Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
권호 표지

Growth Inhibitory Activity of Sulfur Compounds of Garlic against Pathogenic Microorganisms

마늘 황화합물의 병원성미생물 번식억제작용

  • Published : 2006.09.01
Download PDF
⟨ Previous Next ⟩

Abstract

Efforts have been made to explore the possibility of using garlic as an antimicrobial therapeutic agent since garlic extract and its individual sulfur compounds show antimicrobial activities against all kinds of microorganisms including bacteria, molds, yeasts and protozoa. Staphylococcus aureus has been the most studied bacteria along with many other Gram positive and negative pathogenic bacteria, including species of the genera Clostridium, Mycobacterium, Escherichia, Klebsiella, Bacillus, Salmonella and Shigella. Candida albicans has been the most studied among the eukaryotic microorganisms. A pathogenic protozoa, Giardia intestinalis, was also tested. All the microorganisms tested was inhibited by garlic extract or its sulfur components. Garlic has been known to be growth inhibitory only when fresh garlic is crushed, since allicin-generating reaction is enzyme-catalyzed. Allicin is known to be growth inhibitory through a non-specific reaction with sulfhydryl groups of enzyme proteins that are crucial to the metabolism of microorganisms. Another plausible hypothesis is that allicin inhibits specific enzymes in certain biological processes, e.g. acetyl CoA synthetase in fatty acid synthesis in microorganisms. Allicin transforms into other compounds like ajoene and various sulfides which are also inhibitory to microorganisms, but not as potent as their mother compound. It is reported recently that garlic heated at cooking temperatures is growth inhibitory especially against yeasts, and that the growth inhibitory compound is allyl alcohol thermally generated from alliin in garlic.

마늘과 마늘의 황화합물은 여러 가지 미생물(그람양성 및 음성 세균, 곰팡이, 효모, 원생동물)의 번식을 저해하므로 마늘을 감염증치료에 쓰고자 하는 노력이 많았고 따라서 병원성 미생물에 대한 번식저해연구가 많이 수행되었다. 마늘에 의한 병원성 미생물의 번식저해작용을 연구한 대상 미생물 중에서 세균으로는 Staphylococcus aureus가 가장 많이 연구되었고 기타 많은 종류의 그람음성 및 앙성 병원성 세균이 연구대상이었다. 효모와 곰팡이를 통털어 Candide albicans의 번식저해 연구가 전체 진균류 연구의 대부분을 차지하였다. 특이하게 Giardia intestinalis에 대한 연구보고도 있었으며 마늘은 시험한 대부분의 미생물에 대해 강력한 천연 항균제로서 인정되었다. 마늘은 원래 가열하지 않은 생마늘이어야 알린이 alliinase 효소에 의해 분해되어 강력한 항균물질인 알리신을 생성하게 되므로 주로 생마늘의 항균작용연구가 주를 이루었다 알리신은 불안정하여 저장중에 분해되어 여러 가지 물질로 변화하게 되는 데 알리신이 분해되어 생성되는 ajoene이나 기타 여러 가지 sulfide류 역시 세균이나 효모에 매우 강력한 항균작용을 나타낸다. 마늘의 알리신이 나타내는 항균작용은 thiosulfinate기가 미생물의 대사에 중요한 역할을 하는 효소중에서 -SH 기를 가지는 효소단백질과 결합하여 불활성화시키기 때문에 결과적으로 미생물이 사멸하는 것으로 설명되고 있다. 하지만 이와 같은 일반적인 독성 메카니즘 이외에 특이한 효소에 특이하게 저해작용을 나타낸다는 가설이 있고 그 중에서도 지방산 합성에 관여하는 효소를 저해하기 때문이라는 의견이 많다. 최근에 식품의 조리 온도에서 가열한 마늘이 항균작용이 있는 것이 발견되었는데 그 작용은 주로 항진균작용이며 그 항균작용물질은 알린이 열분해 되어 생성되는 allyl alcohol인 것으로 보고되었다.

Keywords

References

  1. Walton, L., Herbold, M. and Lindegren, C. C.: Bactericidal effects of vapors from crushed garlic. Food Res. 1, 163-169 (1936) https://doi.org/10.1111/j.1365-2621.1936.tb17778.x
  2. Cavallito, C. J. and Bailey, J. H.: Allicin, the antibacterial principle of Allium sativum. I: Isolation, physical properties and antimicrobial action. J. Amer. Chem. Soc. 66, 1950-1951 (1944) https://doi.org/10.1021/ja01239a048
  3. Stoll, A. and Seebeck, E.: Chemical investigation of alliin, the specific principle of garlic. Adv. Enzymol. 11, 377-400 (1951)
  4. Small, L. D., Bailey, J. H. and Cavallito, C. J.: Alkyl thiosulfinates. J. Am. Chem. Soc. 69, 1710-1713 (1947) https://doi.org/10.1021/ja01199a040
  5. Cavallito, C. J., Buck, J. S. and Suter, C. M.: Allicin, the antibacterial principles of Allium sativim. II. Determination of the chemical structure. J. Am. Chem. Soc. 66, 1952-1954 (1944) https://doi.org/10.1021/ja01239a049
  6. Block, E., Naganathan, S., Putman, D. and Zhao, S.-H.: Allium chemistry: HPLC analysis of thiosulfinates from onion, garlic, wild garlic (Ramsons), leek, scallion, shallot, elephant (greatheaded) garlic, chive, and Chinese chive. J. Agric. Food Chem. 40, 2418-2430 (1992) https://doi.org/10.1021/jf00024a017
  7. Stoll, A. and Seebeck, E.: Uber Alliin, Die Genuine Muttersubstanz Des Knoblauchols. 1. Mitteilung uber Allium Substanzen. Helv. Chim. Acta 31, 189-210 (1948) https://doi.org/10.1002/hlca.19480310140
  8. Stoll, A. and Seebeck, E. Die Synthese Des Naturlichen Alliins and Seiner Drei Optisch Aktiven Isomeren. 5. Mitteilung uber Allium-Substanzen, Helv. Chim. Acta 34, 481-487 (1951) https://doi.org/10.1002/hlca.19510340212
  9. Rundqvist, C.: Pharmacological investigation of Allium bulbs. Pharmaceutiskt Notisblad. 18, 323-333 (1909)
  10. Caragay, A. B.: Cancer-preventive foods and ingredients. Food Technol. 46, 65-68 (1992)
  11. Augusti, K. T. and Mathew, P. T.: Lipid lowering effect of allicin (diallyl disulphide-oxide) on long term feeding to normal rats. Experientia 30, 468-470 (1974) https://doi.org/10.1007/BF01926297
  12. Rees, L. P., Minney, S. F., Plummer, N. T., Slator, J. H. and Skyrme, D. A.: A quantitative assessment of the antimicrobial activity of garlic (Allium sativum). World J. Microbiol. Biotechnol. 9, 303-307 (1993) https://doi.org/10.1007/BF00383068
  13. Block, E., Ahmed, S., Jain, M. K., Creely, R. W, Apitz-Castro, R. and Cruz, M. R.: (E,Z)-Ajoene: A potent antithrombotic agent from garlic. J. Am. Chem. Soc. 106, 8295-8296 (1984) https://doi.org/10.1021/ja00338a049
  14. Wills, E. D.: Enzyme inhibition by allicin, the active principle of garlic. Biochem. J. 63, 514-520 (1956) https://doi.org/10.1042/bj0630514
  15. Adetumbi, M., Javor, G. T. and Lau, B. H. S.: Allium sativum (garlic) inhibits lipid synthesis in Candida albicans, Antimicrob. Agents Chemother. 30, 499-501 (1986) https://doi.org/10.1128/AAC.30.3.499
  16. Ghannoum, M. A.: Studies of the antimicrobial mode of action of Allium sativum (garlic). J. Gen. Microbiol. 134, 2917-2924 (1988)
  17. Feldberg, R. S., Chang, S. C., Kotik, A. N., Nadler, M., Neuwirth, Z., Sundstrom, D. C. and Thompson, N. H.: In vitro mechanism of inhibition of bacterial cell growth by allicin. Antimicrob. Agents Chemother. 32, 1763-1768 (1988) https://doi.org/10.1128/AAC.32.12.1763
  18. Focke, M., Feld, A. and Lichtenthaler, H. K.: Allicin, a naturally occurring antibiotic from garlic, specifically inhibits acetyl-CoA synthetase. FEBS 261, 106-108 (1990) https://doi.org/10.1016/0014-5793(90)80647-2
  19. Kyung, K. H., Kim, M. H., Park, M. S. and Kim, Y. S.: Alliinase-independent inhibition of Staphylococus aureus B33 by heated garlic. J. Food Sci. 67, 780-785 (2002) https://doi.org/10.1111/j.1365-2621.2002.tb10676.x
  20. Kim, J. W. and Kyung, K. H.: Antiyeast activity ofheated garlic in the absence of alliinase enzyme action. J. Food Sci. 68, 1766-1770 (2003) https://doi.org/10.1111/j.1365-2621.2003.tb12326.x
  21. Dababneh, F. A. and Al-Delaimy, K. S.: Inhibition of Staphylococcus aureus by garlic extract. Lebensm. Wissenschaft. Technol. 17, 29-31 (1984)
  22. Mantis, A.J., Karaioannoglou, P. G., Spanos, G. P. and Panetos, A. G.: The effect of garlic extract on food poisoning bacteria in culture media. I. Staphylococcus aureus. Lebensm. Wissenschaft. Technol. 11, 26-28 (1978)
  23. Johnson, M. G. and Vaughn, R. H.: Death of Salmonella typhimurium and Escherichia coli in the presence of freshly reconstituted dehydrated garlic and onion. Appl. Microbiol. 17, 903-905 (1969)
  24. Saleem, Z. M. and Al-Delaimy, K. S.: Inhibition of Bacillus cereus by garlic extracts. J. Food Prot. 45, 1007-1009 (1982) https://doi.org/10.4315/0362-028X-45.11.1007
  25. De Wit, J. C., Notermans, S., Gorin, N. and Kampelmacher, E. H.: Effects of garlic oil or onion oil on toxin production by Clostridium botulinum in meat slurry. J. Food Prot. 42, 222-224 (1979) https://doi.org/10.4315/0362-028X-42.3.222
  26. Mantis, A. J., and Koidis, P. A., Karaioannoglou, P. G. and Panetos, A. G.: Effect of garlic extract on food poisoning bacteria. Lebensm. Wissenschaft. Technol. 12, 230-232 (1979)
  27. Barone, F. E. and Tansey, M. R.: Isolation, purification, identification, synthesis, and kinetics of activity of the anticandidal component of Allium sativum, and a hypothesis for its mode of action. Mycologia 69, 793-825 (1977) https://doi.org/10.2307/3758870
  28. Al-Delaimy, K. S. and Ali, S. H.: Antibacterial action of vegetable extracts on the growth of pathogenic bacteria. J. Sci. Food Agric. 21, 110-112 (1970) https://doi.org/10.1002/jsfa.2740210214
  29. Srivastava, K. C., Perera, A. D. and Saridakis, H. O.: Bacteriostatic effects of garlic sap on Gram negative pathogenic bacteria: An in vitro study. Lebensm. Wissenschaft. Technol. 15, 74-76 (1982)
  30. Moore, G. S. and Atkins, R. D. The fungicidal and fungistatic effects of aqueous garlic extract on medically important yeastlike fungi. Mycologia 69, 341-348 (1977) https://doi.org/10.2307/3758659
  31. Tansey, M. R. and Appleton, J. A.: Inhibition of fungal growth by garlic extract. Mycologia 67, 409-413 (1975) https://doi.org/10.2307/3758431
  32. Singh, K. V. and Shukula, N. P.: Activity of multiple resistant bacteria of garlic (Allium sativum) extract. Fitoterapia 15, 313-315 (1984)
  33. O'Gara, E. A., Hill, D. J. and Maslin, D. J.: Activities of garlic oil, garlic powder, and their diallyl constituents against Helicobacter pylori. Appl. Environ. Microbiol. 66, 2269-2273 (2000) https://doi.org/10.1128/AEM.66.5.2269-2273.2000
  34. Ross, Z. M., O'Gara, E. A., Hill, D. J., Sleighttholme, H. V. and Maslin, D. J.: Antimicrobial properties of garlic oil against human enteric bacteria: Evaluation of methodologies and comparisons with garlic oil sulfides and garlic powder. Appl. Environ. Microbiol. 67, 475-480 (2001) https://doi.org/10.1128/AEM.67.1.475-480.2001
  35. Small, L. D., Bailey, J. H. and Cavallito, C. J.: Comparison of some properties of thiosulfonates and thiosulfinates. J. Am. Chem. Soc. 71, 3565-3566 (1949) https://doi.org/10.1021/ja01178a531
  36. Brown, H. D., Matzuk, A. R., Becker, H. J., Conbere, J. P., Constantin, J. M., Solotorovsky, M., Winsten, S., Ironson, E. and Quastel, J. H.: The antituberculosis activity of some ethylmercapto compounds. J. Am. Chem. Soc. 76, 3860 (1954)
  37. Naganawa, R., Iwata, N., Ishikawa, K., Fukyda, H., Fujino, T. and Suzuki, A.: Inhibition of microbial growth by ajoene, a sulfur-containing compound derived from garlic. Appl. Environ. Microbiol. 62, 4238-4242 (1996)
  38. Yoshida, S., Kasuga, S., Hayashi, N., Ushiroguchi, T., Matsuura, H. and Nakagawa, S.: Antifungal activity of ajoene derived from garlic. Appl. Environ. Microbiol. 53, 615-617 (1987)
  39. Lemar, K. M., Turner, M. P. and Lloyd, D. : Garlic (Allium sativum) as an anti-Candida agent: a comparison of the efficacy of fresh garlic and freeze-dried extracts. J. Appl. Microbiol. 93, 398-405 (2002) https://doi.org/10.1046/j.1365-2672.2002.01707.x
  40. Lemar, K. M.., Muller, C. T., Plummer, S. and Lloyd, D. : Cell death mechanisms in the human opportunistic pathogen Candida albicans. J. Eukaryot. Microbiol. 685-686 (2003)
  41. Harris, J. C., Plummer, S., Turner, M. P. and Lloyd, D. : The microaerophilic flagellate Giardia intestinlis: Allium sativum (garlic) is an effective antigiardial. Microbiology 146, 3119-3127 (2000) https://doi.org/10.1099/00221287-146-12-3119
  42. Mae, T., Ohira, K. and Fujiwara, A.: Fate of (+)S-methyl-Lcysteine sulfoxide in Chinese cabbage, Brassica pekinesis RUPR. Plant Cell Physiol. 12, 1-11 (1971) https://doi.org/10.1093/oxfordjournals.pcp.a074591
  43. Lawson, L. D. Garlic: A review of its medicinal effects and indicated active compounds. In Lawson, L. D. and Bauer, R.(eds.) Phytomedicines of Europe: Their chemistry & biological activity. ACS Symposium Series 691, 176-209 (1998)
  44. Nomura, J., Nishizuka, Y. and Hayaishi, O.: S-Alkylcysteinase: Enzymatic cleavage of S-methyl-L-cysteine and its sulfoxide. J. Biol. Chem. 238, 1441-1446 (1963)
  45. Murakami, F.: Studies on the nutritional value of Allium Plants(XXXVI) Decomposition of alliin homologues by microorganism and formation of substance with thiamine masking activity. Vitamins (Tokyo) 20, 126 (1960)
  46. Brodnitz, M. H., Pascale, J. V. and von Derslice, L.: Flavor components of garlic extract. J. Agric. Food Chem. 19, 273-275 (1971) https://doi.org/10.1021/jf60174a007
  47. Yu, T.-H. and Wu, C.-M.: Stability of allicin in garlic juice. J. Food Sci. 54, 977-981 (1989) https://doi.org/10.1111/j.1365-2621.1989.tb07926.x
  48. Kim, J. W., Huh, J. E., Kyung, S. H. and Kyung, K. H.: Antimicrobial activity of alk(en)yl sulfides found in essential oils of garlic and onion. Food Sci. Biotechnol. 13, 235-239 (2004)
  49. Choi, J. H. and Kyung, K. H.: Allyl alcohol is the sole antiyeast compound in heated garlic extract. J. Food Sci. 70, M305-M309 (2005)
  50. Pentz, R. and Siegers, C.P.: Garlic preparations: Methods for quantitative and qualitative assessment of their ingredients. In: Garlic, The science and therapeutic application of Allium sativum L. and related species, 2nded. (eds. Koch, H. P. and Lawson, L. D.). Williams and Wilkins (1996)
  51. Kim, J. W., Kim, Y. S. and Kyung, K. H.: Inhibitory activity of essential oils of garlic and onion against bacteria and yeasts. J. Food Prot. 67, 499-504 (2004) https://doi.org/10.4315/0362-028X-67.3.499
  52. Lawson, L. D., Wang, Z. J. and Hughes, B. G.: Identification and HPLC analysis of sulfides and dialk(en)yl thiosulfinates in commercial garlic products. Planta Med. 57, 363-370 (1991) https://doi.org/10.1055/s-2006-960119
  53. Miron, T., Rabinkov, A., Mirelman, D., Wilchek, M. and Einer, L.: The mode of action of allicin: its ready permeability through phospholipid membranes amy contribute to its biological activity. Bioch. Biophys. Acta 1463, 20-30 (2000) https://doi.org/10.1016/S0005-2736(99)00174-1
  54. Silva, J. M. and O'Brien, P. J.: Allyl alcohol- and acroleininduced toxicity in isolated rat hepatocytes. Archiv. Biochem. Biophys. 275, 551-558 (1989) https://doi.org/10.1016/0003-9861(89)90401-3
  55. Lee, S., Woo, Y. H. and Kyung, K. H.: Allyl alcohol found in heated garlic is a potent selective inhibitor for yeasts but not for bacteria. J. Microbiol. Biotechnol. In press (2006)
  56. Youngleson, J. S., Santangelo, J. D., Jones, D. T. and Woods, D. R.: Cloning and expression of a Clostridium acetobutylicum alchohol dehyadrogease gene in Escherichia coli. Appl. Environ. Microbiol. 54, 676-682 (1988)
  57. Rando, R. R.: Allyl alcohol-induced irreversible inhibition of yeast alcohol dehydrogenase. Biochem. Pharmacol. 23, 2328-2331 (1974) https://doi.org/10.1016/0006-2952(74)90563-2
  58. Dickinson, F. and Dalziel, K.: The specifications and configurations of ternary complexes of yeast and liver alcohol dehydrogenases. Biochem. J. 104, 165-172 (1967) https://doi.org/10.1042/bj1040165
  59. Lorowitz, W. and Clark, D.: Escherichia coli mutants with a temperature-sensitive alcohol dehydrogenase. J. Bacteriol. 152, 935-938 (1982)
  60. Wills, C. and Hom, D.: An efficient selection producing structural gene mutants of yeast alcohol dehydrogense resistant to pyrazole. Genetics 11, 791-795 (1988)