Animal botulism in Poland – laboratory and epidemiological investigations

Tomasz Grenda; Magdalena Goldsztejn; Krzysztof Kwiatek; Beata Kozak; Anna Grenda

doi:10.2478/jvetres-2022-0026

Abstract

Introduction

The aim of the study was to present cases of botulism in animals found in Poland in 2019–2021. The analytical laboratory diagnosis and difficulties that occurred in the interpretation of the results are described.

Material and Methods

From 2019 to 2021, samples of serum, intestinal content, liver, spleen, kidney, faeces, wet feed, dry feed, ensilage, water and mixed samples of internal organs associated with 10 suspected animal botulism cases were sent to the National Veterinary Research Institute. Samples were analysed using a mouse bioassay and culture methods in combination with ntnh and bont gene detection.

Results

Among the ten putative botulism cases, only four (40%) were confirmed in the laboratory on the basis of the detection of botulinum toxin (BoNT) or the ntnh or bont genes. The remaining six (60%) were determined as probable despite observable characteristic clinical signs.

Conclusion

The diagnosis of botulism in animals is a very difficult task, made so by the heterogeneity of Clostridium botulinum strains and possible loss of toxinogenicity during laboratory processing or the potential degradation of toxins. Laboratory diagnosis is a complex and problematic process which should utilise different prescribed methods for specific types of sample.

References

Anniballi F., Fiore A., Löfström C., Skarin H., Auricchio B., Woudstra C., Bano L., Segerman B., Koene M., Båverud V., Hansen T., Fach P., Tevell Aberg A., Hedeland M., Olsson Engvall E., De Medici D.: Management of animal botulism outbreaks: from clinical suspicion to practical countermeasures to prevent or minimize outbreaks. Biosecur Bioterror 2013, 11, 191–199, doi: 10.1089/bsp.2012.0089.
Open DOI Search in Google Scholar Back to article
Brunt J., Van Vliet, A.H.M., Carter A.T., Stringer S.C., Amar C., Grant K.A., Godbole G., Peck M.W.: Diversity of the genomes and neurotoxins of strains of Clostridium botulinum group I and Clostridium sporogenes associated with foodborne, infant and wound botulism. Toxins 2020, 12, 586, doi: 10.3390/ toxins12090586.
Open DOI Search in Google Scholar Back to article
Carter A.T., Peck M.W.: Genomes, neurotoxins and biology of Clostridium botulinum Group I and Group II. Res Microbiol 2015, 166, 303–317, doi: 10.1016/j.resmic.2014.10.010.
Open DOI Search in Google Scholar Back to article
Collins M.D., East A.K.: Phylogeny and taxonomy of the food-borne pathogen Clostridium botulinum and its neurotoxins. J App Microbiol 1998, 84, 5–17, doi: 10.1046/j.1365-2672.1997.00313.x.
Open DOI Search in Google Scholar Back to article
Dobritsa A.P., Kutumbaka K.K., Werner K., Wiedmann M., Asmus A., Samadpour M.: Clostridium tepidum sp. nov., a close relative of Clostridium sporogenes and Clostridium botulinum Group I. Int J Syst Evol Microbiol 2017, 67, 2317–2322, doi: 10.1099/ijsem.0.001948.
Open DOI Search in Google Scholar Back to article
Goldsztejn M., Grenda T., Kozieł N., Sapała M., Mazur M., Sieradzki Z., Król B., Kwiatek K.: Potential determinants of Clostridium spp. occurrence in Polish silage. J Vet Res 2020, 64, 549–555, doi: 10.2478/jvetres-2020-0075.
Open DOI Search in Google Scholar Back to article
Grenda T., Kwiatek K., Goldsztejn M., Sapała M., Kozieł N., Domaradzki P.: Clostridia in insect processed animal proteins–is an epidemiological problem possible? Agriculture 2021, 11, 270, doi: 10.3390/agriculture11030270.
Open DOI Search in Google Scholar Back to article
Hubalek Z., Halouzka J.: Thermal sensitivity of Clostridium botulinum type C toxin. Evident Inf 1988, 101, 321–332, doi: 10.1017/s095026880005425x.
Open DOI Search in Google Scholar Back to article
Institute of Meteorology and Water Management (IMGW): Bulletin of Climate Monitoring. https://klimat.imgw.pl/pl/biuletyn-monitoring
Search in Google Scholar Back to article
Johnson A.L., McAdams-Gallagher S.C., Aceto H.: Accuracy of a Mouse Bioassay for the Diagnosis of Botulism in Horses. J Vet Intern Med 2016, 30, 1293–1299, doi: 10.1111/jvim.13950.
Open DOI Search in Google Scholar Back to article
Kirchner S., Krämer K.M., Schulze M., Pauly D., Jacob D., Gessler F., Nitsche A., Dorner B.G., Dorner M.B.: Pentaplexed quantitative real-time PCR assay for the simultaneous detection and quantification of botulinum neurotoxin-producing clostridia in food and clinical samples. Appl Environ Microbiol 2010, 76, 4387–4395, doi: 10.1128/AEM.02490-09.
Open DOI Search in Google Scholar Back to article
Le Maréchal C., Woudstra C., Fach P. Botulism. In: Clostridial Diseases of Animals edited by F.A. Uzal, J.G. Songer, J.F. Prescott, M.R. Popoff, John Wiley & Sons, Hoboken, NJ 2016, pp. 303–330.
Search in Google Scholar Back to article
Lindström M., Korkeala H.: Laboratory diagnostics of botulism. Clin Microbiol Rev 2006, 19, 298–314, doi: 10.1128/CMR.19.2.298-314.2006.
Open DOI Search in Google Scholar Back to article
Lindström M., Nevas M., Kurki J., Sauna-aho R., Latvala-Kiesilä A., Pölönen I., Korkeala H.: Type C botulism due to toxic feed affecting 52,000 farmed foxes and minks in Finland. J Clin Microbiol 2004, 42, 4718–4725, doi: 10.1128/ JCM.42.10.4718-4725.2004.
Open DOI Search in Google Scholar Back to article
Maikanov B., Mustafina R., Auteleyeva L., Wiśniewski J., Anusz K., Grenda T., Kwiatek K., Goldsztejn M., Grabczak M.: Clostridium botulinum and Clostridium perfringens occurrence in Kazakh honey samples. Toxins 2019, 11, 472, doi: 10.3390/toxins11080472.
Open DOI Search in Google Scholar Back to article
Moeller R.B. Jr., Puschner B.: Botulism in Cattle – A Review. Bov Pract 2007, 41, 54–58, doi: 10.21423/bovine-vol41no1p54-58.
Open DOI Search in Google Scholar Back to article
Moeller R.B. Jr., Puschner B., Walker R.L., Rocke T., Galey F.D., Cullor J.S., Ardans A.A.: Determination of the median toxic dose of type C botulinum toxin in lactating dairy cows. J Vet Diagn Invest 2003, 15, 523–526, doi: 10.1177/104063870301500603.
Open DOI Search in Google Scholar Back to article
Myllykoski J., Lindström M., Bekema E., Pölönen I., Korkeala H.: Fur animal botulism hazard due to feed. Res Vet Sci 2011, 90, 412–418, doi: 10.1016/j.rvsc.2010.06.02.
Open DOI Search in Google Scholar Back to article
Nakamura K., Kohda T., Umeda K., Yamamoto H., Mukamoto M., Kozaki S.: Characterization of the D/C mosaic neurotoxin produced by Clostridium botulinum associated with bovine botulism in Japan. Vet Microbiol 2010, 140, 147–154, doi: 10.1016/j.vetmic.2009.07.023.
Open DOI Search in Google Scholar Back to article
Peck M.W., Smith T.J., Anniballi F., Austin J.W., Bano L., Bradshaw M., Cuervo P., Cheng L.W., Derman Y., Dorner B.G., Fisher A., Hill K.K., Kalb S.R., Korkeala H., Lindström M., Lista F., Lúquez C., Mazuet C., Pirazzini M., Popoff M.R., Rossetto O., Rummel A., Sesardic D., Singh B.R., Stringer S.C.: Historical perspectives and guidelines for botulinum neurotoxin subtype nomenclature. Toxins 2017, 9, 38, doi: 10.3390/ toxins9010038.
Open DOI Search in Google Scholar Back to article
Polish Committee for Standardization (PKN): PN-R-64791:1994: Animal feeding stuffs – Requirements and microbiological examinations. Polski Komitet Normalizacyjny, Warsaw, 1994.
Search in Google Scholar Back to article
Raphael B.H., Andreadis J.D.: Real-time PCR detection of the nontoxic nonhemagglutinin gene as a rapid screening method for bacterial isolates harboring the botulinum neurotoxin (A–G) gene complex. J Microbiol Methods 2007, 71, 343–346, doi: 10.1016/j.mimet.2007.09.016.
Open DOI Search in Google Scholar Back to article
Roberts T.A., Collings D.F.: An outbreak of type-C botulism in broiler chickens. Avian Dis 1973, 17, 650–658, doi: 10.1136/ vr.100.18.378.
Open DOI Search in Google Scholar Back to article
Seyboldt C., Discher S., Jordan E., Neubauer H., Jensen K.C., Campe A., Kreienbrock L., Scheu T., Wichern A., Gundling F., DoDuc P., Fohler S., Abdulmawjood A., Klein G., Hoedemaker M.: Occurrence of Clostridium botulinum neurotoxin in chronic disease of dairy cows. Vet Microbiol 2015, 177, 398–402, doi: 10.1016/j.vetmic.2015.03.012.
Open DOI Search in Google Scholar Back to article
Skarin H., Håfström T., Westerberg J., Segerman B.: Clostridium botulinum group III: a group with dual identity shaped by plasmids, phages and mobile elements. BMC Genomics 2011, 12, 185, doi: 10.1186/1471-2164-12-185.
Open DOI Search in Google Scholar Back to article
Smith T.J., Hill K.K., Raphael B.H.: Historical and current perspectives on Clostridium botulinum diversity. Res Microbiol 2015, 166, 290–302, doi: 10.1016/j.resmic.2014.09.007.
Open DOI Search in Google Scholar Back to article
Solomon H.M., Lilly T. Jr.: Clostridium botulinum In: Bacteriological Analytical Manual Online, Revision A edited by R.I. Merker, Center for Food Safety and Applied Nutrition, Food and Drug Administration, Silver Spring, MD, 2001.
Search in Google Scholar Back to article
Souillard R., Le Maréchal C., Balaine L., Rouxel S., Poezevara T., Ballan V., Chemaly M., Le Bouquin S.: Manure contamination with Clostridium botulinum after avian botulism outbreaks: management and potential risk of dissemination. Vet Rec 2020, 19, 233, doi: 10.1136/vr.105898.
Open DOI Search in Google Scholar Back to article
Statistics Poland (GUS): Statistical Yearbook of Agriculture 2020. Statistics Poland, Warsaw, 2021. https://stat.gov.pl/en/topics/statistical-yearbooks/statistical-yearbooks/statistical-yearbook-of-agriculture-2020,6,15.html
Search in Google Scholar Back to article
Tjaberg T.B., Skulberg A.: Minks mottagelighet for C. botulinum type C-toksin (Susceptibility of mink to C. botulinum type C toxin). Nord Vet Med 1968, 20, 313–318.
Search in Google Scholar Back to article
Trampel D.W., Smith S.R., Rocke T.E.: Toxicoinfectious botulism in commercial caponized chickens. Avian Dis 2005, 49, 301–303, doi: 10.1637/7330-011805.
Open DOI Search in Google Scholar Back to article
Wilson D.J., Baldwin T.J., Whitehouse C.H., Hullinger G.: Causes of mortality in farmed mink in the Intermountain West, North America. J Vet Diagn Invest 2015, 27, 470–475, doi: 10.1177/1040638715586438.
Open DOI Search in Google Scholar Back to article
Woudstra C., Le Maréchal C., Souillard R., Bayon-Auboyer M.-H., Mermoud I., Desoutter D., Fach P.: New insights into the genetic diversity of Clostridium botulinum group III through extensive genome exploration. Front Microbiol 2016, 7, 757, doi: 10.3389/fmicb.2016.00757.
Open DOI Search in Google Scholar Back to article
Zhang S., Masuyer G., Zhang J., Shen Y., Lundin D., Henriksson L., Miyashita S.I., Martínez-Carranza M., Dong M., Stenmark P.: Identification and characterization of a novel botulinum neurotoxin. Nat Commun 2017, 8, 14130, doi: 10.1038/ncomms14130.
Open DOI Search in Google Scholar Back to article