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Behavior of Burkholderia thailandensis (Burkholderia pseudomallei surrogate) in Acidified Conditions by Organic Acids Used in Ready-to-Eat Meat Formulations under Different Water Activities

  • Yoon, Yo-Han (Department of Food and Nutrition, Sookmyung Women's University)
  • Received : 2010.11.03
  • Accepted : 2010.12.06
  • Published : 2010.12.31

Abstract

This study evaluated the antimicrobial effects of meat processing-related organic acids on Burkholderia thailandensis (Burkholderia pseudomallei surrogate) with different water activities. B. thailandensis KACC12027 (4 log CFU/mL) was inoculated in microwell plates containing tryptic soy broth pH-adjusted to 4, 5, 6, and 7 with ascorbic acid, citric acid, and lactic acid and with water activities adjusted to 0.94, 0.96, 0.98, and 1.0 with NaCl, followed by incubation at $35^{\circ}C$ for 30 h. The optical density (OD) of the samples was measured at 0, 3, 6, 12, 24, and 30 h at 595 nm to estimate the growth of B. thailandensis. Growth of B. thailandensis was observed only at water activity of 1.0. In general, more bacterial growth (p<0.05) was observed at pH 6 than at pH 7, and the antimicrobial effects of the organic acids on B. thailandensis were in the following order: Ascorbic acid > lactic acid > citric acid after incubation at $35^{\circ}C$ for 30 h. These results indicate that organic acids in meat processing-related formulations should be useful in decreasing the risk related to an emerging high risk agent (B. pseudomallei).

Keywords

References

  1. Ahamad, H. and Marth, E. H. (1989) Behavior of Listeria monocytogenes at 7, 13, 21, and ${35^{\circ}C}$ in tryptose broth and acidified with acetic, citric, or lactic acid. J. Food Prot. 52, 688-695.
  2. Bassetti, S., Bischoff, W. E., and Sherertz, R. J. (2005) Route of infection in melioidosis. Emerg. Infect. Dis. 11, 638-639. https://doi.org/10.3201/eid1104.041051
  3. Booth, I. R. and Kroll, R. G (1989) The preservation of food by low pH. pp. 119-160. In Gould, G. W. (ed.), Mechanisms of Action of Food Preservation Procedures, Elsevier, London.
  4. Bossi, P., Tegnell, A., Baka, A., Van Loock, F., Hendriks, J., Werner. A., Maidhof, H., and Gouvras, G. (2004) Bichat guidelines for the clinical management of glanders and melioidosis and bioterrorism-related glanders and melioidosis. Eur. Surveill. 9, E17-E18.
  5. Bracey, D., Holyoak, C. D., and Coote, P. J. (1998) Determination of the intracellular pH ($pH_{i}$) of growing cells of Saccharomyces cerevisiae: The effect of reduced expression of the membrane $H^{+}$ ATPase. J. Microbiol. Methods 31, 113-125. https://doi.org/10.1016/S0167-7012(97)00095-X
  6. Calicioglu, M., Sofos, J. N., Samelis, J., Kendall, P. A., and Smith, G. C. (2002) Inactivation of acid-adapted and nonadapted Escherichia coli O157:H7 during drying and storage of beef jerky treated with different marinades. J. Food Prot. 65, 1394-1405.
  7. Choy, J. L., Mayo, M., Janmaat, A., and Currie, B. J. (2000) Animal melioidosis in Australia. Acta Trop. 74, 153-158. https://doi.org/10.1016/S0001-706X(99)00065-0
  8. Currie, B. J. and Jacups, S. P. (2003) Intensity of rainfall and severity of melioidosis, Australia. Emerg. Infect. Dis. 9, 1538-1542. https://doi.org/10.3201/eid0912.020750
  9. Dance, D. A. (2000) Ecology of Burkholderia pseudomallei and the interactions between environmental Burkholderia spp. and human-animal hosts. Acta Trop. 74, 159-168. https://doi.org/10.1016/S0001-706X(99)00066-2
  10. Eoin West, T., Frevert, C. W., Denny Liggtt, H., and Skerrett, S. J. (2008) Inhalation of Burkholderia thailandensis results in lethal necrotizing pneumonia in mice: A surrogate model for pneumonic melioidosis. Trans. R. Soc. Trop. Med. Hyg. 102, S119-S126. https://doi.org/10.1016/S0035-9203(08)70028-2
  11. Feng, S., Zeng, W., Luo, F., Zhao, J., Yang, Z., and Sun, Q. (2010) Antibacterial activity of organic acids in aqueous extracts from pine needles (Pinus massoniana Lamb.). Food Sci. Biotechnol. 19, 35-41. https://doi.org/10.1007/s10068-010-0005-2
  12. Fosse, J., Seegers, H., and Magras, C. (2008) Foodborne zoonoses due to meat: A quantitative approach for a comparative risk assessment applied to pig slaughtering in Europe. Vet. Res. 39, 01. https://doi.org/10.1051/vetres:2007039
  13. Glass, K. A. and Doyle, M. P. (1989) Fate of Listeria monocytogenes in processed meat products during refrigerated storage. Appl. Environ. Microbiol. 55, 1565-1569.
  14. Haraga, A, West, T. E., Brittnacher, M. J, Skerrett, S. J., and Miller, S. I. (2008) Burkholderia thailandensis as a model system for the study of the virulence-associated type III secretion system of Burkholderia pseudomallei. Infect. Immun. 76, 5402-5411. https://doi.org/10.1128/IAI.00626-08
  15. Idris, A., Rachmat, A. F. N., and Ali, S. M. N. (1998) Melioidosis: A case of sheep to human transmission. J. Vet. Malaysia 10, 77-79.
  16. Inglis, T. J., Garrow, S. C, Adams, C., Henderson, M., and Mayo, M. (1998) Dry season outbreak of melioidosis in Western Australia. Lancet 352, 1600.
  17. Jitprasutwit, S., Thaewpia, W., Muangsombut, V., Lulitanond, A., Leelayuwat, C., Lertmemongkolchai, G., and Korbsrisate, S. (2010) Effect of acidic pH on the invasion efficiency and the type III secretion system of Burkholderia thailandensis. J. Microbiol. 48, 526-532. https://doi.org/10.1007/s12275-010-0078-x
  18. Ketterer, P. J., Donald, B., and Rogers, R. J. (1975) Bovine melioidosis in south-eastern Queensland. Aust. Vet. J. 51, 395-398. https://doi.org/10.1111/j.1751-0813.1975.tb15607.x
  19. Li, L., Lu, Z., and Han, O. (1994) Epidemiology of melioidosis in China. Zhonghua Liu. Xing. Bing. Xue. Za. Zhi. 15, 292-295.
  20. Mbandi E. and Shelef, L. A. (2002) Enhanced antimicrobial effects of combination of lactate and diacetate on Listeria monocytogenes and Salmonella spp. in beef bologna. Int. J. Food Microbiol. 76, 191-198. https://doi.org/10.1016/S0168-1605(02)00026-0
  21. Mukherjee, A., Yoon, Y., Belk, K. B., Scanga, J. A., Smith, G. C., and Sofos, J. N. (2008) Thermal inactivation of Escherichia coli O157:H7 in beef treated with marination and tenderization ingredients. J. Food Prot. 71, 1349-1356.
  22. Mukherjee, A., Yoon, Y., Geornaras, I., Belk, K. E., Scanga, J. A, Smith, G. C., and Sofos, J. N. (2009) Effect of meat binding formulations on thermal inactivation of Escherichia coli O157:H7 internalized in beef. J. Food Sci. 74, M94-M99. https://doi.org/10.1111/j.1750-3841.2008.01035.x
  23. Qazi, O., Prior, J. L., Judy, B. M., Whitlock, G. C., Barrie Kitto, G., Torres, A. G., Estes, D. M., and Brown, K. A. (2008) Sero-characterization of lipopolysaccharide from Burkholderia thailandensis. Trans. R. Soc. Trop. Med. Hyg. 102, S58-S60. https://doi.org/10.1016/S0035-9203(08)70016-6
  24. Ralph, A., McBride, J., and Currie, B. J. (2004) Transmission of Burkholderia pseudomallei via breast milk in northern Australia. Pediatr. Infect. Dis. J. 12, 1169-1171.
  25. Reckseidler, S. L., DeShazer, D., Sokol, P. A., and Woods, D. E. (2001) Detection of bacterial virulence genes by subtractive hybridization: identification of capsular polysaccharide of Burkholderia pseudomallei as a major virulence determinant. Infect. Immun. 69, 34-44. https://doi.org/10.1128/IAI.69.1.34-44.2001
  26. Sprague, L. D. and Neubauer, H. (2004) Melioidosis in animals: A review on epizootiology, diagnosis and clinical presentation. J. Vet. Med. 51, 305-320. https://doi.org/10.1111/j.1439-0450.2004.00797.x
  27. Thongdee, M., Gallagher, L. A., Schell, M., Dharakul, T., Songsivilai, S., and Manoil, C. (2008) Targeted mutagenesis of Burkholderia thailandensis and Burkholderia pseudomallei through natural transformation of PCR fragments. Appl. Environ. Microbiol. 74, 2985-2989. https://doi.org/10.1128/AEM.00030-08
  28. West, T. E., Frevert, C. W., Liggitt, H. E., and Skerrett, S. J. (2008) Inhalation of Burkholderia thailandensis results in lethal necrotizing pneumonia in mice: a surrogate model for pneumonic melioidosis. Trans. R. Soc. Trop. Med. Hyg. 102, S119-S126. https://doi.org/10.1016/S0035-9203(08)70028-2
  29. Wuthiekanun. V., Smith, M. D., Dance, D. A., Walsh, A. L., Pitt, T. L., and White, N. J. (1996) Biochemical characteristics of clinical and environmental isolates of Burkholderia pseudomallei. J. Med. Microbiol. 45, 408-412. https://doi.org/10.1099/00222615-45-6-408
  30. Yoon, Y., Calicioglu, M., Kendall, P. A., Smith, G. C., and Sofos, J. N. (2005) Influence of inoculum level and acidic marination on inactivation of Escherichia coli O157:H7 during drying and storage of beef jerky. Food Microbiol. 22, 423-431. https://doi.org/10.1016/j.fm.2004.09.012
  31. Yoon, Y. and Choi, K. H. (2010) Antimicrobial activity of oleanolic acid on Listeria monocytogenes under sublethal stresses of NaCl and pH. Korean J. Food Sci. Ani. Resour. 30, 717-721. https://doi.org/10.5851/kosfa.2010.30.5.717
  32. Yoon, Y., Kim, J. H., Byun, M. W., Choi, K. H., and Lee, J. W. (2010) Effect of gamma irradiation on Burkholderia thailandensis (Burkholderia pseudomallei surrogate) survival under combinations of pH and NaCl. Rad. Phys. Chem. 79, 545-548. https://doi.org/10.1016/j.radphyschem.2009.12.004
  33. Yoon. Y., Mukherjee. A., Belk. K. E., Scanga. J. A., Smith. G. C., and Sofos. J. N. (2009) Effect of tenderizers combined with organic acids on Escherichia coli O157:H7 Thermal resistance in non-intact beef. Int. J. Food Microbiol. 133, 78-85. https://doi.org/10.1016/j.ijfoodmicro.2009.05.004
  34. Yu, Y., Kim, H. S., Chua, H. H., Lin, C. H., Sim, S. H., Lin, D., Derr, A., Engels, R., DeShazer, D., Birren, B., Nierman, W. C., and Tan, P. (2006) Genomic patterns of pathogen evolution revealed by comparison of Burkholderia pseudomallei, the causative agent of melioidosis, to avirulent Burkholderia thailandensis. BMC Microbiol. 6, 46. https://doi.org/10.1186/1471-2180-6-46
  35. Zinchenko, O. V., Antonov, V. A., Tkachenko, G. A., Altukhova, V. V., Zamaraev, V. S., Piven, N. N., Goloseev, A., Vasilev, V. P., Lomova, L. V., and Alekseev, V. V. (2008) Comparative assessment of DNA extraction methods for identification of glanders and melioidosis etiological agents by PCR. Zh. Microbiol. Epidemiol. Immunobiol. 1, 55-60.