Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
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Effect of Oral Administration of Korean Red Ginseng on Influenza A (H1N1) Virus Infection

  • Received : 2010.11.26
  • Accepted : 2010.12.10
  • Published : 2011.03.29
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Abstract

Korean red ginseng (RG), which is a ginseng treated by heating and steaming, has biological activity similar to Panax ginseng. The effect of ginseng on influenza infection has not been studied although it is known to have a broad range of biological activities. The aim of the study is to investigate the effect of RG extract on influenza A (H1N1) virus infection. We investigated the inhibitory effect of RG extract on plaque formation by influenza A virus in a cell-based plaque assay, and the effect of orally administered RG on influenza A virus infection in mice. RG extract, which was applied at a non-cytotoxic concentration, inhibited plaque formation by influenza A virus in the cell-based plaque assay. The orally administered RG extract ameliorated body weight loss and significantly increased survival in mice infected with influenza A virus. Our results suggest that RG extract has components that reduce the severity of infection by influenza A virus and could potentially be used as a complement to treatment of influenza A virus infections.

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References

  1. Coleman CI, Hebert JH, Reddy P. The effects of Panax ginseng on quality of life. J Clin Pharm Ther 2003;28:5-15. https://doi.org/10.1046/j.1365-2710.2003.00467.x
  2. Kim MH, Hong HD, Kim YC, Rhee YK, Kim KT, Rho J. Ginsenoside changes in red ginseng manufactured by acid impregnation treatment. J Ginseng Res 2010;34:93-97. https://doi.org/10.5142/jgr.2010.34.2.093
  3. Block KI, Mead MN. Immune system effects of echinacea, ginseng, and astragalus: a review. Integr Cancer Ther 2003;2:247-267. https://doi.org/10.1177/1534735403256419
  4. Keum YS, Park KK, Lee JM, Chun KS, Park JH, Lee SK, Kwon H, Surh YJ. Antioxidant and anti-tumor promoting activities of the methanol extract of heat-processed ginseng. Cancer Lett 2000;150:41-48. https://doi.org/10.1016/S0304-3835(99)00369-9
  5. Kaneko H, Nakanishi K. Proof of the mysterious effi cacy of ginseng: basic and clinical trials: clinical effects of medical ginseng, korean red ginseng: specifically, its anti-stress action for prevention of disease. J Pharmacol Sci 2004;95:158-162. https://doi.org/10.1254/jphs.FMJ04001X5
  6. Sung H, Jung YS, Cho YK. Benefi cial effects of a combination of Korean red ginseng and highly active antiretroviral therapy in human immunodefi ciency virus type 1-infected patients. Clin Vaccine Immunol 2009;16:1127-1131. https://doi.org/10.1128/CVI.00013-09
  7. Hu S, Concha C, Johannisson A, Meglia G, Waller KP. Effect of subcutaneous injection of ginseng on cows with subclinical Staphylococcus aureus mastitis. J Vet Med B Infect Dis Vet Public Health 2001;48:519-528. https://doi.org/10.1046/j.1439-0450.2001.00470.x
  8. Lee YS, Chung IS, Lee IR, Kim KH, Hong WS, Yun YS. Activation of multiple effector pathways of immune system by the antineoplastic immunostimulator acidic polysaccharide ginsan isolated from Panax ginseng. Anticancer Res 1997;17:323-331.
  9. Luo YM, Cheng XJ, Yuan WX. Effects of ginseng root saponins and ginsenoside Rb1 on immunity in cold water swim stress mice and rats. Zhongguo Yao Li Xue Bao 1993;14:401-404.
  10. Sumiyoshi M, Sakanaka M, Kimura Y. Effects of red ginseng extract on allergic reactions to food in Balb/c mice. J Ethnopharmacol 2010;132:206-212. https://doi.org/10.1016/j.jep.2010.08.012
  11. Roxas M, Jurenka J. Colds and influenza: a review of diagnosis and conventional, botanical, and nutritional considerations. Altern Med Rev 2007;12:25-48.
  12. Klenk E, Faillard H, Lempfrid H. Enzymatic effect of the infl uenza virus. Hoppe Seylers Z Physiol Chem 1955;301:235-246. https://doi.org/10.1515/bchm2.1955.301.1-2.235
  13. Cox RJ, Brokstad KA, Ogra P. Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated infl uenza vaccines. Scand J Immunol 2004;59:1-15. https://doi.org/10.1111/j.0300-9475.2004.01382.x
  14. Johnson NP, Mueller J. Updating the accounts: global mortality of the 1918-1920 “Spanish” influenza pandemic. Bull Hist Med 2002;76:105-115. https://doi.org/10.1353/bhm.2002.0022
  15. World Health Organization. Situation updates: pandemic (H1N1) 2009. Available from: http://www.who.int/csr/disease/swineflu/updates/en/.
  16. Bearman GM, Shankaran S, Elam K. Treatment of severe cases of pandemic (H1N1) 2009 infl uenza: review of antivirals and adjuvant therapy. Recent Pat Antiinfect Drug Discov 2010;5:152-156.
  17. Predy GN, Goel V, Lovlin R, Donner A, Stitt L, Basu TK. Efficacy of an extract of North American ginseng containing poly-furanosyl-pyranosyl-saccharides for preventing upper respiratory tract infections: a randomized controlled trial. CMAJ 2005;173:1043-1048. https://doi.org/10.1503/cmaj.1041470
  18. Varkey JB, Varkey B. Viral infections in patients with chronic obstructive pulmonary disease. Curr Opin Pulm Med 2008;14:89-94. https://doi.org/10.1097/MCP.0b013e3282f4a99f
  19. Morimoto K, Nakakariya M, Shirasaka Y, Kakinuma C, Fujita T, Tamai I, Ogihara T. Oseltamivir (Tamiflu) efflux transport at the blood-brain barrier via P-glycoprotein. Drug Metab Dispos 2008;36:6-9.
  20. Reed LJ, Muench H. A simple method of estimating fifty percent endpoints. Am J Hyg 1938;27:493-497.
  21. Fotakis G, Timbrell JA. In vitro cytotoxicity assays: comparison of LDH, neutral red, MTT and protein assay in hepatoma cell lines following exposure to cadmium chloride. Toxicol Lett 2006;160:171-177. https://doi.org/10.1016/j.toxlet.2005.07.001
  22. Hayden FG, Cote KM, Douglas RG Jr. Plaque inhibition assay for drug susceptibility testing of influenza viruses. Antimicrob Agents Chemother 1980;17:865-870. https://doi.org/10.1128/AAC.17.5.865
  23. Saad WA, de Arruda Camargo LA, Simoes S, Saad WA, Guarda RS, Guarda IF. Moxonidine and rilmenidine injected into the medial septal area reduces the salivation induced by pilocarpine. Auton Neurosci 2004;112:31-36. https://doi.org/10.1016/j.autneu.2004.04.001
  24. Yen HL, Monto AS, Webster RG, Govorkova EA. Virulence may determine the necessary duration and dosage of oseltamivir treatment for highly pathogenic A/Vietnam/1203/04 influenza virus in mice. J Infect Dis 2005;192:665-672. https://doi.org/10.1086/432008
  25. Sidwell RW, Huffman JH, Call EW, Alaghamandan H, Cook PD, Robins RK. Effect of selenazofurin on infl uenza A and B virus infections of mice. Antiviral Res 1986;6:343-353. https://doi.org/10.1016/0166-3542(86)90016-1
  26. Sidwell RW, Huffman JH, Barnard DL, Bailey KW, Wong MH, Morrison A, Syndergaard T, Kim CU. Inhibition of influenza virus infections in mice by GS4104, an orally effective infl uenza virus neuraminidase inhibitor. Antiviral Res 1998;37:107-120. https://doi.org/10.1016/S0166-3542(97)00065-X
  27. Kiso M, Kubo S, Ozawa M, Le QM, Nidom CA, Yamashita M, Kawaoka Y. Efficacy of the new neuraminidase inhibitor CS-8958 against H5N1 influenza viruses. PLoS Pathog 2010;6:e1000786. https://doi.org/10.1371/journal.ppat.1000786
  28. Taubenberger JK, Morens DM. The pathology of influenza virus infections. Annu Rev Pathol 2008;3:499-522. https://doi.org/10.1146/annurev.pathmechdis.3.121806.154316
  29. Barnard DL. Animal models for the study of influenza pathogenesis and therapy. Antiviral Res 2009;82:A110-A122. https://doi.org/10.1016/j.antiviral.2008.12.014
  30. Cilloniz C, Pantin-Jackwood MJ, Ni C, Goodman AG, Peng X, Proll SC, Carter VS, Rosenzweig ER, Szretter KJ, Katz JM, et al. Lethal dissemination of H5N1 infl uenza virus is associated with dysregulation of infl ammation and lipoxin signaling in a mouse model of infection. J Virol 2010;84:7613-7624. https://doi.org/10.1128/JVI.00553-10
  31. Kobasa D, Jones SM, Shinya K, Kash JC, Copps J, Ebihara H, Hatta Y, Kim JH, Halfmann P, Hatta M, et al. Aberrant innate immune response in lethal infection of macaques with the 1918 influenza virus. Nature 2007;445:319-323. https://doi.org/10.1038/nature05495
  32. Yeung HW, Cheung K, Leung KN. Immunopharmacology of Chinese medicine 1, ginseng induced immunosuppression in virus-infected mice. Am J Chin Med 1982;10:44-54. https://doi.org/10.1142/S0192415X82000087
  33. Biondo PD, Goruk S, Ruth MR, O’Connell E, Field CJ. Effect of CVT-E002 (COLD-fX) versus a ginsenoside extract on systemic and gut-associated immune function. Int Immunopharmacol 2008;8:1134-1142. https://doi.org/10.1016/j.intimp.2008.04.003
  34. Steinhauer DA, Domingo E, Holland JJ. Lack of evidence for proofreading mechanisms associated with an RNA virus polymerase. Gene 1992;122:281-288. https://doi.org/10.1016/0378-1119(92)90216-C
  35. Moscona A. Global transmission of oseltamivir-resistant influenza. N Engl J Med 2009;360:953-956. https://doi.org/10.1056/NEJMp0900648
  36. Hatakeyama S. Drug-resistant infl uenza viruses: an overview. Nippon Rinsho 2010;68:1671-1678.
  37. Centers for Disease Control and Prevention. 2008-2009 influenza season week 35 ending September 5, 2009. Available from: http://www.cdc.gov/flu/weekly/pdf/External_F0935.pdf.
  38. Intharathep P, Laohpongspaisan C, Rungrotmongkol T, Loisruangsin A, Malaisree M, Decha P, Aruksakunwong O, Chuenpennit K, Kaiyawet N, Sompornpisut P, et al. How amantadine and rimantadine inhibit proton transport in the M2 protein channel. J Mol Graph Model 2008;27:342-348. https://doi.org/10.1016/j.jmgm.2008.06.002
  39. Moscona A. Neuraminidase inhibitors for influenza. N Engl J Med 2005;353:1363-1373. https://doi.org/10.1056/NEJMra050740

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