Honey Sold Directly by Producers in the Silesian Region of Poland as a Source of Clostridium botulinum
Types A, B, E, and F

https://doi.org/10.17221/376/2016-CJFSCitation:

Wysok B., Wojtacka J., Karczmarczyk R., Wiszniewska-Łaszczych A., Gomółka-Pawlicka M., Szteyn J., Liedtke K. (2017): Honey sold directly by producers in the Silesian region of Poland as a source of Clostridium botulinum types A, B, E, and F. Czech J. Food Sci., 35: 194–199.

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The level of contamination of honey with Clostridium botulinum spores is considered as an indicator of the adequacy of hygienic practices during collection, extraction, and subsequent processing. A total of 39 honey samples purchased directly from beekeepers at outdoor markets and from small amateur apiaries in Silesia were analysed for Clostridium botulinum spores. The samples were prepared using a dilution centrifugation method and cultured in parallel in cooked meat medium (CMM) and tripticase peptone glucose yeast (TPGY) enrichment broths. Identification of C. botulinum toxin types A, B, E, and F was performed with the use of a multiplex PCR method. The analysis showed six (15.4%) samples to be contaminated with C. botulinum spores. The major serotypes detected were type A – in two (5.1%) and type B – in two (5.1%) honey samples, respectively. Types E and F were found in 1 (2.6%) and 1 (2.6%) positive honey sample analysed, respectively.

References:
Arnon S.S. (1998): Infant botulism. In: Feifen R.D., Cherry J.D., Saunders W.B. (eds): Textbook of Pediatric Infectious Diseases. Philadelphia, Elsevier Inc.: 1758–1766.
 
Arnon S.S., Midura T.F., Damus K., Thompson B., Wood R.M., Chin J. (1979): Honey and other environmental risk factors for infant botulism. The Journal of Pediatrics, 94: 331–336. https://doi.org/10.1016/S0022-3476(79)80863-X
 
Bianco M.I., Luquez C., de Jong L.I.T., Fernanadez R.A. (2009): Linden flower (Tilia spp) as potential vehicle of Clostridium botulinum spores in the transmission of infant botulism. Revista Argentina de Microbiología, 41: 232–236.
 
Böhnel H., Behrens S., Loch P., Lube K., Gessler F. (2001): Is there a link between infant botulism and sudden infant death? Bacteriological results obtained in Central Germany. European Journal of Pediatrics, 160: 623–628. https://doi.org/10.1007/s004310100807
 
Estevinho L.M., Feás X., Seijas J.A., Vazquez-Tato M.P. (2012): Organic honey from Trás-Os-Montes region (Portugal): Chemical, palynological, microbiological and bioactive compounds characterization. Food and Chemical Toxicology, 50: 258–264. https://doi.org/10.1016/j.fct.2011.10.034
 
Fenicia L., Anniballi F., De Medici D., Delibato E., Aureli P. (2007): SYBR green real-time PCR method to detect Clostridium botulinum type A. Applied and Environmental Microbiology, 73: 2891–2896. https://doi.org/10.1128/AEM.02234-06
 
Gale P., Drew T., Phipps L.P., David G., Wooldridge M. (2009): The effect of climate change on the occurrence and prevalence of livestock diseases in Great Britain: a review. Journal of Applied Microbiology, 106: 1409–1423. https://doi.org/10.1111/j.1365-2672.2008.04036.x
 
Huss H.H. (1980): Distribution of Clostridium botulinum. Applied and Environmental Microbiology, 39: 764–769. https://doi.org/10.1128/AEM.39.4.764-769.1980
 
Kędzia B., Kędzia A., Hołderna-Kędzia E. (1996): Badania nad występowaniem w miodzie przetrwalników laseczek Bacillus i Clostridium. In: Proceedings XXXIIIth Naukowa Konferencja Pszczelarska, March 12–13, 1996, Puławy, Poland: 37–39.
 
Kędzia B., Hołderna-Kędzia E. (2010): Lecznicze działanie miodu pszczelego w chorobach wewnętrznych. Wrocław, MedPharm Polska: 363–372.
 
Koluman A., Melikoglu Golcu B., Derin O., Ozkok S., Anniballi F. (2013): Clostridium botulinum in honey: prevalence and antibiotic susceptibility of isolated strains. Turkish Journal of Veterinary and Animal Sciences, 37: 706–711. https://doi.org/10.3906/vet-1209-40
 
Küplülü Ö., Göncüoğlu M., Özdemir H., Koluman A. (2006): Incidence of Clostridium botulinum spores in honey in Turkey. Food Control, 17: 222–224. https://doi.org/10.1016/j.foodcont.2004.10.004
 
Loncaric I., Ruppitsch W., Licek E., Moosbeckhofer R., Busse H.J., Rosengarten R. (2011): Characterization of selected Gram-negative non-fermenting bacteria isolated from honey bees (Apis melifera carnica). Apidologie, 42: 312–325. https://doi.org/10.1007/s13592-011-0019-7
 
Luquez C., Bianco M.I., de Jong L.I.T., Sagua M.D., Arenas G.N., Ciccarelli A.S., Fernandez R.A. (2005): Distribution of botulinum toxin-producing Clostridia in soils of Argentina. Applied and Environmental Microbiology, 71: 4137–4139. https://doi.org/10.1128/AEM.71.7.4137-4139.2005
 
Madras-Majewska B., Nowakowska A., Rosiak E. (2014): Evaluation of microbial quality of imported honeys available on the Warsaw market. In: Proceedings of International Symposium on Bee Products. 3rd Ed. Annual meeting of the International Honey Commission (IHC), Sept 28–Oct 1, 2014, Opatija, Croatia: 117.
 
Nakano H., Kizaki H., Sakaguchi G. (1994): Multiplication of Clostridium botulinum in dead honey-bees and bee pupae, a likely source of heavy contamination of honey. International Journal of Food Microbiology, 21: 247–252. https://doi.org/10.1016/0168-1605(94)90031-0
 
Nevas M., Hielm S., Lindström M., Koivulehto M., Horn H., Korkeala H. (2002): High prevalence of Clostridium botulinum types A and B in honey samples detected by polymerase chain reaction. International Journal of Food Microbiology, 72: 45–52. https://doi.org/10.1016/S0168-1605(01)00615-8
 
Nevas M., Lindström M., Hautamäki K., Puoskari S., Korkeala H. (2005): Prevalence and diversity of Clostridium botulinum types A, B, E and F in honey produced in the Nordic countries. International Journal of Food Microbiology, 105: 145–151. https://doi.org/10.1016/j.ijfoodmicro.2005.04.007
 
Nevas M., Lindström M., Hörman A., Keto-Timonen R., Korkeala H. (2006): Contamination routes of Clostridium botulinum in the honey production environment. Environmental Microbiology, 8: 1085–1094. https://doi.org/10.1111/j.1462-2920.2006.001000.x
 
Palacio A.M., Figini E.F., Ruffinengo S.R., Rodriguez E.M., del Hoyo M.L., Bedascarrasbure E.L. (2000): Changes in a population of Apis mellifera L. selected for hygienic behaviour and its relation to brood disease tolerance. Apidologie, 31: 471–478. https://doi.org/10.1051/apido:2000139
 
PN-88/A-77626 (1988): “Miód pszczeli”. Dziennik Norm i Miar nr 8. Warszawa, Polska, Wydawnictwo Normalizacyjne Alfa.
 
Roman A., Popiela-Pleban E., Kozak M. (2013): Factors influencing consumer behavior relating to the purchasing of honey. Part 1. The buying process and the level of consumption. Journal of Apicultural Science, 57: 159–172. https://doi.org/10.2478/jas-2013-0026
 
Różańska H. (2011): Microbiological quality of Polish honey. Bulletin of the Veterinary Institute in Pulawy, 55: 443–445.
 
Satorres S.E., Alcaraz L.E., Fernández R.A., Centorbi O.N. (1999): Isolation of Clostridium botulinum in medical plants. Anaerobe, 5: 173–175. https://doi.org/10.1006/anae.1999.0205
 
Semkiw P., Ochal J. (2012): Sektor pszczelarski w Polsce w 2012 roku. Instytut Ogrodnictwa Oddział Pszczelnictwa, Puławy. Available at: www.opisik.pulawy.pl/pdf/SP2012.pdf (accessed August 22, 2016)
 
Sobel J. (2005): Botulism. Clinical Infectious Diseases, 41: 1167–1173. https://doi.org/10.1086/444507
 
Spivak M., Downey D.L. (1998): Field Assays for Hygienic Behavior in Honey Bees (Hymenoptera: Apidae). Journal of Economic Entomology, 91: 64–70. https://doi.org/10.1093/jee/91.1.64
 
Arnon S.S. (1998): Infant botulism. In: Feifen R.D., Cherry J.D., Saunders W.B. (eds): Textbook of Pediatric Infectious Diseases. Philadelphia, Elsevier Inc.: 1758–1766.
 
Arnon S.S., Midura T.F., Damus K., Thompson B., Wood R.M., Chin J. (1979): Honey and other environmental risk factors for infant botulism. The Journal of Pediatrics, 94: 331–336. https://doi.org/10.1016/S0022-3476(79)80863-X
 
Bianco M.I., Luquez C., de Jong L.I.T., Fernanadez R.A. (2009): Linden flower (Tilia spp) as potential vehicle of Clostridium botulinum spores in the transmission of infant botulism. Revista Argentina de Microbiología, 41: 232–236.
 
Böhnel H., Behrens S., Loch P., Lube K., Gessler F. (2001): Is there a link between infant botulism and sudden infant death? Bacteriological results obtained in Central Germany. European Journal of Pediatrics, 160: 623–628. https://doi.org/10.1007/s004310100807
 
Estevinho L.M., Feás X., Seijas J.A., Vazquez-Tato M.P. (2012): Organic honey from Trás-Os-Montes region (Portugal): Chemical, palynological, microbiological and bioactive compounds characterization. Food and Chemical Toxicology, 50: 258–264. https://doi.org/10.1016/j.fct.2011.10.034
 
Fenicia L., Anniballi F., De Medici D., Delibato E., Aureli P. (2007): SYBR green real-time PCR method to detect Clostridium botulinum type A. Applied and Environmental Microbiology, 73: 2891–2896. https://doi.org/10.1128/AEM.02234-06
 
Gale P., Drew T., Phipps L.P., David G., Wooldridge M. (2009): The effect of climate change on the occurrence and prevalence of livestock diseases in Great Britain: a review. Journal of Applied Microbiology, 106: 1409–1423. https://doi.org/10.1111/j.1365-2672.2008.04036.x
 
Huss H.H. (1980): Distribution of Clostridium botulinum. Applied and Environmental Microbiology, 39: 764–769. https://doi.org/10.1128/AEM.39.4.764-769.1980
 
Kędzia B., Kędzia A., Hołderna-Kędzia E. (1996): Badania nad występowaniem w miodzie przetrwalników laseczek Bacillus i Clostridium. In: Proceedings XXXIIIth Naukowa Konferencja Pszczelarska, March 12–13, 1996, Puławy, Poland: 37–39.
 
Kędzia B., Hołderna-Kędzia E. (2010): Lecznicze działanie miodu pszczelego w chorobach wewnętrznych. Wrocław, MedPharm Polska: 363–372.
 
Koluman A., Melikoglu Golcu B., Derin O., Ozkok S., Anniballi F. (2013): Clostridium botulinum in honey: prevalence and antibiotic susceptibility of isolated strains. Turkish Journal of Veterinary and Animal Sciences, 37: 706–711. https://doi.org/10.3906/vet-1209-40
 
Küplülü Ö., Göncüoğlu M., Özdemir H., Koluman A. (2006): Incidence of Clostridium botulinum spores in honey in Turkey. Food Control, 17: 222–224. https://doi.org/10.1016/j.foodcont.2004.10.004
 
Loncaric I., Ruppitsch W., Licek E., Moosbeckhofer R., Busse H.J., Rosengarten R. (2011): Characterization of selected Gram-negative non-fermenting bacteria isolated from honey bees (Apis melifera carnica). Apidologie, 42: 312–325. https://doi.org/10.1007/s13592-011-0019-7
 
Luquez C., Bianco M.I., de Jong L.I.T., Sagua M.D., Arenas G.N., Ciccarelli A.S., Fernandez R.A. (2005): Distribution of botulinum toxin-producing Clostridia in soils of Argentina. Applied and Environmental Microbiology, 71: 4137–4139. https://doi.org/10.1128/AEM.71.7.4137-4139.2005
 
Madras-Majewska B., Nowakowska A., Rosiak E. (2014): Evaluation of microbial quality of imported honeys available on the Warsaw market. In: Proceedings of International Symposium on Bee Products. 3rd Ed. Annual meeting of the International Honey Commission (IHC), Sept 28–Oct 1, 2014, Opatija, Croatia: 117.
 
Nakano H., Kizaki H., Sakaguchi G. (1994): Multiplication of Clostridium botulinum in dead honey-bees and bee pupae, a likely source of heavy contamination of honey. International Journal of Food Microbiology, 21: 247–252. https://doi.org/10.1016/0168-1605(94)90031-0
 
Nevas M., Hielm S., Lindström M., Koivulehto M., Horn H., Korkeala H. (2002): High prevalence of Clostridium botulinum types A and B in honey samples detected by polymerase chain reaction. International Journal of Food Microbiology, 72: 45–52. https://doi.org/10.1016/S0168-1605(01)00615-8
 
Nevas M., Lindström M., Hautamäki K., Puoskari S., Korkeala H. (2005): Prevalence and diversity of Clostridium botulinum types A, B, E and F in honey produced in the Nordic countries. International Journal of Food Microbiology, 105: 145–151. https://doi.org/10.1016/j.ijfoodmicro.2005.04.007
 
Nevas M., Lindström M., Hörman A., Keto-Timonen R., Korkeala H. (2006): Contamination routes of Clostridium botulinum in the honey production environment. Environmental Microbiology, 8: 1085–1094. https://doi.org/10.1111/j.1462-2920.2006.001000.x
 
Palacio A.M., Figini E.F., Ruffinengo S.R., Rodriguez E.M., del Hoyo M.L., Bedascarrasbure E.L. (2000): Changes in a population of Apis mellifera L. selected for hygienic behaviour and its relation to brood disease tolerance. Apidologie, 31: 471–478. https://doi.org/10.1051/apido:2000139
 
PN-88/A-77626 (1988): “Miód pszczeli”. Dziennik Norm i Miar nr 8. Warszawa, Polska, Wydawnictwo Normalizacyjne Alfa.
 
Roman A., Popiela-Pleban E., Kozak M. (2013): Factors influencing consumer behavior relating to the purchasing of honey. Part 1. The buying process and the level of consumption. Journal of Apicultural Science, 57: 159–172. https://doi.org/10.2478/jas-2013-0026
 
Różańska H. (2011): Microbiological quality of Polish honey. Bulletin of the Veterinary Institute in Pulawy, 55: 443–445.
 
Satorres S.E., Alcaraz L.E., Fernández R.A., Centorbi O.N. (1999): Isolation of Clostridium botulinum in medical plants. Anaerobe, 5: 173–175. https://doi.org/10.1006/anae.1999.0205
 
Semkiw P., Ochal J. (2012): Sektor pszczelarski w Polsce w 2012 roku. Instytut Ogrodnictwa Oddział Pszczelnictwa, Puławy. Available at: www.opisik.pulawy.pl/pdf/SP2012.pdf (accessed August 22, 2016)
 
Sobel J. (2005): Botulism. Clinical Infectious Diseases, 41: 1167–1173. https://doi.org/10.1086/444507
 
Spivak M., Downey D.L. (1998): Field Assays for Hygienic Behavior in Honey Bees (Hymenoptera: Apidae). Journal of Economic Entomology, 91: 64–70. https://doi.org/10.1093/jee/91.1.64
 
Arnon S.S. (1998): Infant botulism. In: Feifen R.D., Cherry J.D., Saunders W.B. (eds): Textbook of Pediatric Infectious Diseases. Philadelphia, Elsevier Inc.: 1758–1766.
 
Arnon S.S., Midura T.F., Damus K., Thompson B., Wood R.M., Chin J. (1979): Honey and other environmental risk factors for infant botulism. The Journal of Pediatrics, 94: 331–336. https://doi.org/10.1016/S0022-3476(79)80863-X
 
Bianco M.I., Luquez C., de Jong L.I.T., Fernanadez R.A. (2009): Linden flower (Tilia spp) as potential vehicle of Clostridium botulinum spores in the transmission of infant botulism. Revista Argentina de Microbiología, 41: 232–236.
 
Böhnel H., Behrens S., Loch P., Lube K., Gessler F. (2001): Is there a link between infant botulism and sudden infant death? Bacteriological results obtained in Central Germany. European Journal of Pediatrics, 160: 623–628. https://doi.org/10.1007/s004310100807
 
Estevinho L.M., Feás X., Seijas J.A., Vazquez-Tato M.P. (2012): Organic honey from Trás-Os-Montes region (Portugal): Chemical, palynological, microbiological and bioactive compounds characterization. Food and Chemical Toxicology, 50: 258–264. https://doi.org/10.1016/j.fct.2011.10.034
 
Fenicia L., Anniballi F., De Medici D., Delibato E., Aureli P. (2007): SYBR green real-time PCR method to detect Clostridium botulinum type A. Applied and Environmental Microbiology, 73: 2891–2896. https://doi.org/10.1128/AEM.02234-06
 
Gale P., Drew T., Phipps L.P., David G., Wooldridge M. (2009): The effect of climate change on the occurrence and prevalence of livestock diseases in Great Britain: a review. Journal of Applied Microbiology, 106: 1409–1423. https://doi.org/10.1111/j.1365-2672.2008.04036.x
 
Huss H.H. (1980): Distribution of Clostridium botulinum. Applied and Environmental Microbiology, 39: 764–769. https://doi.org/10.1128/AEM.39.4.764-769.1980
 
Kędzia B., Kędzia A., Hołderna-Kędzia E. (1996): Badania nad występowaniem w miodzie przetrwalników laseczek Bacillus i Clostridium. In: Proceedings XXXIIIth Naukowa Konferencja Pszczelarska, March 12–13, 1996, Puławy, Poland: 37–39.
 
Kędzia B., Hołderna-Kędzia E. (2010): Lecznicze działanie miodu pszczelego w chorobach wewnętrznych. Wrocław, MedPharm Polska: 363–372.
 
Koluman A., Melikoglu Golcu B., Derin O., Ozkok S., Anniballi F. (2013): Clostridium botulinum in honey: prevalence and antibiotic susceptibility of isolated strains. Turkish Journal of Veterinary and Animal Sciences, 37: 706–711. https://doi.org/10.3906/vet-1209-40
 
Küplülü Ö., Göncüoğlu M., Özdemir H., Koluman A. (2006): Incidence of Clostridium botulinum spores in honey in Turkey. Food Control, 17: 222–224. https://doi.org/10.1016/j.foodcont.2004.10.004
 
Loncaric I., Ruppitsch W., Licek E., Moosbeckhofer R., Busse H.J., Rosengarten R. (2011): Characterization of selected Gram-negative non-fermenting bacteria isolated from honey bees (Apis melifera carnica). Apidologie, 42: 312–325. https://doi.org/10.1007/s13592-011-0019-7
 
Luquez C., Bianco M.I., de Jong L.I.T., Sagua M.D., Arenas G.N., Ciccarelli A.S., Fernandez R.A. (2005): Distribution of botulinum toxin-producing Clostridia in soils of Argentina. Applied and Environmental Microbiology, 71: 4137–4139. https://doi.org/10.1128/AEM.71.7.4137-4139.2005
 
Madras-Majewska B., Nowakowska A., Rosiak E. (2014): Evaluation of microbial quality of imported honeys available on the Warsaw market. In: Proceedings of International Symposium on Bee Products. 3rd Ed. Annual meeting of the International Honey Commission (IHC), Sept 28–Oct 1, 2014, Opatija, Croatia: 117.
 
Nakano H., Kizaki H., Sakaguchi G. (1994): Multiplication of Clostridium botulinum in dead honey-bees and bee pupae, a likely source of heavy contamination of honey. International Journal of Food Microbiology, 21: 247–252. https://doi.org/10.1016/0168-1605(94)90031-0
 
Nevas M., Hielm S., Lindström M., Koivulehto M., Horn H., Korkeala H. (2002): High prevalence of Clostridium botulinum types A and B in honey samples detected by polymerase chain reaction. International Journal of Food Microbiology, 72: 45–52. https://doi.org/10.1016/S0168-1605(01)00615-8
 
Nevas M., Lindström M., Hautamäki K., Puoskari S., Korkeala H. (2005): Prevalence and diversity of Clostridium botulinum types A, B, E and F in honey produced in the Nordic countries. International Journal of Food Microbiology, 105: 145–151. https://doi.org/10.1016/j.ijfoodmicro.2005.04.007
 
Nevas M., Lindström M., Hörman A., Keto-Timonen R., Korkeala H. (2006): Contamination routes of Clostridium botulinum in the honey production environment. Environmental Microbiology, 8: 1085–1094. https://doi.org/10.1111/j.1462-2920.2006.001000.x
 
Palacio A.M., Figini E.F., Ruffinengo S.R., Rodriguez E.M., del Hoyo M.L., Bedascarrasbure E.L. (2000): Changes in a population of Apis mellifera L. selected for hygienic behaviour and its relation to brood disease tolerance. Apidologie, 31: 471–478. https://doi.org/10.1051/apido:2000139
 
PN-88/A-77626 (1988): “Miód pszczeli”. Dziennik Norm i Miar nr 8. Warszawa, Polska, Wydawnictwo Normalizacyjne Alfa.
 
Roman A., Popiela-Pleban E., Kozak M. (2013): Factors influencing consumer behavior relating to the purchasing of honey. Part 1. The buying process and the level of consumption. Journal of Apicultural Science, 57: 159–172. https://doi.org/10.2478/jas-2013-0026
 
Różańska H. (2011): Microbiological quality of Polish honey. Bulletin of the Veterinary Institute in Pulawy, 55: 443–445.
 
Satorres S.E., Alcaraz L.E., Fernández R.A., Centorbi O.N. (1999): Isolation of Clostridium botulinum in medical plants. Anaerobe, 5: 173–175. https://doi.org/10.1006/anae.1999.0205
 
Semkiw P., Ochal J. (2012): Sektor pszczelarski w Polsce w 2012 roku. Instytut Ogrodnictwa Oddział Pszczelnictwa, Puławy. Available at: www.opisik.pulawy.pl/pdf/SP2012.pdf (accessed August 22, 2016)
 
Sobel J. (2005): Botulism. Clinical Infectious Diseases, 41: 1167–1173. https://doi.org/10.1086/444507
 
Spivak M., Downey D.L. (1998): Field Assays for Hygienic Behavior in Honey Bees (Hymenoptera: Apidae). Journal of Economic Entomology, 91: 64–70. https://doi.org/10.1093/jee/91.1.64
 
Arnon S.S. (1998): Infant botulism. In: Feifen R.D., Cherry J.D., Saunders W.B. (eds): Textbook of Pediatric Infectious Diseases. Philadelphia, Elsevier Inc.: 1758–1766.
 
Arnon S.S., Midura T.F., Damus K., Thompson B., Wood R.M., Chin J. (1979): Honey and other environmental risk factors for infant botulism. The Journal of Pediatrics, 94: 331–336. https://doi.org/10.1016/S0022-3476(79)80863-X
 
Bianco M.I., Luquez C., de Jong L.I.T., Fernanadez R.A. (2009): Linden flower (Tilia spp) as potential vehicle of Clostridium botulinum spores in the transmission of infant botulism. Revista Argentina de Microbiología, 41: 232–236.
 
Böhnel H., Behrens S., Loch P., Lube K., Gessler F. (2001): Is there a link between infant botulism and sudden infant death? Bacteriological results obtained in Central Germany. European Journal of Pediatrics, 160: 623–628. https://doi.org/10.1007/s004310100807
 
Estevinho L.M., Feás X., Seijas J.A., Vazquez-Tato M.P. (2012): Organic honey from Trás-Os-Montes region (Portugal): Chemical, palynological, microbiological and bioactive compounds characterization. Food and Chemical Toxicology, 50: 258–264. https://doi.org/10.1016/j.fct.2011.10.034
 
Fenicia L., Anniballi F., De Medici D., Delibato E., Aureli P. (2007): SYBR green real-time PCR method to detect Clostridium botulinum type A. Applied and Environmental Microbiology, 73: 2891–2896. https://doi.org/10.1128/AEM.02234-06
 
Gale P., Drew T., Phipps L.P., David G., Wooldridge M. (2009): The effect of climate change on the occurrence and prevalence of livestock diseases in Great Britain: a review. Journal of Applied Microbiology, 106: 1409–1423. https://doi.org/10.1111/j.1365-2672.2008.04036.x
 
Huss H.H. (1980): Distribution of Clostridium botulinum. Applied and Environmental Microbiology, 39: 764–769. https://doi.org/10.1128/AEM.39.4.764-769.1980
 
Kędzia B., Kędzia A., Hołderna-Kędzia E. (1996): Badania nad występowaniem w miodzie przetrwalników laseczek Bacillus i Clostridium. In: Proceedings XXXIIIth Naukowa Konferencja Pszczelarska, March 12–13, 1996, Puławy, Poland: 37–39.
 
Kędzia B., Hołderna-Kędzia E. (2010): Lecznicze działanie miodu pszczelego w chorobach wewnętrznych. Wrocław, MedPharm Polska: 363–372.
 
Koluman A., Melikoglu Golcu B., Derin O., Ozkok S., Anniballi F. (2013): Clostridium botulinum in honey: prevalence and antibiotic susceptibility of isolated strains. Turkish Journal of Veterinary and Animal Sciences, 37: 706–711. https://doi.org/10.3906/vet-1209-40
 
Küplülü Ö., Göncüoğlu M., Özdemir H., Koluman A. (2006): Incidence of Clostridium botulinum spores in honey in Turkey. Food Control, 17: 222–224. https://doi.org/10.1016/j.foodcont.2004.10.004
 
Loncaric I., Ruppitsch W., Licek E., Moosbeckhofer R., Busse H.J., Rosengarten R. (2011): Characterization of selected Gram-negative non-fermenting bacteria isolated from honey bees (Apis melifera carnica). Apidologie, 42: 312–325. https://doi.org/10.1007/s13592-011-0019-7
 
Luquez C., Bianco M.I., de Jong L.I.T., Sagua M.D., Arenas G.N., Ciccarelli A.S., Fernandez R.A. (2005): Distribution of botulinum toxin-producing Clostridia in soils of Argentina. Applied and Environmental Microbiology, 71: 4137–4139. https://doi.org/10.1128/AEM.71.7.4137-4139.2005
 
Madras-Majewska B., Nowakowska A., Rosiak E. (2014): Evaluation of microbial quality of imported honeys available on the Warsaw market. In: Proceedings of International Symposium on Bee Products. 3rd Ed. Annual meeting of the International Honey Commission (IHC), Sept 28–Oct 1, 2014, Opatija, Croatia: 117.
 
Nakano H., Kizaki H., Sakaguchi G. (1994): Multiplication of Clostridium botulinum in dead honey-bees and bee pupae, a likely source of heavy contamination of honey. International Journal of Food Microbiology, 21: 247–252. https://doi.org/10.1016/0168-1605(94)90031-0
 
Nevas M., Hielm S., Lindström M., Koivulehto M., Horn H., Korkeala H. (2002): High prevalence of Clostridium botulinum types A and B in honey samples detected by polymerase chain reaction. International Journal of Food Microbiology, 72: 45–52. https://doi.org/10.1016/S0168-1605(01)00615-8
 
Nevas M., Lindström M., Hautamäki K., Puoskari S., Korkeala H. (2005): Prevalence and diversity of Clostridium botulinum types A, B, E and F in honey produced in the Nordic countries. International Journal of Food Microbiology, 105: 145–151. https://doi.org/10.1016/j.ijfoodmicro.2005.04.007
 
Nevas M., Lindström M., Hörman A., Keto-Timonen R., Korkeala H. (2006): Contamination routes of Clostridium botulinum in the honey production environment. Environmental Microbiology, 8: 1085–1094. https://doi.org/10.1111/j.1462-2920.2006.001000.x
 
Palacio A.M., Figini E.F., Ruffinengo S.R., Rodriguez E.M., del Hoyo M.L., Bedascarrasbure E.L. (2000): Changes in a population of Apis mellifera L. selected for hygienic behaviour and its relation to brood disease tolerance. Apidologie, 31: 471–478. https://doi.org/10.1051/apido:2000139
 
PN-88/A-77626 (1988): “Miód pszczeli”. Dziennik Norm i Miar nr 8. Warszawa, Polska, Wydawnictwo Normalizacyjne Alfa.
 
Roman A., Popiela-Pleban E., Kozak M. (2013): Factors influencing consumer behavior relating to the purchasing of honey. Part 1. The buying process and the level of consumption. Journal of Apicultural Science, 57: 159–172. https://doi.org/10.2478/jas-2013-0026
 
Różańska H. (2011): Microbiological quality of Polish honey. Bulletin of the Veterinary Institute in Pulawy, 55: 443–445.
 
Satorres S.E., Alcaraz L.E., Fernández R.A., Centorbi O.N. (1999): Isolation of Clostridium botulinum in medical plants. Anaerobe, 5: 173–175. https://doi.org/10.1006/anae.1999.0205
 
Semkiw P., Ochal J. (2012): Sektor pszczelarski w Polsce w 2012 roku. Instytut Ogrodnictwa Oddział Pszczelnictwa, Puławy. Available at: www.opisik.pulawy.pl/pdf/SP2012.pdf (accessed August 22, 2016)
 
Sobel J. (2005): Botulism. Clinical Infectious Diseases, 41: 1167–1173. https://doi.org/10.1086/444507
 
Spivak M., Downey D.L. (1998): Field Assays for Hygienic Behavior in Honey Bees (Hymenoptera: Apidae). Journal of Economic Entomology, 91: 64–70. https://doi.org/10.1093/jee/91.1.64
 
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