Anaerobic sporeformers and their significance with respect to milk and dairy products

International Journal of Food Microbiology

Volumn 197, Issue , 2015, Pages 77-87

  Doyle, Conor J ^a,b   Gleeson, David ^c   Jordan, Kieran ^a   Beresford, Tom P ^a   Ross, R Paul ^a,d   Fitzgerald, Gerald F ^b,d   Cotter, Paul D ^a,d  

^a TEAGASC FOOD RESEARCH CENTRE   (Ireland)

^b UNIVERSITY COLLEGE CORK   (Ireland)

^c ANIMAL AND GRASSLAND RESEARCH AND INNOVATION CENTRE   (Ireland)

^d UNIVERSITY COLLEGE CORK   (Ireland)

Author keywords

Botulism; Clostridium; Milk; Pathogens; Spoilage; Spores

Indexed keywords

BOTULINUM TOXIN; BOTULINUM TOXIN B; BUTYRIC ACID; CLOSTRIDIUM TOXIN; LACTIC ACID; SULFITE; YOGHURT;

ANAEROBIC BACTERIUM; ARTIFICIAL MILK; BACILLUS; BACTERIAL STRAIN; BOTULISM; CHEESE; CLOSTRIDIUM; CLOSTRIDIUM BOTULINUM; CLOSTRIDIUM PERFRINGENS; DAIRY PRODUCT; EPIDEMIOLOGICAL DATA; FARMING SYSTEM; FERMENTATION; FOOD CONTAMINATION; FOOD INDUSTRY; FOOD INTAKE; FOOD POISONING; GAS GANGRENE; GENUS; HUMAN; MILK; NONHUMAN; REVIEW; SPOROGENESIS; SULPHITE REDUCING CLOSTRIDIA; TAXONOMY; THERMOPHILIC BACTERIUM; ANIMAL; CLASSIFICATION; CLOSTRIDIUM INFECTIONS; DAIRYING; FOOD CONTROL; FOODBORNE DISEASES; MICROBIOLOGY; PHYSIOLOGY; PUBLIC HEALTH; STANDARDS; TRANSMISSION;

CLOSTRIDIA; CLOSTRIDIUM;

ANIMALS; CLOSTRIDIUM; CLOSTRIDIUM INFECTIONS; DAIRY PRODUCTS; DAIRYING; FOOD MICROBIOLOGY; FOODBORNE DISEASES; HUMANS; MILK; PUBLIC HEALTH;

EID: 84920915043     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.12.022     Document Type: Review

References (184)

1. Allison C., Macfarlane G.T. Regulation of protease production in Clostridium sporogenes. Appl. Environ. Microbiol. 1990, 56(11):3485-3490.
2. Andersson A., Rönner U., Granum P.E. What problems does the food industry have with the spore-forming pathogens Bacillus cereus and Clostridium perfringens?. Int. J. Food Microbiol. 1995, 28(2):145-155.
3. Anon Disease attributed to dairy products. Br. Med. J. 1982, 285(6355):1664.
4. Arias C., Oliete B., Seseña S., Jimenez L., Pérez-Guzmán M., Arias R. Importance of on-farm management practices on lactate-fermenting Clostridium spp. spore contamination of Manchega ewe milk: determination of risk factors and characterization of Clostridium population. Small Rumin. Res. 2013, 111(1):120-128.
5. Arnon S.S. Infant botulism. Annu. Rev. Med. 1980, 31(1):541-560.
6. Arnon S.S. Infant botulism. Textbook of Pediatric Infectious Diseases 1998, 1570-1577. WB Saunders Co, Philadelphia, Pa. 4th ed.
7. Arnon S.S., Midura T.F., Damus K., Thompson B., Wood R.M., Chin J. Honey and other environmental risk factors for infant botulism. J. Pediatr. 1979, 94(2):331-336.
8. Aureli P., Franciosa G. Clostridium spp. Encycl. Dairy Sci. 2002, 1:456-463.
9. Aureli P., Franciosa G., Pourshaban M. Foodborne botulism in Italy. Lancet 1996, 348(9041):1594.
10. Balslev T., Østergaard E., Madsen I., Wandall D. Infant botulism. The first culture-confirmed Danish case. Neuropediatrics 1997, 28(05):287-289.
11. Barash J.R., Arnon S.S. Dual toxin-producing strain of Clostridium botulinum type Bf isolated from a California patient with infant botulism. J. Clin. Microbiol. 2004, 42(4):1713-1715.
12. Barash J.R., Hsia J.K., Arnon S.S. Presence of soil-dwelling clostridia in commercial powdered infant formulas. J. Pediatr. 2010, 156(3):402-408.
13. Barnes C., Gerstle J.T., Freedman M.H., Carcao M.D. Clostridium septicum myonecrosis in congenital neutropenia. Pediatrics 2004, 114(6):e757-e760.
14. Bergère J., Gouet P., Hermier J., Mocquot G. Les Clostridium du groupe butyrique dans les produits laitiers. Ann. Inst. Pasteur Lille 1968, 19:41-54.
15. Billon J., Guerin J., Sebald M. Toxinogenesis of Clostridium botulinum type B during maturation of soft cheese. Lait 1980, 60(597):329-342.
16. Blocher J., Busta F. Bacterial spore resistance to acid. Food Technol. 1983, 37.
17. Brett M., McLauchlin J., Harris A., O'Brien S., Black N., Forsyth R., Roberts D., Bolton F. A case of infant botulism with a possible link to infant formula milk powder: evidence for the presence of more than one strain of Clostridium botulinum in clinical specimens and food. J. Med. Microbiol. 2005, 54(8):769-776.
18. Brook I. Clostridial infection in children. J. Med. Microbiol. 1995, 42(2):78-82.
19. Brook I. Infant botulism. J. Perinatol. 2007, 27(3):175-180.
20. Brynestad S., Granum P.E. Clostridium perfringens and foodborne infections. Int. J. Food Microbiol. 2002, 74(3):195-202.
21. Burgess S.A., Lindsay D., Flint S.H. Thermophilic bacilli and their importance in dairy processing. Int. J. Food Microbiol. 2010, 144(2):215-225.
22. CAC Code of hygienic practice for powdered infant formulae for infants and young children CAC/RCP C. A. Commission. http://www.codexalimentarius.org/input/download/standards/11026/CXP_066e.pdf.
23. Campbell L.L., Postgate J.R. Classification of the spore-forming sulfate-reducing bacteria. Bacteriol. Rev. 1965, 29(3):359.
24. Cano R.J., Borucki M.K. Revival and identification of bacterial spores in 25-to 40-million-year-old Dominican amber. Science 1995, 268(5213):1060-1064.
25. Carlin F., Broussolle V., Perelle S., Litman S., Fach P. Prevalence of Clostridium botulinum in food raw materials used in REPFEDs manufactured in France. Int. J. Food Microbiol. 2004, 91(2):141-145.
26. Cato E., George W.L., Finegold S. Genus Clostridium. Bergey's Manual of Systematic Bacteriology 1986, 2:1141-1200.
27. Cavalcanti M.T.H., Porto T., Porto A.L.F., Brandi I.V., Lima Filho J.L.D., Pessoa Junior A. Large scale purification of Clostridium perfringens toxins: a review. Rev. Bras. Ciências Farm. 2004, 40(2):151-164.
28. Charlebois A., Jacques M., Archambault M. Biofilm formation of Clostridium perfringens and its exposure to low-dose antimicrobials. Front. Microbiol. 2014, 5.
29. Chen L., Daniel R.M., Coolbear T. Detection and impact of protease and lipase activities in milk and milk powders. Int. Dairy J. 2003, 13(4):255-275.
30. Christiansson A., Bertilsson J., Svensson B. Bacillus cereus spores in raw milk: factors affecting the contamination of milk during the grazing period. J. Dairy Sci. 1999, 82(2):305-314.
31. Cocolin L., Innocente N., Biasutti M., Comi G. The late blowing in cheese: a new molecular approach based on PCR and DGGE to study the microbial ecology of the alteration process. Int. J. Food Microbiol. 2004, 90(1):83-91.
32. Cogan T. A review of heat resistant lipases and proteinases and the quality of dairy products. Irish J. Food Sci. Technol. 1977, 95-105.
33. Collins M., Lawson P., Willems A., Cordoba J., Fernandez-Garayzabal J., Garcia P., Cai J., Hippe H., Farrow J. The phylogeny of the genus Clostridium: proposal of five new genera and eleven new species combinations. Int. J. Syst. Bacteriol. 1994, 44(4):812-826.
34. Collins-Thompson D.L., Wood D.S. Control in dairy products. Ecology and Control in Food 1992, 261-277. Marcel Dekker, New York.
35. Council U.D.E. US Dairy Export Council 2013.
36. Cousin M. Presence and activity of psychrotrophic microorganisms in milk and dairy products: a review. J. Food Prot. (USA) 1982, 45:172-207.
37. Cox W. Subject: bitty cream and related problems: problems associated with bacterial spores in heat-treated milk and dairy products. Int. J. Dairy Technol. 1975, 28(2):59-68.
38. Cremonesi P., Vanoni L., Silvetti T., Morandi S., Brasca M. Identification of Clostridium beijerinckii, Cl. butyricum, Cl. sporogenes, Cl. tyrobutyricum isolated from silage, raw milk and hard cheese by a multiplex PCR assay. J. Dairy Res. 2012, 79(03):318-323.
39. Crielly E., Logan N., Anderton A. Studies on the Bacillus flora of milk and milk products. J. Appl. Bacteriol. 1994, 77(3):256-263.
40. Critchley E., Hayes P., Isaacs P. Outbreak of botulism in north west England and Wales, June, 1989. Lancet 1989, 334(8667):849-853.
41. Derman Y., Lindström M., Selby K., Korkeala H. Growth of group II Clostridium botulinum strains at extreme temperatures. J. Food Prot. 2011, 74(11):1797-1804.
42. Dhaked R.K., Singh M.K., Singh P., Gupta P. Botulinum toxin: bioweapon & magic drug. Indian J. Med. Res. 2010, 132(5):489.
43. Dodds K.L. Clostridium botulinum in foods. Clostridium botulinum: Ecology and Control in Foods 1993, 53-68.
44. Donnelly L.S., Busta F.F. Heat resistance of Desulfotomaculum nigrificans spores in soy protein infant formula preparations. Appl. Environ. Microbiol. 1980, 40:721-725.
45. Dover N., Barash J.R., Hill K.K., Xie G., Arnon S.S. Molecular characterization of a novel botulinum neurotoxin type H gene. J. Infect. Dis. 2014, 209(2):192-202.
46. Doyle M.E., Glass K. Spores of Clostridium botulinum in Dried Dairy Products 2013.
47. Durre P. From Pandora's box to cornucopia: clostridia-a historical perspective. Clostridia-Biotechnology and Medical Applications 2001, 1-17. Wiley-VCH, New York, NY.
48. Eklund M., Wieler D., Poysky F. Outgrowth and toxin production of nonproteolytic type B Clostridium botulinum at 3.3 to 5.6°C. J. Bacteriol. 1967, 93(4):1461.
49. Elmoslemany A., Keefe G., Dohoo I., Jayarao B. Risk factors for bacteriological quality of bulk tank milk in Prince Edward Island dairy herds. Part 2: bacteria count-specific risk factors. J. Dairy Sci. 2009, 92(6):2644-2652.
50. FAO/WHO Enterobacter sakazakii and other microorganisms in powdered infant formula: meeting report. Microbiological Risk Assessment Series 2004, 6. (from ftp://ftp.fao.org/docrep/fao/007/y5502e/y5502e00.pdf).
51. Federation R. Federal Law on Technical Regulations for Milk and Milk Products 2008, Russian Federation, (No 88-FZ).
52. Fenicia L., Da Dalt L., Anniballi F., Franciosa G., Zanconato S., Aureli P. A case of infant botulism due to neurotoxigenic Clostridium butyricum type E associated with Clostridium difficile colitis. Eur. J. Clin. Microbiol. Infect. Dis. 2002, 21(10):736-738.
53. Fischer M., Zhu S., de Ree E. Culture media for the detection and enumeration of clostridia in food. Handbook of Culture Media for Food and Water Microbiology 2012, 66.
54. Fisher D.J., Miyamoto K., Harrison B., Akimoto S., Sarker M.R., McClane B.A. Association of beta2 toxin production with Clostridium perfringens type A human gastrointestinal disease isolates carrying a plasmid enterotoxin gene. Mol. Microbiol. 2005, 56(3):747-762.
55. Flint S., Bremer P., Brooks J. Biofilms in dairy manufacturing plant-description, current concerns and methods of control. Biofouling 1997, 11(1):81-97.
56. Franciosa G., Pourshaban M., Gianfranceschi M., Gattuso A., Fenicia L., Ferrini A.M., Mannoni V., De Luca G., Aureli P. Clostridium botulinum spores and toxin in mascarpone cheese and other milk products. J. Food Prot. 1999, 62(8):867-871.
57. Fritze D. Taxonomy of the genus Bacillus and related genera: the aerobic endospore-forming bacteria. Phytopathology 2004, 94(11):1245-1248.
58. Fuchs A.-R., Bonde G. The nutritional requirements of Clostridium perfringens. J. Gen. Microbiol. 1957, 16(2):317-329.
59. Garde S., Arias R., Gaya P., Nuñez M. Occurrence of Clostridium spp. in ovine milk and Manchego cheese with late blowing defect: identification and characterization of isolates. Int. Dairy J. 2011, 21(4):272-278.
60. Garde S., Gaya P., Arias R., Nuñez M. Enhanced PFGE protocol to study the genomic diversity of Clostridium spp. isolated from Manchego cheeses with late blowing defect. Food Control 2012, 28(2):392-399.
61. Gibbs B., Freame B. Methods for the recovery of clostridia from foods. J. Appl. Microbiol. 1965, 28(1):95-111.
62. Gibert M., Jolivet-Renaud C., Popoff M.R. Beta2 toxin, a novel toxin produced by Clostridium perfringens. Gene 1997, 203(1):65-73.
63. Gimenez D.F., Ciccarelli A.S. New strains of Clostridium botulinum subtype Af. Zentralbl. Bakteriol. Orig. A 1978, 240(2):215-220.
64. Gkiourtzidis K., Frey J., Bourtzi-Hatzopoulou E., Iliadis N., Sarris K. PCR detection and prevalence of α-, β-, β2-, ε-, ι-and enterotoxin genes in Clostridium perfringens isolated from lambs with clostridial dysentery. Vet. Microbiol. 2001, 82(1):39-43.
65. Gleeson D., O'Connell A., Jordan K. Review of potential sources and control of thermoduric bacteria in bulk-tank milk. Irish J. Agric. Food Res. 2013, 52(2):217-227.
66. Goudkov A., Sharpe M.E. Clostridia in dairying. J. Appl. Microbiol. 1965, 28(1):63-73.
67. Graham A., Mason D., Maxwell F., Peck M. Effect of pH and NaCl on growth from spores of non-proteolytic Clostridium botulinum at chill temperature. Lett. Appl. Microbiol. 1997, 24(2):95-100.
68. Griffiths M., Phillips J., West I., Muir D. The effect of extended low-temperature storage of raw milk on the quality of pasteurized and UHT milk. Food Microbiol. 1988, 5(2):75-87.
69. Gui L., Subramony C., Fratkin J., Hughson M.D. Fatal enteritis necroticans (pigbel) in a diabetic adult. Mod. Pathol. 2002, 15(1):66-70.
70. Hall J., McCroskey L., Pincomb B., Hatheway C. Isolation of an organism resembling Clostridium barati which produces type F botulinal toxin from an infant with botulism. J. Clin. Microbiol. 1985, 21(4):654-655.
71. Hanson M., Wendorff W., Houck K. Effect of heat treatment of milk on activation of Bacillus spores. J. Food Prot. 2005, 68(7):1484-1486.
72. Hassan K.A., Elbourne L.D., Tetu S.G., Melville S.B., Rood J.I., Paulsen I.T. Genomic analyses of Clostridium perfringens isolates from five toxinotypes. Res. Microbiol. 2014, 10.1016/j.resmic.2014.10.003.
73. Hatheway C.L. Toxigenic clostridia. Clin. Microbiol. Rev. 1990, 3(1):66-98.
74. Hatheway C.L., McCroskey L.M. Examination of feces and serum for diagnosis of infant botulism in 336 patients. J. Clin. Microbiol. 1987, 25(12):2334-2338.
75. Hippe H., Andreesen J.R., Gottschalk G. The genus Clostridium - nonmedical. The Prokaryotes 1992, vol. 2:1800-1866. 2nd edn.
76. Huck J., Sonnen M., Boor K. Tracking heat-resistant, cold-thriving fluid milk spoilage bacteria from farm to packaged product. J. Dairy Sci. 2008, 91(3):1218-1228.
77. Hussong R., Hammer B. Anaerobic bacteria in dairy products: I. Numbers of spores of anaerobic bacteria in milk and cream. J. Bacteriol. 1930, 19(2):89.
78. ICMSF Usefulness of Testing for Clostridium botulinum in Powdered Infant Formula and Dairy-based Ingredients for Infant Formula 2014, ICMSF.
79. Jabbari A., Tekyei F., Esmaeilizad M., Langroudi R.Pilehchian Occurrence of Beta2 toxigenic Clostridium perfringens isolates with different toxin types in Iran. Arch. Razi 2012, 67(2):133-137.
80. Jayarao B., Pillai S., Sawant A., Wolfgang D., Hegde N. Guidelines for monitoring bulk tank milk somatic cell and bacterial counts. J. Dairy Sci. 2004, 87(10):3561-3573.
81. Johnson E.A., Tepp W.H., Bradshaw M., Gilbert R.J., Cook P.E., McIntosh E.D.G. Characterization of Clostridium botulinum strains associated with an infant botulism case in the United Kingdom. J. Clin. Microbiol. 2005, 43(6):2602-2607.
82. Josephson K., Gerba C., Pepper I. Polymerase chain reaction detection of nonviable bacterial pathogens. Appl. Environ. Microbiol. 1993, 59(10):3513-3515.
83. Julien M.-C., Dion P., Lafreniere C., Antoun H., Drouin P. Sources of clostridia in raw milk on farms. Appl. Environ. Microbiol. 2008, 74(20):6348-6357.
84. Juneja V., Thippareddi H. Inhibitory effects of organic acid salts on growth of Clostridium perfringens from spore inocula during chilling of marinated ground turkey breast. Int. J. Food Microbiol. 2004, 93(2):155-163.
85. Kakinuma H., Maruyama H., Takahashi H., Yamakawa K., Nakamura S. The first case of type B infant botulism in Japan. Pediatr. Int. 1996, 38(5):541-543.
86. Klijn N., Nieuwenhof F., Hoolwerf J.D., Van Der Waals C., Weerkamp A.H. Identification of Clostridium tyrobutyricum as the causative agent of late blowing in cheese by species-specific PCR amplification. Appl. Environ. Microbiol. 1995, 61(8):2919-2924.
87. Kosikowski F., Fox P. Low heat, hydrogen peroxide, and bactofugation treatments of milk to control coliforms in cheddar cheese. J. Dairy Sci. 1968, 51(7):1018-1022.
88. Kramer J.M., Gilbert R.J. Bacillus cereus and other Bacillus species. Foodborne Bact. Pathog. 1989, 19:21-70.
89. Lahti P., Heikinheimo A., Johansson T., Korkeala H. Clostridium perfringens type A strains carrying a plasmid-borne enterotoxin gene (genotype IS1151-cpe or IS1470-like-cpe) as a common cause of food poisoning. J. Clin. Microbiol. 2008, 46(1):371-373.
90. Le Bourhis A.-G., Doré J., Carlier J.-P., Chamba J.-F., Popoff M.-R., Tholozan J.-L. Contribution of C. beijerinckii and C. sporogenes in association with C. tyrobutyricum to the butyric fermentation in Emmental type cheese. Int. J. Food Microbiol. 2007, 113(2):154-163.
91. Li J., McClane B.A. Comparative effects of osmotic, sodium nitrite-induced, and pH-induced stress on growth and survival of Clostridium perfringens type A isolates carrying chromosomal or plasmid-borne enterotoxin genes. Appl. Environ. Microbiol. 2006, 72(12):7620-7625.
92. Li J., McClane B.A. Further comparison of temperature effects on growth and survival of Clostridium perfringens type A isolates carrying a chromosomal or plasmid-borne enterotoxin gene. Appl. Environ. Microbiol. 2006, 72(7):4561-4568.
93. Li J., Adams V., Bannam T.L., Miyamoto K., Garcia J.P., Uzal F.A., Rood J.I., McClane B.A. Toxin plasmids of Clostridium perfringens. Microbiol. Mol. Biol. Rev. 2013, 77(2):208-233.
94. Lindström M., Keto R., Markkula A., Nevas M., Hielm S., Korkeala H. Multiplex PCR assay for detection and identification of Clostridium botulinum types A, B, E, and F in food and fecal material. Appl. Environ. Microbiol. 2001, 67(12):5694-5699.
95. Lindström M., Heikinheimo A., Lahti P., Korkeala H. Novel insights into the epidemiology of Clostridium perfringens type A food poisoning. Food Microbiol. 2011, 28(2):192-198.
96. López-Enríquez L., Rodríguez-Lázaro D., Hernández M. Quantitative detection of Clostridium tyrobutyricum in milk by real-time PCR. Appl. Environ. Microbiol. 2007, 73(11):3747-3751.
97. Ludwig W., Schleifer K.-H., Whitman W.B. Revised road map to the phylum Firmicutes. Bergey's Manual® of Systematic Bacteriology 2009, 1-13. Springer.
98. Magnusson M., Christiansson A., Svensson B., Kolstrup C. Effect of different premilking manual teat-cleaning methods on bacterial spores in milk. J. Dairy Sci. 2006, 89(10):3866-3875.
99. Magnusson M., Christiansson A., Svensson B. Bacillus cereus spores during housing of dairy cows: factors affecting contamination of raw milk. J. Dairy Sci. 2007, 90(6):2745-2754.
100. Mahant N., Clouston P., Lorentz I. The current use of botulinum toxin. J. Clin. Neurosci. 2000, 7(5):389-394.
101. Manafi M. New developments in chromogenic and fluorogenic culture media. Int. J. Food Microbiol. 2000, 60(2):205-218.
102. Martin S. Clostridium botulinum type D intoxication in a dairy herd in Ontario. Can. Vet. J. 2003, 44(6):493.
103. May M., Coulthard M., Delbridge G., McEniery J., Burke C., Nissen M. Difficulties in the diagnosis and management of infant botulism. J. Paediatr. Child Health 2002, 38(4):425-426. (author reply 426-427).
104. McAuley C.M., McMillan K., Moore S.C., Fegan N., Fox E.M. Prevalence and characterization of foodborne pathogens from Australian dairy farm environments. J. Dairy Sci. 2014, 97(12):7402-7412.
105. McDonnell A., Holmes L. Haemoglobinuria due to Clostridium perfringens type A mastitis in a ewe. Br. Vet. J. 1990, 146(4):380-381.
106. McKinnon C.H., Pettipher G.L. A survey of sources of heat-resistant bacteria in milk with particular reference to psychrotrophic spore-forming bacteria. J. Dairy Res. 1983, 50(02):163-170.
107. Mead G. The use of sulphite-containing media in the isolation of Clostridium welchii. J. Appl. Microbiol. 1969, 32(3):358-361.
108. Medini D., Donati C., Tettelin H., Masignani V., Rappuoli R. The microbial pan-genome. Curr. Opin. Genet. Dev. 2005, 15(6):589-594.
109. Melin M., Wiktorsson H., Christiansson A., McLean J., Sinclair M., West B. Teat cleaning efficiency before milking in DeLaval VMSTM versus conventional manual cleaning, using Clostridium tyrobutyricum spores as marker. First North American Conference on Robotic Milking, Toronto, Canada, 20-22 March, 2002 2002, Wageningen Pers.
110. Meyer K., Eddie B. Perspectives concerning botulism. Z. Hyg. Infekt. 1951, 133(4):255-263.
111. Minamisawa K., Nishioka K., Miyaki T., Ye B., Miyamoto T., You M., Saito A., Saito M., Barraquio W.L., Teaumroong N. Anaerobic nitrogen-fixing consortia consisting of clostridia isolated from gramineous plants. Appl. Environ. Microbiol. 2004, 70(5):3096-3102.
112. Moschonas G., Bolton D., Sheridan J., McDowell D. The effect of storage temperature and inoculum level on the time of onset of 'blown pack' spoilage. J. Appl. Microbiol. 2010, 108(2):532-539.
113. Murphy S., Boor K. Trouble-shooting sources and causes of high bacteria counts in raw milk. Dairy, Food Environ. Sanit. 2000, 20(8):606-611.
114. Murphy P.M., Lynch D., Kelly P.M. Growth of thermophilic spore forming bacilli in milk during the manufacture of low heat powders. Int. J. Dairy Technol. 1999, 52(2):45-50.
115. 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(1):147-154.
116. Nocker A., Sossa-Fernandez P., Burr M.D., Camper A.K. Use of propidium monoazide for live/dead distinction in microbial ecology. Appl. Environ. Microbiol. 2007, 73(16):5111-5117.
117. Oh M.-H., Ham J.-S., Cox J.M. Diversity and toxigenicity among members of the Bacillus cereus group. Int. J. Food Microbiol. 2012, 152(1):1-8.
118. O'Mahony M., Mitchell E., Gilbert R., Hutchinson D., Begg N., Rodhouse J., Morris J. An outbreak of foodborne botulism associated with contaminated hazelnut yoghurt. Epidemiol. Infect. 1990, 104(03):389-395.
119. Osman K., El-Enbaawy M., Ezzeldeen N., Hussein H. Mastitis in dairy buffalo and cattle in Egypt due to Clostridium perfringens: prevalence, incidence, risk factors and costs. Rev. Sci. Tech. 2009, 28(3):975-986.
120. Pahlow G., Muck R., Driehuis F., Oude Elferink S., Spoelstra S., Buxton D., RE M. Silage Science and Technology 2003.
121. Pankey J. Premilking udder hygiene. J. Dairy Sci. 1989, 72(5):1308-1312.
122. Peck M.W., Plowman J., Aldus C.F., Wyatt G.M., Izurieta W.P., Stringer S.C., Barker G.C. Development and application of a new method for specific and sensitive enumeration of spores of nonproteolytic Clostridium botulinum types B, E, and F in foods and food materials. Appl. Environ. Microbiol. 2010, 76(19):6607-6614.
123. Phillips J., Griffiths M. Factors contributing to the seasonal variation of Bacillus spp. in pasteurized dairy products. J. Appl. Bacteriol. 1986, 61(4):275-285.
124. Pickett J., Berg B., Chaplin E., Brunstetter-Shafer M.-A. Syndrome of botulism in infancy: clinical and electrophysiologic study. N. Engl. J. Med. 1976, 295(14):770-772.
125. Prevost S., Cayol J.-L., Zuber F., Tholozan J.-L., Remize F. Characterization of clostridial species and sulfite-reducing anaerobes isolated from foie gras with respect to microbial quality and safety. Food Control 2013, 32(1):222-227.
126. Prevot A. Recherches sur la réduction des sulfates et des sulfites minéraux par les bactéries anaérobies. Annales de L Institut Pasteur 1948, Masson Editeur, 120 Blvd Saint-Germain, 75280 Paris 06, France.
127. Prévot V., Tweepenninckx F., Van Nerom E., Linden A., Kimpe A. Optimization of polymerase chain reaction for detection of Clostridium botulinum type C and D in bovine samples. Zoonoses Public Health 2007, 54(8):320-327.
128. Princewell T., Agba M. Examination of bovine faeces for the isolation and identification of Clostridium species. J. Appl. Microbiol. 1982, 52(1):97-102.
129. Rammer C. Quality of grass silage infected with spores of Clostridium tyrobutyricum. Grass Forage Sci. 1996, 51(1):88-95.
130. Ranieri M., Huck J., Sonnen M., Barbano D., Boor K. High temperature, short time pasteurization temperatures inversely affect bacterial numbers during refrigerated storage of pasteurized fluid milk. J. Dairy Sci. 2009, 92(10):4823-4832.
131. Ranieri M.L., Ivy R.A., Mitchell W.R., Call E., Masiello S.N., Wiedmann M., Boor K.J. Real-time PCR detection of Paenibacillus spp. in raw milk to predict shelf life performance of pasteurized fluid milk products. Appl. Environ. Microbiol. 2012, 78(16):5855-5863.
132. Reinemann D.J., Wolters G., Billon P., Lind O., Rasmussen M.D. Review of practices for cleaning and sanitation of milking machines 2003, 3-18. Bulletin-International Dairy Federation.
133. Ribeiro M., Lara G., Bicudo S., Souza A., Salerno T., Siqueira A., Geraldo J. An unusual gangrenous goat mastitis caused by Staphylococcus aureus, Clostridium perfringens and Escherichia coli co-infection. Arq. Bras. Med. Vet. Zootec. 2007, 59(3):810-812.
134. Roberts T., Hitchins A. Resistance of spores. The Bacterial Spore 1969, 2.
135. Robinson A., Manser P. Mastitis in a heifer caused by Clostridium welchii, type "A". Vet. Rec. 1977, 101(2):37.
136. Rogers P., Gottschalk G. Biochemistry and regulation of acid and solvent production in clostridia. Biotechnology Series 1993, 25-50.
137. Ronimus R.S., Parker L.E., Turner N., Poudel S., Rückert A., Morgan H.W. A RAPD-based comparison of thermophilic bacilli from milk powders. Int. J. Food Microbiol. 2003, 85(1):45-61.
138. Ronimus R.S., Rueckert A., Morgan H.W. Survival of thermophilic spore-forming bacteria in a 90+ year old milk powder from Ernest Shackelton's Cape Royds Hut in Antarctica. J. Dairy Res. 2006, 73(2):235-243.
139. Russell A. Bacterial spores and chemical sporicidal agents. Clin. Microbiol. Rev. 1990, 3(2):99-119.
140. Rysstad G., Kolstad J. Extended shelf life milk-advances in technology. Int. J. Dairy Technol. 2006, 59(2):85-96.
141. Santos-Buelga J.A., Collins M.D., East A.K. Characterization of the genes encoding the botulinum neurotoxin complex in a strain of Clostridium botulinum producing type B and F neurotoxins. Curr. Microbiol. 1998, 37(5):312-318.
142. Sarker M.R., Shivers R.P., Sparks S.G., Juneja V.K., McClane B.A. Comparative experiments to examine the effects of heating on vegetative cells and spores of Clostridium perfringens isolates carrying plasmid genes versus chromosomal enterotoxin genes. Appl. Environ. Microbiol. 2000, 66(8):3234-3240.
143. Savoy D.G.G., Font D.V.G., Pesce D.R.H.A., Oliver G. Isolation and identification of anaerobic contaminants from a machine for producing processed cheese. Rev. Argent. Microbiol. 1981, 14(2):105-110.
144. Scallan E., Hoekstra R.M., Angulo F.J., Tauxe R.V., Widdowson M.-A., Roy S.L., Jones J.L., Griffin P.M. Foodborne illness acquired in the United States-major pathogens. Emerg. Infect. Dis. 2011, 17(1).
145. Schmidt-Dannert C., Rua M.L., Schmid R.D. Two novel lipases from thermophile Bacillus thermocatenulatus: screening, purification, cloning, overexpression, and properties. Methods Enzymol. 1997, 284:194-220.
146. Schreiner D., Ruegg P. Relationship between udder and leg hygiene scores and subclinical mastitis. J. Dairy Sci. 2003, 86(11):3460-3465.
147. Sebald M., Jouglard J., Gilles G. Type B botulism in man due to cheese (author's transl). Ann. Microbiol (Paris) 1974, 125A(3):349-357.
148. Shapiro R.L., Hatheway C., Swerdlow D.L. Botulism in the United States: a clinical and epidemiologic review. Ann. Intern. Med. 1998, 129(3):221-228.
149. Silva A.R., Paulo E.N., Sant'Ana A.S., Chaves R.D., Massaguer P.R. Involvement of Clostridium gasigenes and C. algidicarnis in 'blown pack' spoilage of Brazilian vacuum-packed beef. Int. J. Food Microbiol. 2011, 148(3):156-163.
150. Skanderby M., Westergaard V., Partridge A., Muir D. 5 dried milk products. Dairy Powders and Concentrated Products 2009, 180.
151. SkjelkvÅLe R., Uemura T. Experimental diarrhoea in human volunteers following oral administration of Clostridium perfringens enterotoxin. J. Appl. Bacteriol. 1977, 43(2):281-286.
152. Slaghuis B.A., Te Giffel M.C., Beumer R.R., André G. Effect of pasturing on the incidence of Bacillus cereus spores in raw milk. Int. Dairy J. 1997, 7(4):201-205.
153. Smokvina T., Wels M., Polka J., Chervaux C., Brisse S., Boekhorst J., van Hylckama Vlieg J.E., Siezen R.J. Lactobacillus paracasei comparative genomics: towards species pan-genome definition and exploitation of diversity. PLoS One 2013, 8(7):e68731.
154. Sobel J. Botulism. Clin. Infect. Dis. 2005, 41(8):1167-1173.
155. Song Y., Liu C., Finegold S.M. Real-time PCR quantitation of clostridia in feces of autistic children. Appl. Environ. Microbiol. 2004, 70(11):6459-6465.
156. Sørhaug T., Stepaniak L. Psychrotrophs and their enzymes in milk and dairy products: quality aspects. Trends Food Sci. Technol. 1997, 8(2):35-41.
157. Stadhouders J., Jørgensen K. Prevention of the contamination of raw milk by a hygienic milk production. Bull. Int. Dairy Fed. 1990, (251):32-36.
158. Standards I.O.O. Microbiology of food and animal feeding stuffs - horizontal method for the enumeration of sulfite-reducing bacteria growing under anaerobic conditions. ISO 2003 2003.
159. Standards I.O.O. Microbiology of food and animal feeding stuffs - horizontal method for the enumeration of Clostridium perfringens - colony-count technique. ISO 2004 2004.
160. Stiles B.G., Barth G., Barth H., Popoff M.R. Clostridium perfringens epsilon toxin: a malevolent molecule for animals and man?. Toxins 2013, 5(11):2138-2160.
161. Su Y.-C., Ingham S.C. Influence of milk centrifugation, brining and ripening conditions in preventing gas formation by Clostridium spp. in Gouda cheese. Int. J. Food Microbiol. 2000, 54(3):147-154.
162. Suen J.C., Hatheway C.L., Steigerwalt A.G., Brenner D. Genetic confirmation of identities of neurotoxigenic Clostridium baratii and Clostridium butyricum implicated as agents of infant botulism. J. Clin. Microbiol. 1988, 26(10):2191-2192.
163. Sugiyama H. Studies on factors affecting the heat resistance of spores of Clostridium botulinum. J. Bacteriol. 1951, 62(1):81.
164. Te Giffel M., Beumer R., Slaghuis B., Rombouts F. Occurrence and characterization of (psychrotrophic) Bacillus cereus on farms in the Netherlands. Ned. Melk Zuiveltijdschrift 1995, 49(2-3):125-138.
165. Te Giffel M., Beumer R., Granum P., Rombouts F. Isolation and characterisation of Bacillus cereus from pasteurised milk in household refrigerators in the Netherlands. Int. J. Food Microbiol. 1997, 34(3):307-318.
166. Te Giffel M., Wagendorp A., Herrewegh A., Driehuis F. Bacterial spores in silage and raw milk. Antonie Van Leeuwenhoek 2002, 81(1-4):625-630.
167. Tettelin H., Masignani V., Cieslewicz M.J., Donati C., Medini D., Ward N.L., Angiuoli S.V., Crabtree J., Jones A.L., Durkin A.S. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial "pan-genome". Proc. Natl. Acad. Sci. U. S. A. 2005, 102(39):13950-13955.
168. Ting P.T., Freiman A. The story of Clostridium botulinum: from food poisoning to Botox. Clin. Med. 2004, 4(3):258-261.
169. Uzal F.A., Freedman J.C., Shrestha A., Theoret J.R., Garcia J., Awad M.M., Adams V., Moore R.J., Rood J.I., McClane B.A. Towards an understanding of the role of Clostridium perfringens toxins in human and animal disease. Future Microbiol 2014, 9(3):361-377.
170. Velthuis A., van Asseldonk M. Association between product quality control and process quality control of bulk milk. 9th Wageningen International Conference on Chain and Network Management 2010, (Wageningen, The Netherlands).
171. Vissers M., Driehuis F., Te Giffel M., De Jong P., Lankveld J. Improving farm management by modeling the contamination of farm tank milk with butyric acid bacteria. J. Dairy Sci. 2006, 89(3):850-858.
172. Vissers M., Driehuis F., Te Giffel M., De Jong P., Lankveld J. Concentrations of butyric acid bacteria spores in silage and relationships with aerobic deterioration. J. Dairy Sci. 2007, 90(2):928-936.
173. Vissers M., Driehuis F., Te Giffel M., De Jong P., Lankveld J. Minimizing the level of butyric acid bacteria spores in farm tank milk. J. Dairy Sci. 2007, 90(7):3278-3285.
174. Vissers M., Te Giffel M., Driehuis F., De Jong P., Lankveld J. Minimizing the level of Bacillus cereus spores in farm tank milk. J. Dairy Sci. 2007, 90(7):3286-3293.
175. Waes G. Aerobic mesophilic spores in raw milk. Milchwissenschaft (Germany, FR) 1976, (31):521-525.
176. Walstra P., Walstra P., Wouters J.T., Geurts T.J. Dairy Science and Technology 2010, CRC Press.
177. Weenk G., Fitzmaurice E., Mossel D. Selective enumeration of spores of Clostridium species in dried foods. J. Appl. Microbiol. 1991, 70(2):135-143.
178. Weenk G., Van den Brink J., Struijk C., Mossel D. Modified methods for the enumeration of spores of mesophilic Clostridium species in dried foods. Int. J. Food Microbiol. 1995, 27(2):185-200.
179. Wiegel J., Tanner R., Rainey F.A. An introduction to the family Clostridiaceae. The Prokaryotes 2006, 654-678. Springer.
180. Wilson W.J., Blair E.M.M.V. The application of a sulphite-glucose-iron agar medium to the quantitative estimation of B. welchii and other reducing bacteria in water supplies. The Journal of Pathology and Bacteriology 1924, 27(1):119-121.
181. Xiao Y., Wagendorp A., Abee T., Wells-Bennik M.H. Differential outgrowth potential of Clostridium perfringens food borne isolates with various cpe-genotypes in vacuum-packed ground beef during storage at 12°C. Int. J. Food Microbiol. 2014, 194:40-45.
182. Xu D., CÔté J.-C. Phylogenetic relationships between Bacillus species and related genera inferred from comparison of 3' end 16S rDNA and 5' end 16S-23S ITS nucleotide sequences. Int. J. Syst. Evol. Microbiol. 2003, 53(3):695-704.
183. Yan R.-T., Zhu C.-X., Golemboski C., Chen J.-S. Expression of solvent-forming enzymes and onset of solvent production in batch cultures of Clostridium beijerinckii ("Clostridium butylicum"). Appl. Environ. Microbiol. 1988, 54(3):642-648.
184. Yutin N., Galperin M.Y. A genomic update on clostridial phylogeny: Gram-negative spore formers and other misplaced clostridia. Environ. Microbiol. 2013, 15(10):2631-2641.