Bacillus cereus

Bacillus cereus
B. cereus colonies on a sheep-blood agar plate
Scientific classification
Domain: Bacteria
Phylum: Firmicutes
Class: Bacilli
Order: Bacillales
Family: Bacillaceae
Genus: Bacillus
Species: B. cereus
Binomial name
Bacillus cereus
Frankland & Frankland 1887
Electron micrograph of Bacillus cereus

Bacillus cereus is a Gram-positive, rod-shaped, aerobic, motile, beta hemolytic bacterium commonly found in soil and food. Some strains are harmful to humans and cause foodborne illness, while other strains can be beneficial as probiotics for animals.[1]. It is the cause of "fried rice syndrome", as the bacteria are classically contracted from fried rice dishes that have been sitting at room temperature for hours (such as at a buffet).[2] B. cereus bacteria are facultative anaerobes, and like other members of the genus Bacillus, can produce protective endospores. Its virulence factors include cereolysin and phospholipase C.

It was from this species that two new enzymes, named AlkC and AlkD, which are involved in DNA repair, were discovered in 2006.[3]

History

Colonies of Bacillus cereus were originally isolated from an agar plate left exposed to the air in a cow shed.[4] In the 2010s, examination of warning letters issued by the US Food and Drug Administration issued to pharmaceutical manufacturing facilities addressing facility microbial contamination revealed that the most common contaminant was B. cereus.[5]

Ecology

B. cereus competes with other microorganisms such as Salmonella and Campylobacter in the gut, so its presence reduces the numbers of those microorganisms. In food animals such as chickens,[6] rabbits[7] and pigs,[8] some harmless strains of B. cereus are used as a probiotic feed additive to reduce Salmonella in the intestines and cecum. This improves the animals' growth as well as food safety for humans who eat their meat.

Bacillus cereus and other members of Bacillus are not easily killed by alcohol; in fact, they have been known to colonize distilled liquors and alcohol-soaked swabs and pads in numbers sufficient to cause infection.[9][10]

Some strains of B. cereus produce cereins, bacteriocins active against different B. cereus strains or other Gram-positive bacteria.[11]

Reproduction

At 30 °C (86 °F), a population of B. cereus can double in as little as 20 minutes or as long as 3 hours, depending on the food product.[12]

FoodMinutes to double, 30 °C (86 °F)Hours to multiply by 1,000,000
Milk20-366.6 - 12
Cooked rice26-318.6 - 10.3
Infant formula5618.6

Pathogenesis

B. cereus is responsible for a minority of foodborne illnesses (2–5%), causing severe nausea, vomiting, and diarrhea.[13] Bacillus foodborne illnesses occur due to survival of the bacterial endospores when food is improperly cooked.[14] Cooking temperatures less than or equal to 100 °C (212 °F) allow some B. cereus spores to survive.[15] This problem is compounded when food is then improperly refrigerated, allowing the endospores to germinate.[16] Cooked foods not meant for either immediate consumption or rapid cooling and refrigeration should be kept at temperatures below 10 °C (50 °F) or above 50 °C (122 °F).[15] Germination and growth generally occur between 10 °C and 50 °C,[15] though some strains are psychrotrophic.[17] Bacterial growth results in production of enterotoxins, one of which is highly resistant to heat and acids (pH levels between 2 and 11);[18] ingestion leads to two types of illness, diarrheal and emetic (vomiting) syndrome.[19]

  • The diarrheal type is associated with a wide range of foods, has an 8.0- to 16-hour incubation time, and is associated with diarrhea and gastrointestinal pain. Also known as the 'long-incubation' form of B. cereus food poisoning, it might be difficult to differentiate from poisoning caused by Clostridium perfringens.[18] Enterotoxin can be inactivated after heating at 56 °C (133 °F) for 5 minutes however it is unclear whether its presence in food causes the symptom since it degrades in stomach enzymes; its subsequent production by surviving B. cereus spores within the small intestine may be the cause of illness.[20]
  • The 'emetic' form is commonly caused by rice cooked for a time and temperature insufficient to kill any spores present, then improperly refrigerated. It can produce a toxin, cereulide, which is not inactivated by later reheating. This form leads to nausea and vomiting one to five hours after consumption. It can be difficult to distinguish from other short-term bacterial foodborne intoxications such as by Staphylococcus aureus.[18] Emetic toxin can withstand 121 °C (250 °F) for 90 minutes.[20]

The diarrhetic syndromes observed in patients are thought to stem from the three toxins: hemolysin BL (Hbl), nonhemolytic enterotoxin (Nhe) and cytotoxin K (CytK).[21] The nhe/hbl/cytK genes are located on the chromosome of the bacteria. Transcription of these genes is controlled by PlcR. These genes occur in the taxonomically related B. thuringiensis and B. anthracis, as well. These enterotoxins are all produced in the small intestine of the host, thus thwarting digestion by host endogenous enzymes. The Hbl and Nhe toxins are pore-forming toxins closely related to ClyA of E. coli. The proteins exhibit a conformation known as "beta-barrel" that can insert into cellular membranes due to a hydrophobic exterior, thus creating pores with hydrophilic interiors. The effect is loss of cellular membrane potential and eventually cell death. CytK is a pore-forming protein more related to other hemolysins.

The timing of the toxin production was previously thought to be possibly responsible for the two different courses of disease, but in fact the emetic syndrome is caused by a toxin, cereulide, found only in emetic strains and is not part of the "standard toolbox" of B. cereus. Cereulide is a cyclic polypeptide containing three repeats of four amino acids: D-oxy-Leu—D-Ala—L-oxy-Val—L-Val (similar to valinomycin produced by Streptomyces griseus) produced by nonribosomal peptide synthesis. Cereulide is believed to bind to 5-hydroxytryptamine 3 (5-HT3) serotonin receptors, activating them and leading to increased afferent vagus nerve stimulation.[22] It was shown independently by two research groups to be encoded on multiple plasmids: pCERE01[23] or pBCE4810.[24] Plasmid pBCE4810 shares homology with the Bacillus anthracis virulence plasmid pXO1, which encodes the anthrax toxin. Periodontal isolates of B. cereus also possess distinct pXO1-like plasmids. Like most of cyclic peptides containing nonproteogenic amino acids, cereulid is resistant to heat, proteolysis, and acid conditions.[25]

B. cereus is also known to cause difficult-to-eradicate chronic skin infections, though less aggressive than necrotizing fasciitis. B. cereus can also cause keratitis.[26]

Diagnosis

In case of foodborne illness, the diagnosis of B. cereus can be confirmed by the isolation of more than 105 B. cereus organisms per gram from epidemiologically implicated food, but such testing is often not done because the illness is relatively harmless and usually self-limiting.[27]

Prognosis

Most emetic patients recover within six to 24 hours,[19] but in some cases, the toxin can be fatal.[28][29][30][31][32] In 2014, 23 neonates receiving total parenteral nutrition contaminated with B. cereus developed septicaemia, with three of the infants later dying as a result of infection.[33][34]

References

  1. ↑ Ryan KJ; Ray CG, eds. (2004). Sherris Medical Microbiology (4th ed.). McGraw Hill. ISBN 0-8385-8529-9.
  2. ↑ Asaeda, Glenn; Caicedo, Gilbert; Swanson, Christopher (December 2005). "Fried Rice Syndrome". Journal of Emergency Medical Services. 30 (12): 30–32. doi:10.1016/s0197-2510(05)70258-8. PMID 16373130.
  3. ↑ Alseth, Ingrun; Rognes, Torbjørn; Lindbäck, Toril; Solberg, Inger; et al. (2006). "A new protein superfamily includes two novel 3-methyladenine DNA glycosylases Bacillus cereus, AlkC and AlkD". Molecular Microbiology. 59 (5): 1602–9. doi:10.1111/j.1365-2958.2006.05044.x. PMC 1413580Freely accessible. PMID 16468998.
  4. ↑ Frankland, G. C.; Frankland, P. F. (1 January 1887). "Studies on Some New Micro-Organisms Obtained from Air". Philosophical Transactions of the Royal Society B: Biological Sciences. 178: 257–287. doi:10.1098/rstb.1887.0011.
  5. ↑ Sandle, Tim (28 November 2014). "The Risk of Bacillus cereus to Pharmaceutical Manufacturing". American Pharmaceutical Review (Paper). 17 (6): 56.
  6. ↑ Vilà, B.; Fontgibell, A.; Badiola, I.; Esteve-Garcia, E.; et al. (2009). "Reduction of Salmonella enterica var. Enteritidis colonization and invasion by Bacillus cereus var. toyoi inclusion in poultry feeds". Poultry Science. HighWire Press. 88 (55): 975–9. doi:10.3382/ps.2008-00483. PMID 19359685.
  7. ↑ Bories, Georges; Brantom, Paul; de Barberà, Joaquim Brufau; et al. (9 December 2008). "Safety and efficacy of the product Toyocerin (Bacillus cereus var. toyoi) as feed additive for rabbit breeding does". EFSA Journal. Scientific Opinion of the Panel on Additives and Products or Substances used in Animal Feed. European Food Safety Authority. 2009 (1): 913. doi:10.2903/j.efsa.2009.913. eISSN 1831-4732. EFSA-Q-2008-287. Retrieved 14 May 2009.
  8. ↑ Bories, Georges; Brantom, Paul; de Barberà, Joaquim Brufau; et al. (16 March 2007). "Opinion of the Scientific Panel on Additives and Products or Substances used in Animal Feed on the safety and efficacy of the product Toyocerin (Bacillus cereus var. Toyoi) as a feed additive for sows from service to weaning, in accordance with Regulation (EC) No 1831/2003". EFSA Journal. Scientific Opinion of the Panel on Additives and Products or Substances used in Animal Feed. European Food Safety Authority. 2007 (3): 458. doi:10.2903/j.efsa.2007.458. eISSN 1831-4732. EFSA-Q-2006-037. Retrieved 14 May 2009.
  9. ↑ "Notes from the Field: Contamination of Alcohol Prep Pads with Bacillus cereus Group and Bacillus Species --- Colorado, 2010". CDC. March 25, 2011.
  10. ↑ Hsueh, PR; et al. (1999). "Nosocomial pseudoepidemic caused by Bacillus cereus traced to contaminated ethyl alcohol from a liquor factory". J Clin Microbiol. 37: 2280–4. PMC 85137Freely accessible. PMID 10364598.
  11. ↑ Naclerio, G; Ricca, E; Sacco, M; De Felice, M (December 1993). "Antimicrobial activity of a newly identified bacteriocin of Bacillus cereus". Appl Environ Microbiol. 59 (12): 4313–6. PMID 8285719.
  12. ↑ Mikkola, Raimo. Food and Indoor Air Isolated Bacillus Non-Protein Toxins: Structures, Physico-Chemical Properties and Mechanisms of Effects on Eukaryotic Cells (PDF). p. 12. Retrieved 2015-10-24.
  13. ↑ Kotiranta A, Lounatmaa K, Haapasalo M (2000). "Epidemiology and pathogenesis of Bacillus cereus infections". Microbes Infect. 2 (2): 189–98. doi:10.1016/S1286-4579(00)00269-0. PMID 10742691.
  14. ↑ Turnbull PCB (1996). Baron S; et al., eds. Bacillus. In: Baron's Medical Microbiology (4th ed.). Univ of Texas Medical Branch. ISBN 0-9631172-1-1. (via NCBI Bookshelf).
  15. 1 2 3 Roberts, T. A.; Baird-Parker, A. C.; Tompkin, R. B. (1996). Characteristics of microbial pathogens. London: Blackie Academic & Professional. p. 24. ISBN 0-412-47350-X. Retrieved 25 November 2010.
  16. ↑ McKillip JL (2000). "Prevalence and expression of enterotoxins in Bacillus cereus and other Bacillus spp., a literature review". Antonie Van Leeuwenhoek. 77 (4): 393–9. doi:10.1023/A:1002706906154. PMID 10959569.
  17. ↑ Davis, Judi Ratliff; Lawley, Richard; Davis, Judy; Laurie Curtis (2008). The food safety hazard guidebook. Cambridge, UK: RSC Pub. p. 17. ISBN 0-85404-460-4. Retrieved 25 November 2010.
  18. 1 2 3 "Bacillus cereus". Todar's Online Textbook of Bacteriology. Retrieved 19 September 2009.
  19. 1 2 Ehling-Schulz M, Fricker M, Scherer S (2004). "Bacillus cereus, the causative agent of an emetic type of food-borne illness". Mol Nutr Food Res. 48 (7): 479–87. doi:10.1002/mnfr.200400055. PMID 15538709.
  20. 1 2 Watson, David (1998). Natural Toxicants in Food. pp. 133–134.
  21. ↑ Guinebretière MH, Broussolle V, Nguyen-The C (August 2002). "Enterotoxigenic Profiles of Food-poisoning and Food-borne Bacillus cereus Strains". J. Clin. Microbiol. 40 (8): 3053–6. doi:10.1128/JCM.40.8.3053-3056.2002. PMC 120679Freely accessible. PMID 12149378.
  22. ↑ Agata N, Ohta M, Mori M, Isobe M (1995). "A novel dodecadepsipeptide, cereulide, is an emetic toxin of Bacillus cereus". FEMS Microbiol Lett. 129 (1): 17–20. doi:10.1016/0378-1097(95)00119-P. PMID 7781985.
  23. ↑ Hoton FM, Andrup L, Swiecicka I, Mahillon J (2005). "The cereulide genetic determinants of emetic Bacillus cereus are plasmid-borne". Microbiology. 151 (7): 2121–4. doi:10.1099/mic.0.28069-0. PMID 16000702.
  24. ↑ Ehling-Schulz M, Fricker M, Grallert H, Rieck P, Wagner M, Scherer S (2006). "Cereulide synthetase gene cluster from emetic Bacillus cereus: Structure and location on a mega virulence plasmid related to Bacillus anthracis toxin plasmid pXO1". BMC Microbiol. 6: 20. doi:10.1186/1471-2180-6-20. PMC 1459170Freely accessible. PMID 16512902.
  25. ↑ Stenfors Arnesen LP, Fagerlund A, Granum PE (2008). "From soil to gut: Bacillus cereus and its food poisoning toxins". FEMS Microbiol Rev. 32 (4): 579–606. doi:10.1111/j.1574-6976.2008.00112.x. PMID 18422617.
  26. ↑ Pinna A; Sechi LA; Zanetti S; et al. (October 2001). "Bacillus cereus keratitis associated with contact lens wear". Ophthalmology. 108 (10): 1830–4. doi:10.1016/S0161-6420(01)00723-0. PMID 11581057.
  27. ↑ Bacillus cereus Food Poisoning Associated with Fried Rice at Two Child Day Care Centers from Morbidity and Mortality Weekly Report from Centers for Disease Control and Prevention. 18 March 1994 / Vol. 43 / No. 10 U.S.
  28. ↑ Takabe F, Oya M (1976). "An autopsy case of food poisoning associated with Bacillus cereus". Forensic Science. 7 (2): 97–101. doi:10.1016/0300-9432(76)90024-8. PMID 823082.
  29. ↑ Mahler H; et al. (1997). "Fulminant liver failure in association with the emetic toxin of Bacillus cereus". N Engl J Med. 336 (16): 1142–1148. doi:10.1056/NEJM199704173361604. PMID 9099658.
  30. ↑ Dierick K; et al. (2005). "Fatal family outbreak of Bacillus cereus-associated food poisoning". J Clin Microbiol. 43 (8): 4277–4279. doi:10.1128/JCM.43.8.4277-4279.2005. PMC 1233987Freely accessible. PMID 16082000.
  31. ↑ Shiota, M; et al. (2010). "Rapid Detoxification of Cereulide in Bacillus cereus Food Poisoning". Pediatrics. 125 (4): e951–e955. doi:10.1542/peds.2009-2319. PMID 20194285.
  32. ↑ Naranjo, M; et al. (2011). "Sudden Death of a Young Adult Associated with Bacillus cereus Food Poisoning". J Clin Microbiol. 49 (12): 4379–4381. doi:10.1128/JCM.05129-11. PMC 3232990Freely accessible. PMID 22012017.
  33. ↑ Lipid Phase only of Parenteral Nutrition - potential contamination with Bacillus cereus. UK Medicines and Healthcare products Regulatory Agency. Medical safety alert (4 June 2014)
  34. ↑ Cooper, Charlie (1 July 2014) Third baby dies from contaminated 'Total Parenteral Nutrition' drip feed. The Independent

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