650238.
Zerbino, D. R., & Birney, E. (2008). Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Research, 18, 821-829.