Carvacrol suppresses high pressure high temperature inactivation of Bacillus cereus spores

International Journal of Food Microbiology

Volumn 197, Issue , 2015, Pages 45-52

  Luu Thi, Hue ^a   Corthouts, Jorinde ^a   Passaris, Ioannis ^a   Grauwet, Tara ^a   Aertsen, Abram ^a   Hendrickx, Marc ^a   Michiels, Chris W ^a  

^a LEUVEN FOOD SCIENCE AND NUTRITION RESEARCH CENTRE LFORCE   (Belgium)

Author keywords

Bacillus cereus spores; Carvacrol; Dipicolinic acid; Germination and inactivation; High pressure high temperature treatment; Spore refractility

Indexed keywords

CARVACROL; DIPICOLINIC ACID; ANTIINFECTIVE AGENT; PICOLINIC ACID DERIVATIVE; TERPENE;

ARTICLE; BACILLUS CEREUS; BACTERIAL SPORE; BACTERIAL VIABILITY; HEAT TOLERANCE; HEAT TREATMENT; HIGH PRESSURE HIGH TEMPERATURE TREATMENT; HIGH TEMPERATURE; HYDROLYSIS; HYPERBARISM; MINIMUM INHIBITORY CONCENTRATION; NONHUMAN; PH; PKA; SPORE GERMINATION; CHEMISTRY; DRUG EFFECTS; HEAT; METABOLISM; MICROBIAL VIABILITY; PHYSIOLOGY; PRESSURE;

BACILLUS CEREUS; BACTERIA (MICROORGANISMS);

ANTI-BACTERIAL AGENTS; BACILLUS CEREUS; HOT TEMPERATURE; MICROBIAL VIABILITY; MONOTERPENES; PICOLINIC ACIDS; PRESSURE; SPORES, BACTERIAL;

EID: 84920195995     PISSN: 01681605     EISSN: 18793460     Source Type: Journal    
DOI: 10.1016/j.ijfoodmicro.2014.12.016     Document Type: Article

References (43)

1. Bevilacqua A., Sinigaglia M., Corbo M.R. Effects of pH, cinnamaldehyde and heat-treatment time on spore viability of Alicyclobacillus acidoterrestris. Int. J. Food Sci. Technol. 2009, 44:380-385.
2. Bevilacqua A., Corbo M.R., Sinigaglia M. Use of essential oils to inhibit Alicyclobacillus acidoterrestris: a short overview of the literature. Front. Microbiol. 2011, 2:195.
3. Black E.P., Koziol-Dube K., Guan D., Wei J., Setlow B., Cortezzo D.E., Hoover D.G., Setlow P. Factors influencing germination of Bacillus subtilis spores via activation of nutrient receptors by high pressure. Appl. Environ. Microbiol. 2005, 71:5879-5887.
4. Black E.P., Wei J., Atluri S., Cortezzo D.E., Koziol-Dube K., Hoover D.G., Setlow P. Analysis of factors influencing the rate of germination of spores of Bacillus subtilis by very high pressure. J. Appl. Microbiol. 2007, 102:65-76.
5. Black E.P., Linton M., McCall R.D., Curran W., Fitzgerald G.F., Kelly A.L., Patterson M.F. The combined effects of high pressure and nisin on germination and inactivation of Bacillus spores in milk. J. Appl. Microbiol. 2008, 105:78-87.
6. Bruins M.E., Matser A.M., Janssen A.E.M., Boom R.M. Buffer selection for HP treatment of biomaterials and its consequences for enzyme inactivation studies. High Press. Res. 2007, 27(1):101-107.
7. Coleman W.H., Chen D., Li Y.-q., Cowan A.E., Setlow P. How moist heat kills spores of Bacillus subtilis. J. Bacteriol. 2007, 189:8458-8466.
8. Coleman W.H., Zhang P., Li Y.-q., Setlow P. Mechanism of killing of spores of Bacillus cereus and Bacillus megaterium by wet heat. Lett. Appl. Microbiol. 2010, 50:507-514.
9. Cortezzo D.E., Setlow B., Setlow P. Analysis of the action of compounds that inhibit the germination of spores of Bacillus species. J. Appl. Microbiol. 2004, 96:725-741.
10. Gayan E., Torres J.A., Paredes-Sabja D. Hurdle approach to increase the microbial inactivation by high pressure processing: effect of essential oils. Food Eng. Rev. 2012, 4:141-148.
11. Grauwet T., Van der Plancken I., Vervoort L., Matser A., Hendrickx M., Van Loey A. Temperature uniformity mapping in a high pressure high temperature reactor by process impact evaluation on a temperature sensitive indicator. J. Food Eng. 2011, 105(1):36-47.
12. Haberbeck L.U., Riehl C.A.S., Salomao B.C.M., Aragão G.M.F. Bacillus coagulans spore inactivation through the application of oregano essential oil and heat. LWT Food Sci. Technol. 2012, 46:267-273.
13. Hofstetter S., Gebhardt D., Ho L., Gänzle M.G., McMullen L.M. Effects of nisin and reutericyclin on resistance of endospores of Clostridium spp. to heat and high pressure. Food Microbiol. 2013, 34:46-51.
14. Hofstetter S., Winter R., McMullen L.M., Gänzle M.G. In situ determination of membrane fluidity of endospores of Clostridium spp. during pressure-assisted thermal processing in combination with nisin or reutericyclin. Appl. Environ. Microbiol. 2013, 79:2103-2106.
15. Juneja V.K., Friedman M. Carvacrol, cinnamaldehyde, oregano oil, and thymol inhibit Clostridium perfringens spore germination and outgrowth in ground turkey during chilling. J. Food Prot. 2007, 70:218-222.
16. Juneja V.K., Thippareddi H., Friedman M. Control of Clostridium perfringens in cooked ground beef by carvacrol, cinnamaldehyde, thymol or oregano oil during chilling. J. Food Prot. 2006, 69:1546-1551.
17. Kong L., Zhang P., Yu J., Setlow P., Li Y.-q. Monitoring the kinetics of uptake of a nucleic acid dye during the germination of single spores of Bacillus species. Anal. Chem. 2010, 82:8717-8724.
18. Kort R., O'Brien A.C., van Stokkum I.H.M., Oomes S.J.C.M., Crielaard W., Hellingwerf K.J., Brul S. Assessment of heat resistance of bacterial spores from food product isolates by fluorescence monitoring of dipicolinic acid release. Appl. Environ. Microbiol. 2005, 71:3556-3564.
19. Marco A., Ferrer C., Velasco L.M., Rodrigo D., Muguerza B., Martinez A. Effect of olive powder and high hydrostatic pressure on the inactivation of Bacillus cereus spores in a reference medium. Foodborne Pathog. Dis. 2011, 8:681-685.
20. Margosch D., Ehrmann M.A., Gänzle M.G., Vogel R.F. Comparison of pressure and heat resistance of Clostridium botulinum and other endospores in mashed carrots. J. Food Prot. 2004, 67:2530-2537.
21. Margosch D., Ehrmann M.A., Buckow R., Heinz V., Vogel R.F., Ganzle M.G. High-pressure-mediated survival of Clostridium botulinum and Bacillus amyloliquefaciens endospores at high temperature. Appl. Environ. Microbiol. 2006, 3476-3481.
22. Olivier S.A., Bull M.K., Stone G., van Diepenbeek R.J., Kormelink F. Strong and consistently synergistic inactivation of spores of spoilage-associated Bacillus and Geobacillus spp. by high pressure and heat compared with inactivation by heat alone. Appl. Environ. Microbiol. 2011, 77:2317-2324.
23. Paidhungat M., Setlow P. Spore germination and outgrowth. Bacillus subtilis and Its Closest Relatives: From Genes to Cells 2002, 537-548. American Society for Microbiology, Washington DC. A.L. Sonenshein, J. Hoch, R. Losick (Eds.).
24. Paidhungat M., Setlow B., Daniels W.B., Hoover D., Papafragkou E., Setlow P. Mechanisms of induction of germination of Bacillus subtilis spores by high pressure. Appl. Environ. Microbiol. 2002, 68:3172-3175.
25. Patazca E., Koutchma T., Ramaswamy H.S. Inactivation kinetics of Geobacillus stearothermophilus spores in water using high-pressure processing at elevated temperatures. J. Food Sci. 2006, 71:110.
26. Periago P.M., Conesa R., Delago B., Fernandez P.S., Palop A. Bacillus magaterium spore germination and growth inhibition by a treatment combining heat with natural antimicrobials. Food Technol. Biotechnol. 2006, 44:17-23.
27. Reineke K., Mathys A., Knorr D. The impact of high pressure and temperature on bacterial spores: inactivation mechanisms of Bacillus subtilis above 500MPa. J. Food Sci. 2011, 76:189-197.
28. Reineke K., Doehner I., Schlumbach K., Baier D., Mathys A., Knorr D. The different pathways of spore germination and inactivation in dependence of pressure and temperature. Innov. Food Sci. Emerg. Technol. 2012, 13:31-41.
29. Reineke K., Mathys A., Heinz V., Knorr D. Mechanisms of endospore inactivation under high pressure. Trends Microbiol. 2013, 21:296-304.
30. Reineke K., Schlumbach K., Baier D., Mathys A., Knorr D. The release of dipicolinic acid - the rate-limiting step of Bacillus endospore inactivation during the high pressure thermal sterilization process. Int. J. Food Microbiol. 2013, 162:55-63.
31. Reineke K., Ellinger N., Berger D., Baier D., Mathys A., Setlow P., Knorr D. Structural analysis of high pressure treated Bacillus subtilis spores. Innov. Food Sci. Emerg. Technol. 2013, 17:43-53.
32. Rosato A., Vitali C., de Laurentis N., Armenise D., Nulillo M.A. Antibacterial effect of some essential oils administered alone or in combination with norfloxacin. Phytomedicine 2007, 14:727-732.
33. Setlow P. Spore germination. Curr. Opin. Biotechnol. 2003, 6:550-556.
34. Setlow P. When the sleepers wake: the germination of spores of Bacillus species. J. Appl. Microbiol. 2013, 115:1251-1268.
35. Sokolowska B., Skapska S., Fonberg-Broczek M., Niezgoda J., Chotkiewicz M., Dekowska A., Rzoska S. The combined effect of high pressure and nisin or lysozyme on the inactivation of Alicyclobacillus acidoterrestris spores in apple juice. High Press. Res. 2012, 32:119-127.
36. Sorg J.A., Sonenshein A.L. Inhibiting the initiation of Clostridium difficile spore germination using analogs of chenodeoxycholic acid, a bile acid. J. Bacteriol. 2010, 192:4983-4990.
37. van Melis C.C.J., Nierop Groot M.N., Tempelaars M.H., Moezelaar R., Abee T. Characterization of germination and outgrowth of sorbic acid-stressed Bacillus cereus ATCC14579 spores: phenotype and transcriptome analysis. Food Microbiol. 2011, 28:275-283.
38. van Melis C.C.J., Nierop Groot M.N., Abee T. Impact of sorbic acid on germinant receptor-dependent and -independent germination pathways in Bacillus cereus. Appl. Environ. Microbiol. 2011, 77:2552-2554.
39. van Melis C.C., Almeida C.B., Kort R., Groot M.N., Abee T. Germination inhibition of Bacillus cereus spores: impact of the lipophilic character of inhibiting compounds. Int. J. Food Microbiol. 2012, 160:124-130.
40. Vervoort L., Van der Plancken I., Grauwet T., Verjans P., Courtin C.M., Hendrickx M.E., Van Loey A. Xylanase B from the hyperthermophile Thermotoga maritima as an indicator for temperature gradients in high pressure high temperature processing. Innov. Food Sci. Emerg. Technol. 2011, 12:187-196.
41. Wuytack E.Y., Boven S., Michiels C.W. Comparative study of pressure-induced germination of spores at low and high pressures. Appl. Environ. Microbiol. 1998, 64:3220-3224.
42. Wuytack E.Y., Soons J., Poschet F., Michiels C.W. Comparative study of pressure and nutrient-induced germination of Bacillus subtilis spores. Appl. Environ. Microbiol. 2000, 66:257-261.
43. Zhu S., Naim F.M., Marcotte H., Ramaswamy H., Shao Y. High-pressure destruction kinetics of Clostridium sporogenes spores in ground beef at elevated temperatures. Int. J. Food Microbiol. 2008, 126:86-92.