Epidemiological and epizootological aspects of botulism in Ukraine
Abstract
Botulism remains one of the most dangerous toxic infections in humans and animals, characterized by severe neuroparalytic manifestations and a high mortality rate. The causative agent Clostridium botulinum is a naturally occurring anaerobe capable of long-term preservation in spore form and production of an extremely potent botulinum neurotoxin (BoNT). Despite considerable attention being paid to this disease and changes in European veterinary legislation, botulism remains a pressing problem worldwide and, in particular, in Ukraine, both in terms of veterinary safety and public health. The study was conducted to analyze the epizootological and epidemiological characteristics of botulism in Ukraine over the past 15 years among animals and 10 years – among humans. The data sources were reports from regional laboratories of the State Service of Ukraine for Food Safety and Consumer Protection, research results from the State Scientific and Research Institute of Laboratory Diagnostics and Veterinary and Sanitary Expertise, and information from the Public Health Center of the Ministry of Health of Ukraine. All cases were confirmed by laboratory tests (immunofluorescence assay, bioassay on laboratory animals). For statistical analysis, binomial confidence intervals (BCI) calculated using the Klopper-Pearson method were used, and for visualization, the QGIS 3.16 program was used with cartographic layers of the admi n istrative boundaries of Ukraine. During the period under review, 7 , 031 positive cases of botulism were registered among animals and in feed, of which 77.9% (BCI, 77.0–78.9%) were isolates from feed and 22.1% (BCI, 21.1–23.1%) were from animals. Among the affected farm animals, pigs (41.6%), cattle (21.9%), and horses (7.8%) dominated. A significant number of cases were registered among cats, dogs, minks, foxes, wild rodents, and poultry, which were grouped into the category “others” and accounted for 28.8% (BCI, 26.5–31.1%). The highest number of positive cases among animals and feed was recorded in the Luhansk (80.2%), Vinnytsia (12.7%), and Donetsk (5.0%) regions. At the same time, between 2018 and 2024, the number of tests decreased significantly: only one positive sample was found in feed, which is more than 500 times less than in the previous seven years. Between 2015 and 2024, 1,070 cases of botulism were registered in humans, mainly in the central and northwestern regions. The results indicate a decrease in the intensity of diagnostic st u dies, which may lead to an underestimation of the real epizootic situation. It is necessary to restore syst e matic monitoring, feed control, and strengthen biosafety o n farms as key elements of botulism prevention in Ukraine.References
Anniballi, F., Lonati, D., Fiore, A., Auricchio, B., De Medici, D., & Locatelli, C. A. (2014). New targets in the search for preventive and therapeutic agents for botulism. Expert Review of Anti-Infective Therapy, 12(9), 1075–1086.
Arnon, S. S., Schechter, R., Inglesby, T. V., Henderson, D. A., Bartlett, J. G., Ascher, M. S., Eitzen, E., Fine, A. D., Hauer, J., Layton, M., Lillibridge, S., Osterholm, M. T., O'Toole, T., Parker, G., Perl, T. M., Russell, P. K., Swerdlow, D. L., & Tonat, K. (2001). Botulinum toxin as a biological weapon: Medical and public health management. Journal of the American Medical Association, 285(8), 1059–1070.
Baum, S. E., Machalaba, C., Daszak, P., Salerno, R. H., & Karesh, W. B. (2016). Evaluating one health: Are we demonstrating effectiveness? One Health, 3, 5–10.
Bordier, M., Uea-Anuwong, T., Binot, A., Hendrikx, P., & Goutard, F. L. (2020). Characteristics of One Health surveillance systems: A systematic literature review. Preventive Veterinary Medicine, 181, 104560.
Castor, C., Mazuet, C., Saint-Leger, M., Vygen, S., Coutureau, J., Durand, M., Popoff, M. R., & Jourdan Da Silva, N. (2015). Cluster of two cases of botulism due to Clostridium baratii type F in France, November 2014. European Communicable Disease Bulletin, 20(6), 21031.
Czerwiński, M., Czarkowski, M. P., & Kondej, B. (2018). Foodborne botulism in Poland in 2016. Przeglad Epidemiologiczny, 72(2), 149–155.
Defilippo, F., Luppi, A., Maioli, G., Marzi, D., Fontana, M. C., Paoli, F., Bonilauri, P., Dottori, M., & Merialdi, G. (2013). Outbreak of type C botulism in birds and mammals in the Emilia Romagna Region, Northern Italy. Journal of Wildlife Diseases, 49(4), 1042–1046.
Divers, T. J., Bartholomew, R. C., Messick, J. B., Whitlock, R. H., & Sweeney, R. W. (1986). Clostridium botulinum type B toxicosis in a herd of cattle and a group of mules. Journal of the American Veterinary Medical Association, 188(4), 382–386.
Duncan, R. M., & Jensen, W. L. (1976). A relationship between avian carcasses and living invertebrates in the epizootiology of avian botulism. Journal of Wildlife Diseases, 12(1), 116–126.
Espelund, M., & Klaveness, D. (2014). Botulism outbreaks in natural environments – an update. Frontiers in Microbiology, 5, 287.
Fillo, S., Giordani, F., Tonon, E., Drigo, I., Anselmo, A., Fortunato, A., Lista, F., & Bano, L. (2021). Extensive genome exploration of Clostridium botulinum group III field strains. Microorganisms, 9(11), 2347.
Fleck-Derderian, S., Shankar, M., Rao, A. K., Chatham-Stephens, K., Adjei, S., Sobel, J., Meltzer, M. I., Meaney-Delman, D., & Pillai, S. K. (2017). The epidemiology of foodborne botulism outbreaks: A systematic review. Clinical Infectious Diseases, 66(1), 73–81.
Frye, E. A., Egan, C., Perry, M. J., Crouch, E. E., Burbank, K. E., & Kelly, K. M. (2020). Outbreak of botulism type A in dairy cows detected by MALDI-TOF mass spectrometry. Journal of Veterinary Diagnostic Investigation, 32(5), 722–726.
Galey, F. D. (2001). Botulism in the horse. The Veterinary Clinics of North America, Equine Practice, 17(3), 579–588.
Galey, F. D., Terra, R., Walker, R., Adaska, J., Etchebarne, M. A., Puschner, B., Fisher, E., Whitlock, R. H., Rocke, T., Willoughby, D., & Tor, E. (2000). Type C botulism in dairy cattle from feed contaminated with a dead cat. Journal of Veterinary Diagnostic Investigation, 12(3), 204–209.
Guizelini, C. C., Lemos, R. A. A., de Paula, J. L. P., Pupin, R. C., Gomes, D. C., Barros, C. S. L., Neves, D. A., Alcântara, L. O. B., Silva, R. O. S., Lobato, F. C. F., & Martins, T. B. (2019). Type C botulism outbreak in feedlot cattle fed contaminated corn silage. Anaerobe, 55, 103–106.
Hannett, G. E., Stone, W. B., Davis, S. W., & Wroblewski, D. (2011). Biodiversity of Clostridium botulinum type E associated with a large outbreak of botulism in wildlife from Lake Erie and Lake Ontario. Applied and Environmental Microbiology, 77(3), 1061–1068.
Harris, R., Tchao, C., Prystajecky, N., Cutler, J., & Austin, J. W. (2021). A summary of surveillance, morbidity and microbiology of laboratory-confirmed cases of infant botulism in Canada, 1979–2019. Canada Communicable Disease Report, 47(78), 322–328.
Hill, K. K., & Smith, T. J. (2013). Genetic diversity within Clostridium botulinum serotypes, botulinum neurotoxin gene clusters and toxin subtypes. Current Topics in Microbiology and Immunology, 364, 1–20.
Janik, E., Ceremuga, M., Saluk-Bijak, J., & Bijak, M. (2019). Biological toxins as the potential tools for bioterrorism. International Journal of Molecular Sciences, 20(5), 1181.
Johnson, A. L., McAdams, S. C., & Whitlock, R. H. (2010). Type A botulism in horses in the United States: A review of the past ten years (1998–2008). Journal of Veterinary Diagnostic Investigation, 22(2), 165–173.
Johnson, A. L., McAdams-Gallagher, S. C., & Aceto, H. (2016). Accuracy of a mouse bioassay for the diagnosis of botulism in horses. Journal of Veterinary Internal Medicine, 30(4), 1293–1299.
Kalb, S. R., Baudys, J., Raphael, B. H., Dykes, J. K., Lúquez, C., Maslanka, S. E., & Barr, J. R. (2015). Functional characterization of botulinum neurotoxin serotype H as a hybrid of known serotypes F and A (BoNT F/A). Analytical Chemistry, 87(7), 3911–3917.
Karsen, H., Ceylan, M. R., Bayındır, H., & Akdeniz, H. (2019). Foodborne botulism in Turkey, 1983 to 2017. Infectious Diseases, 51(2), 91–96.
Kelch, W. J., Kerr, L. A., Pringle, J. K., Rohrbach, B. W., & Whitlock, R. H. (2000). Fatal Clostridium botulinum toxicosis in eleven Holstein cattle fed round bale barley haylage. Journal of Veterinary Diagnostic Investigation, 12(5), 453–455.
Kenri, T., Sekizuka, T., Yamamoto, A., Iwaki, M., Komiya, T., Hatakeyama, T., Nakajima, H., Takahashi, M., Kuroda, M., & Shibayama, K. (2014). Genetic characterization and comparison of Clostridium botulinum isolates from botulism cases in Japan between 2006 and 2011. Applied and Environmental Microbiology, 80(22), 6954–6964.
Khorasan, M. R. M., Rahbar, M., Bialvaei, A. Z., Gouya, M. M., Shahcheraghi, F., & Eshrati, B. (2020). Prevalence, risk factors, and epidemiology of food-borne botulism in Iran. Journal of Epidemiology and Global Health, 10(4), 288–292.
Krüger, M., Neuhaus, J., Herrenthey, A. G., Gökce, M. M., Schrödl, W., & Shehata, A. A. (2014). Chronic botulism in a Saxony dairy farm: Sources, predisposing factors, development of the disease and treatment possibilities. Anaerobe, 28, 220–225.
Le Bouquin, S., Lucas, C., Souillard, R., Le Maréchal, C., Petit, K., Kooh, P., Jourdan-Da Silva, N., Meurens, F., Guillier, L., & Mazuet, C. (2022). Human and animal botulism surveillance in France from 2008 to 2019. Frontiers in Public Health, 10, 1003917.
Le Maréchal, C., Ballan, V., Rouxel, S., Bayon-Auboyer, M. H., Baudouard, M. A., Morvan, H., Houard, E., Poëzevara, T., Souillard, R., Woudstra, C., Le Bouquin, S., Fach, P., & Chemaly, M. (2016). Livers provide a reliable matrix for real-time PCR confirmation of avian botulism. Anaerobe, 38, 7–13.
Le Maréchal, C., Rouxel, S., Ballan, V., Houard, E., Poezevara, T., Bayon-Auboyer, M. H., Souillard, R., Morvan, H., Baudouard, M. A., Woudstra, C., Mazuet, C., Le Bouquin, S., Fach, P., Popoff, M., & Chemaly, M. (2017). Development and validation of a new reliable method for the diagnosis of avian botulism. PloS One, 12(1), e0169640.
Lindström, M., Nevas, M., Kurki, J., Sauna-aho, R., Latvala-Kiesilä, A., Pölönen, I., & Korkeala, H. (2004). Type C botulism due to toxic feed affecting 52,000 farmed foxes and minks in Finland. Journal of Clinical Microbiology, 42(10), 4718–4725.
Maslanka, S. E., Lúquez, C., Dykes, J. K., Tepp, W. H., Pier, C. L., Pellett, S., Raphael, B. H., Kalb, S. R., Barr, J. R., Rao, A., & Johnson, E. A. (2016). A novel botulinum neurotoxin, previously reported as serotype H, has a hybrid-like structure with regions of similarity to the structures of serotypes A and F and is neutralized with serotype A antitoxin. The Journal of Infectious Diseases, 213(3), 379–385.
Myllykoski, J., Lindström, M., Keto-Timonen, R., Söderholm, H., Jakala, J., Kallio, H., Sukura, A., & Korkeala, H. (2009). Type C bovine botulism outbreak due to carcass contaminated non-acidified silage. Epidemiology and Infection, 137(2), 284–293.
Nakamura, K., Kohda, T., Seto, Y., Mukamoto, M., & Kozaki, S. (2013). Improved detection methods by genetic and immunological techniques for botulinum C/D and D/C mosaic neurotoxins. Veterinary Microbiology, 162(2–4), 881–890.
Notermans, S. H., Havelaar, A. H., Dufrenne, J. B., & Oosterom, J. (1985). Voorkomen van Clostridium botulinum op rundveehouderij bedrijven [Incidence of Clostridium botulinum on cattle farms]. Tijdschrift Voor Diergeneeskunde, 110(5), 175–180.
Panditrao, M. V., Dabritz, H. A., Kazerouni, N. N., Damus, K. H., Meissinger, J. K., & Arnon, S. S. (2020). Descriptive epidemiology of infant botulism in California: The first 40 years. The Journal of Pediatrics, 227, 247–257.
Peck, M. W. (2009). Biology and genomic analysis of Clostridium botulinum. Advances in Microbial Physiology, 55, 183–320.
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., & Stringer, S. C. (2017). Historical perspectives and guidelines for botulinum neurotoxin subtype nomenclature. Toxins, 9(1), 38.
Popoff, M. R. (1989). Revue scientifique et technique. International Office of Epizootics, 8(1), 129–145.
Rasetti-Escargueil, C., Lemichez, E., & Popoff, M. R. (2019). Public health risk associated with botulism as foodborne zoonoses. Toxins, 12(1), 17.
Rasetti-Escargueil, C., Lemichez, E., & Popoff, M. R. (2020). Toxemia in human naturally acquired botulism. Toxins, 12(11), 716.
Rawson, A. M., Dempster, A. W., Humphreys, C. M., & Minton, N. P. (2023). Pathogenicity and virulence of Clostridium botulinum. Virulence, 14(1), 2205251.
Relun, A., Dorso, L., Douart, A., Chartier, C., Guatteo, R., Mazuet, C., Popoff, M. R., & Assié, S. (2017). A large outbreak of bovine botulism possibly linked to a massive contamination of grass silage by type D/C Clostridium botulinum spores on a farm with dairy and poultry operations. Epidemiology and Infection, 145(16), 3477–3485.
Rogers, K. H., Viera, O. G., Uzal, F. A., Peronne, L., & Mete, A. (2021). Mortality of western gulls (Larus occidentalis) associated with botulism type a in coastal Southern California, USA. Journal of Wildlife Diseases, 57(3), 657–661.
Rossetto, O., Pirazzini, M., Fabris, F., & Montecucco, C. (2021). Botulinum neurotoxins: Mechanism of action. Handbook of Experimental Pharmacology, 263, 35–47.
Schocken-Iturrino, R. P., Avila, F. A., Berchielli, S. C., & Nader Filho, A. (1990). First case of type A botulism in zebu (Bos indicus). The Veterinary record, 126(9), 217–218.
Semenko, N., Mokhort, H., Sokolovska, O., Kolesnikova, I., Kuzin, I., & Saylors, K. (2021). Foodborne botulism in Ukraine from 1955 to 2018. Foodborne Pathogens and Disease, 18(4), 260–266.
Smith, T. J., Lou, J., Geren, I. N., Forsyth, C. M., Tsai, R., Laporte, S. L., Tepp, W. H., Bradshaw, M., Johnson, E. A., Smith, L. A., & Marks, J. D. (2005). Sequence variation within botulinum neurotoxin serotypes impacts antibody binding and neutralization. Infection and Immunity, 73(9), 5450–5457.
Sobel, J. (2005). Botulism. Clinical Infectious Diseases, 41(8), 1167–1173.
Souillard, R., Woudstra, C., Le Maréchal, C., Dia, M., Bayon-Auboyer, M. H., Chemaly, M., Fach, P., & Le Bouquin, S. (2014). Investigation of Clostridium botulinum in commercial poultry farms in France between 2011 and 2013. Avian Pathology, 43(5), 458–464.
Takeda, M., Tsukamoto, K., Kohda, T., Matsui, M., Mukamoto, M., & Kozaki, S. (2005). Characterization of the neurotoxin produced by isolates associated with avian botulism. Avian Diseases, 49(3), 376–381.
Therre, H. (1999). Botulism in the European Union. European Communicable Disease Bulletin, 4(1), 2–7.
Tréhard, H., Poujol, I., Mazuet, C., Blanc, Q., Gillet, Y., Rossignol, F., Popoff, M. R., & Jourdan Da Silva, N. (2016). A cluster of three cases of botulism due to Clostridium baratii type F, France, August 2015. European Communicable Disease Bulletin, 21(4), 10.2807/1560-7917.ES.2016.21.4. 30117.
Ventujol, A., Decors, A., Le Maréchal, C., Toux, J. Y., Allain, V., & Mazuet, C. (2017). Le botulisme aviaire en France: Etude des cas signales dans la faune sauvage et dans les élevages par deux reseaux de surveillance entre 2000 et 2013. Epidemiologique Sante Animale, 72, 85–102.
Vidal, D., Anza, I., Taggart, M. A., Pérez-Ramírez, E., Crespo, E., Hofle, U., & Mateo, R. (2013). Environmental factors influencing the prevalence of a Clostridium botulinum type C/D mosaic strain in nonpermanent Mediterranean wetlands. Applied and Environmental Microbiology, 79(14), 4264–4271.
Wilson, R. B., Boley, M. T., & Corwin, B. (1995). Presumptive botulism in cattle associated with plastic-packaged hay. Journal of Veterinary Diagnostic Investigation, 7(1), 167–169.
Woudstra, C., Skarin, H., Anniballi, F., Fenicia, L., Bano, L., Drigo, I., Koene, M., Bäyon-Auboyer, M. H., Buffereau, J. P., De Medici, D., & Fach, P. (2012). Neurotoxin gene profiling of Clostridium botulinum types C and D native to different countries within Europe. Applied and Environmental Microbiology, 78(9), 3120–3127.
Yeruham, I., Elad, D., Avidar, Y., Grinberg, K., Tiomkin, D., & Monbaz, A. (2003). Outbreak of botulism type B in a dairy cattle herd: Clinical and epidemiological aspects. The Veterinary Record, 153(9), 270–272.
Zhang, S., Masuyer, G., Zhang, J., Shen, Y., Lundin, D., Henriksson, L., Miyashita, S. I., Martínez-Carranza, M., Dong, M., & Stenmark, P. (2017). Identification and characterization of a novel botulinum neurotoxin. Nature Communications, 8, 14130.
Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons «Attribution» 4.0 License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.
