Ganoderma lucidum Spore: The Reason Why Its Wall Should be Broken for Medicinal Use
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May 15, 2018
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Abstract
Ganoderma lucidum, commonly known as reishi or lingzhi mushroom, is regarded as a precious highvalue medicinal herb. It can stimulate the immune system in cancer patients. It is used to relieve pain, protect against nerve degeneration, reduce blood sugar and cholesterol, and it shows anti-oxidative and anti-inflammatory activites. The active substances are polysaccharides and triterpenes which are found in the spores. Broken spores contain more active compounds and are more active than unbroken spores because of their thick two-layer walls. The result of this study showed that alcohol and dichloromethane did not extract the triterpenes from unbroken spores. Moreover, boiling unbroken spores in water can extract some polysaccharides but their quantity is less than that of broken spores. Furthermore, the acid or alkaline condition which simulates gastric or intestinal conditions, respectively, is not able to break the spore wall as proven by electron microscopic examination, TLC chromatograms, or active substances analysis. Therefore, broken spores should be used as a medicinal product for oral administration in order to achieve higher amounts of the active principles, better gastrointestinal absorption and hence better therapeutic value.
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1.ชยันต์ พิเชียรสุนทร. เห็ดหลินจือกับฤทธิ์ทางเภสัชวิทยา. บทความบรรยายในการประชุมวิชาการวิทยาศาสตร์สุขภาพ ครั้งที่ ๑๕. วันที่ ๑๗ กรกฎาคม ๒๕๔๐ ณ อาคารรวมวิจัยและบัณฑิตศึกษา, มหาวิทยาลัยเชียงใหม่, จังหวัดเชียงใหม่; ๒๕๔๐.
2. Gao Y, Tang W, Dai X, Gao H, Chen G, Ye J, et al. Effects of watersoluble Ganoderma lucidum polysaccharides on the immune functions of patients with advanced lung cancer. J Med Food 2005;8:159-68.
3. Chen X, Hu ZP, Yang XX, Huang M, Gao Y, Tang W, et al. Monitoring of immune responses to a herbal immuno-modulator in patients with advanced colorectal cancer. Int Immunopharmacol 2006;6:499-508.
4. Gao Y, Zhou S, Jiang W, Huang M, Dai X. Effects of ganopoly (a Ganoderma lucidum polysaccharide extract) on the immune functions in advanced-stage cancer patients. Immunol Invest 2003;32:201-15.
5. Li EK, Tam LS, Wong CK, Li WC, Lam CW, Wachtel-Galor S, et al. Safety and efficacy of Ganoderma lucidum (lingzhi) and San Miao San supplementation in patients with rheumatoid arthritis: a double-blind, randomized, placebo-controlled pilot trial. Arthritis Rheum 2007;57: 1143-50.
6. Tang W, Gao Y, Chen G, Gao H, Dai X, Ye J, et al. A randomized, double-blind and placebo-controlled study of a Ganoderma lucidum polysaccharide extract in neurasthenia. J Med Food 2005;8:53-8.
7. Noguchi M, Kakuma T, Tomiyasu K, Kurita Y, Kukihara H, Konishi F, et al. Effect of an extract of Ganoderma lucidum in men with lower urinary tract symptoms: a double-blind, placebo-controlled randomized and dose-ranging study. Asian J Androl 2008;10:651-8.
8. Noguchi M, Kakuma T, Tomiyasu K, Yamada A, Itoh K, Konishi F, et al. Randomized clinical trial of an ethanol extract of Ganoderma lucidum in men with lower urinary tract symptoms. Asian J Androl 2008;10:777-85.
9. Hijikata Y, Yasuhara A, Sahashi Y. Effect of an herbal formula containing Ganoderma lucidum on reduction of herpes zoster pain: a pilot clinical trial. Am J Chin Med 2005;33:517-23.
10. Lin ZB, Zhang HN. Anti-tumor and immunoregulatory activities of Ganoderma lucidum and its possible mechanisms. Acta Pharmacol Sin 2004;25:1387-95.
11. Nonaka Y, Shibata H, Nakai M, Kurihara H, Ishibashi H, Kiso Y, et al. Anti-tumor activities of the antlered form of Ganoderma lucidum in allogeneic and syngeneic tumor-bearing mice. Biosci Biotechnol Biochem 2006;70:2028-34.
12. Zhu XL, Chen AF, Lin ZB. Ganoderma lucidum polysaccharides enhance the function of immunological effector cells in immunosuppressed mice. J Ethnopharmacol 2007;111:219-26.
13. Ma C, Guan SH, Yang M, Liu X, Guo DA. Differential protein expression in mouse splenic mononuclear cells treated with polysaccharides from spores of Ganoderma lucidum. Phytomedicine 2008;15:268-76.
14. Cheng KC, Huang HC, Chen JH, Hsu JW, Cheng HC, Ou CH, et al. Ganoderma lucidum polysaccharides in human monocytic leukemia cells: from gene expression to network construction. BMC Genomics 2007;8:411.
15. Gao Y, Gao H, Chan E, Tang W, Xu A, Yang H, et al. Antitumor activity and underlying mechanisms of ganopoly, the refined polysaccharides extracted from Ganoderma lucidum, in mice. Immunol Invest 2005;34:171-98.
16. Li YB, Wang R, Wu HL, Li YH, Zhong LJ, Yu HM, et al. Serum amyloid A mediates the inhibitory effect of Ganoderma lucidum polysaccharides on tumor cell adhesion to endothelial cells. Oncol Rep 2008;20:549-56.
17. Zhao HB, Lin SQ, Liu JH, Lin ZB. Polysaccharide extract isolated from Ganoderma lucidum protects rat cerebral cortical neurons from hypoxia/reoxygenation injury. J Pharmacol Sci 2004;95:294-8.
18. Zhu WW, Liu ZL, Xu HW, Chu WZ, Ye QY, et al. Effect of the oil from Ganoderma lucidum spores on pathological changes in the substantia nigra and behaviors of MPTP-treated mice. Di Yi Jun Yi Da Xue Xue Bao 2005;25:667-71.
19. Chen LW, Wang YQ, Wei LC, Shi M, Chan YS. Chinese herbs and herbal extracts for neuroprotection of dopaminergic neurons and potential therapeutic treatment of Parkinsonûs disease. CNS Neurol Disord Drug Targets 2007;6:273-81.
20. Fatmawati S, Kurashiki K, Takeno S, Kim YU, Shimizu K, Sato M, etal. The inhibitory effect on aldose reductase by an extract of Ganoderma lucidum. Phytother Res 2009;23:28-32.
21. Seto SW, Lam TY, Tam HL, Au AL, Chan SW, Wu JH, et al. Novel hypoglycemic effects of Ganoderma lucidum water-extract in obese/diabetic (+db/+db) mice. Phytomedicine 2008; Dec 22 [Epub ahead of print].
22. Zhang HN, Lin ZB. Hypoglycemic effect of Ganoderma lucidum polysaccharides. Acta Pharmacol Sin 2004;25:191-5.
23. Chen WQ, Luo SH, Ll HZ, Yang H. Effects of Ganoderma lucidum polysaccharides on serum lipids and lipoperoxidation in experimental hyperlipidemic rats. Zhongguo Zhong Yao Za Zhi 2005;30:1358-60.
24. Berger A, Rein D, Kratky E, Monnard I, Hajjaj H, Meirim I, et al. Cholesterol-lowering properties of Ganoderma lucidum in vitro, exvivo, and in hamsters and minipigs. Lipids Health Dis 2004;3:2-12.
25. Wang SQ, Qin WB, Kang YM, Ma XR, Liu L, Liu JX, et al. Intervention effect of Ganoderma lucidum spores on the changes of XOD, MPO and SDH in the testis tissue of NIDDM rats. Zhonghua Nan Ke Xue 2008;14:792-5.
26. Wu Y, Wang D. A new class of natural glycopeptides with sugar moiety-dependent antioxidant activities derived from Ganoderma lucidum fruiting bodies. J Proteome Res 2009;8:436-42.
27. You YH, Lin ZB. Antioxidant effect of Ganoderma polysaccharide peptide. Yao Xue Xue Bao 2003;38:85-8.
28. Ko HH, Hung CF, Wang JP, Lin CN. Antiinflammatory triterpenoids and steroids from Ganoderma lucidum and G. tsugae. Phytochemistry 2008;69:234-9.
29. Ho YW, Yeung JS, Chiu PK, Tang WM, Lin ZB, Man RY, et al. Ganoderma lucidum polysaccharide peptide reduced the production of proinflammatory cytokines in activated rheumatoid synovial fibroblast. Mol Cell Biochem 2007;301:173-9.
30. Akihisa T, Nakamura Y, Tagata M, Tokuda H, Yasukawa K, Uchiyama E, et al. Anti-inflammatory and anti-tumor-promoting effects of triterpene acids and sterols from the fungus Ganoderma lucidum. Chem Biodivers 2007;4:224-31.
31. Miyamoto I, Liu J, Shimizu K, Sato M, Kukita A, Kukita T, et al. Regulation of osteoclastogenesis by ganoderic acid DM isolated from Ganoderma lucidum. Eur J Pharmacol 2009;602:1-7.
32. Yue QX, Cao ZW, Guan SH, Liu XH, Tao L, Wu WY, et al. Proteomic characterization of the cytotoxic mechanism of ganoderic acid D and computer automated estimation of the possible drug-target network. Mol Cell Proteomics 2008;7:949-61.
33. Wang X, Liu R, Sun J, Guan S, Yang M, Bi K, et al. HPLC method for the determination and pharmacokinetic studies of four triterpenoids in rat plasma after oral administration of Ganoderma lucidum extract. Biomed Chromatogr 2007;21:389-96.
34. Zhang CR, Yang SP, Yue JM. Sterols and triterpenoids from the spores of Ganoderma lucidum. Nat Prod Res 2008;22:1137-42.
35. Zhang XQ, Pang GL, Cheng Y, Wang Y, Ye WC. Chemical constituents of the spores of Ganoderma lucidum. Zhong Yao Cai 2008;31:41-4.
36. Yuan JP, Wang JH, Liu X. Distribution of free and esterified ergosterols in the medicinal fungus Ganoderma lucidum. Appl Microbiol Biotechnol 2007;77:159-65.
37. Fukuzawa M, Yamaguchi R, Hide I, Chen Z, Hirai Y, Sugimoto A, etal. Possible involvement of long chain fatty acids in the spores of Ganoderma lucidum (Reishi Houshi) to its anti-tumor activity. Biol Pharm Bull 2008;31:1933-7.
38. Tong MH, Chien PJ, Chang HH, Tsai MJ, Sheu F. High processing tolerances of immunomodulatory proteins in Enoki and Reishi mushrooms. J Agric Food Chem 2008;56:3160-6.
39. Shi Y, Sun J, He H, Guo H, Zhang S. Hepatoprotective effects of Ganoderma lucidum peptides against D-galactosamine-induced liver injury in mice. J Ethnopharmacol 2008;117:415-9.
40. Wang HX, Ng TB. A laccase from the medicinal mushroom Ganoderma lucidum. Appl Microbiol Biotechnol 2006;72:508-13.
41. Wang H, Ng TB. Ganodermin, an antifungal protein from fruiting bodies of the medicinal mushroom Ganoderma lucidum. Peptides 2006;27:27-30.
42. Gao JJ, Nakamura N, Min BS, Hirakawa A, Zuo F, Hattori M. Quantitative determination of bitter principles in specimens of Ganoderma lucidum using high-performance liquid chromatography and its application to the evaluation of ganoderma products. Chem Pharm Bull 2004;52:688-95.
43. Yue GG, Fung KP, Leung PC, Lau CB. Comparative studies on the immunomodulatory and antitumor activities of the different parts of fruiting body of Ganoderma lucidum and Ganoderma spores. Phytother Res 2008;22:1282-91.
44. Yuen JW, Gohel MD. The dual roles of Ganoderma antioxidants on urothelial cell DNA under carcinogenic attack. J Ethnopharmacol 2008;118:324-30.
45. Wang PY, Wang SZ, Lin SQ, Lin ZB. Comparison of the immunomodulatory effects of spore polysaccharides and broken spore polysaccharides isolated from Ganoderma lucidum on murine splenic lymphocytes and peritoneal macrophages in vitro. Beijing Da Xue Xue Bao 2005;37:569-74.
46. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem 1956;28:350-6.
47. Blumenkrantz N, Asboe-Hansen G. New method for quantitative determination of uronic acid. Anal Biochem 1973;54:484-9.
48. Chen YXM, Gong XF. Microwave-assisted extraction used for the isolation of total triterpenoid saponins from Ganoderma atrum. J Food Eng 2007;81:162-70.
49. The United States Pharmacopeia 29/ The National Formulary 24. MD: The United States Pharmacopeial Convention; 2006.
50. ดาราวรรณ วนะชิวนาวิน, อนงค์ เพียรกิจกรรม, อังคณา ฉายประเสริฐ, พันธ์พบ เลิศฉายต่วน, อัญชลี ตั้งตรงจิตร, พิสิฏธ์ ชินบุตร. Ganoderma lucidum: a cause of pseudoparasitosis. Southeast Asian J Trop Med Public Health 2006;37:1099-102.
2. Gao Y, Tang W, Dai X, Gao H, Chen G, Ye J, et al. Effects of watersoluble Ganoderma lucidum polysaccharides on the immune functions of patients with advanced lung cancer. J Med Food 2005;8:159-68.
3. Chen X, Hu ZP, Yang XX, Huang M, Gao Y, Tang W, et al. Monitoring of immune responses to a herbal immuno-modulator in patients with advanced colorectal cancer. Int Immunopharmacol 2006;6:499-508.
4. Gao Y, Zhou S, Jiang W, Huang M, Dai X. Effects of ganopoly (a Ganoderma lucidum polysaccharide extract) on the immune functions in advanced-stage cancer patients. Immunol Invest 2003;32:201-15.
5. Li EK, Tam LS, Wong CK, Li WC, Lam CW, Wachtel-Galor S, et al. Safety and efficacy of Ganoderma lucidum (lingzhi) and San Miao San supplementation in patients with rheumatoid arthritis: a double-blind, randomized, placebo-controlled pilot trial. Arthritis Rheum 2007;57: 1143-50.
6. Tang W, Gao Y, Chen G, Gao H, Dai X, Ye J, et al. A randomized, double-blind and placebo-controlled study of a Ganoderma lucidum polysaccharide extract in neurasthenia. J Med Food 2005;8:53-8.
7. Noguchi M, Kakuma T, Tomiyasu K, Kurita Y, Kukihara H, Konishi F, et al. Effect of an extract of Ganoderma lucidum in men with lower urinary tract symptoms: a double-blind, placebo-controlled randomized and dose-ranging study. Asian J Androl 2008;10:651-8.
8. Noguchi M, Kakuma T, Tomiyasu K, Yamada A, Itoh K, Konishi F, et al. Randomized clinical trial of an ethanol extract of Ganoderma lucidum in men with lower urinary tract symptoms. Asian J Androl 2008;10:777-85.
9. Hijikata Y, Yasuhara A, Sahashi Y. Effect of an herbal formula containing Ganoderma lucidum on reduction of herpes zoster pain: a pilot clinical trial. Am J Chin Med 2005;33:517-23.
10. Lin ZB, Zhang HN. Anti-tumor and immunoregulatory activities of Ganoderma lucidum and its possible mechanisms. Acta Pharmacol Sin 2004;25:1387-95.
11. Nonaka Y, Shibata H, Nakai M, Kurihara H, Ishibashi H, Kiso Y, et al. Anti-tumor activities of the antlered form of Ganoderma lucidum in allogeneic and syngeneic tumor-bearing mice. Biosci Biotechnol Biochem 2006;70:2028-34.
12. Zhu XL, Chen AF, Lin ZB. Ganoderma lucidum polysaccharides enhance the function of immunological effector cells in immunosuppressed mice. J Ethnopharmacol 2007;111:219-26.
13. Ma C, Guan SH, Yang M, Liu X, Guo DA. Differential protein expression in mouse splenic mononuclear cells treated with polysaccharides from spores of Ganoderma lucidum. Phytomedicine 2008;15:268-76.
14. Cheng KC, Huang HC, Chen JH, Hsu JW, Cheng HC, Ou CH, et al. Ganoderma lucidum polysaccharides in human monocytic leukemia cells: from gene expression to network construction. BMC Genomics 2007;8:411.
15. Gao Y, Gao H, Chan E, Tang W, Xu A, Yang H, et al. Antitumor activity and underlying mechanisms of ganopoly, the refined polysaccharides extracted from Ganoderma lucidum, in mice. Immunol Invest 2005;34:171-98.
16. Li YB, Wang R, Wu HL, Li YH, Zhong LJ, Yu HM, et al. Serum amyloid A mediates the inhibitory effect of Ganoderma lucidum polysaccharides on tumor cell adhesion to endothelial cells. Oncol Rep 2008;20:549-56.
17. Zhao HB, Lin SQ, Liu JH, Lin ZB. Polysaccharide extract isolated from Ganoderma lucidum protects rat cerebral cortical neurons from hypoxia/reoxygenation injury. J Pharmacol Sci 2004;95:294-8.
18. Zhu WW, Liu ZL, Xu HW, Chu WZ, Ye QY, et al. Effect of the oil from Ganoderma lucidum spores on pathological changes in the substantia nigra and behaviors of MPTP-treated mice. Di Yi Jun Yi Da Xue Xue Bao 2005;25:667-71.
19. Chen LW, Wang YQ, Wei LC, Shi M, Chan YS. Chinese herbs and herbal extracts for neuroprotection of dopaminergic neurons and potential therapeutic treatment of Parkinsonûs disease. CNS Neurol Disord Drug Targets 2007;6:273-81.
20. Fatmawati S, Kurashiki K, Takeno S, Kim YU, Shimizu K, Sato M, etal. The inhibitory effect on aldose reductase by an extract of Ganoderma lucidum. Phytother Res 2009;23:28-32.
21. Seto SW, Lam TY, Tam HL, Au AL, Chan SW, Wu JH, et al. Novel hypoglycemic effects of Ganoderma lucidum water-extract in obese/diabetic (+db/+db) mice. Phytomedicine 2008; Dec 22 [Epub ahead of print].
22. Zhang HN, Lin ZB. Hypoglycemic effect of Ganoderma lucidum polysaccharides. Acta Pharmacol Sin 2004;25:191-5.
23. Chen WQ, Luo SH, Ll HZ, Yang H. Effects of Ganoderma lucidum polysaccharides on serum lipids and lipoperoxidation in experimental hyperlipidemic rats. Zhongguo Zhong Yao Za Zhi 2005;30:1358-60.
24. Berger A, Rein D, Kratky E, Monnard I, Hajjaj H, Meirim I, et al. Cholesterol-lowering properties of Ganoderma lucidum in vitro, exvivo, and in hamsters and minipigs. Lipids Health Dis 2004;3:2-12.
25. Wang SQ, Qin WB, Kang YM, Ma XR, Liu L, Liu JX, et al. Intervention effect of Ganoderma lucidum spores on the changes of XOD, MPO and SDH in the testis tissue of NIDDM rats. Zhonghua Nan Ke Xue 2008;14:792-5.
26. Wu Y, Wang D. A new class of natural glycopeptides with sugar moiety-dependent antioxidant activities derived from Ganoderma lucidum fruiting bodies. J Proteome Res 2009;8:436-42.
27. You YH, Lin ZB. Antioxidant effect of Ganoderma polysaccharide peptide. Yao Xue Xue Bao 2003;38:85-8.
28. Ko HH, Hung CF, Wang JP, Lin CN. Antiinflammatory triterpenoids and steroids from Ganoderma lucidum and G. tsugae. Phytochemistry 2008;69:234-9.
29. Ho YW, Yeung JS, Chiu PK, Tang WM, Lin ZB, Man RY, et al. Ganoderma lucidum polysaccharide peptide reduced the production of proinflammatory cytokines in activated rheumatoid synovial fibroblast. Mol Cell Biochem 2007;301:173-9.
30. Akihisa T, Nakamura Y, Tagata M, Tokuda H, Yasukawa K, Uchiyama E, et al. Anti-inflammatory and anti-tumor-promoting effects of triterpene acids and sterols from the fungus Ganoderma lucidum. Chem Biodivers 2007;4:224-31.
31. Miyamoto I, Liu J, Shimizu K, Sato M, Kukita A, Kukita T, et al. Regulation of osteoclastogenesis by ganoderic acid DM isolated from Ganoderma lucidum. Eur J Pharmacol 2009;602:1-7.
32. Yue QX, Cao ZW, Guan SH, Liu XH, Tao L, Wu WY, et al. Proteomic characterization of the cytotoxic mechanism of ganoderic acid D and computer automated estimation of the possible drug-target network. Mol Cell Proteomics 2008;7:949-61.
33. Wang X, Liu R, Sun J, Guan S, Yang M, Bi K, et al. HPLC method for the determination and pharmacokinetic studies of four triterpenoids in rat plasma after oral administration of Ganoderma lucidum extract. Biomed Chromatogr 2007;21:389-96.
34. Zhang CR, Yang SP, Yue JM. Sterols and triterpenoids from the spores of Ganoderma lucidum. Nat Prod Res 2008;22:1137-42.
35. Zhang XQ, Pang GL, Cheng Y, Wang Y, Ye WC. Chemical constituents of the spores of Ganoderma lucidum. Zhong Yao Cai 2008;31:41-4.
36. Yuan JP, Wang JH, Liu X. Distribution of free and esterified ergosterols in the medicinal fungus Ganoderma lucidum. Appl Microbiol Biotechnol 2007;77:159-65.
37. Fukuzawa M, Yamaguchi R, Hide I, Chen Z, Hirai Y, Sugimoto A, etal. Possible involvement of long chain fatty acids in the spores of Ganoderma lucidum (Reishi Houshi) to its anti-tumor activity. Biol Pharm Bull 2008;31:1933-7.
38. Tong MH, Chien PJ, Chang HH, Tsai MJ, Sheu F. High processing tolerances of immunomodulatory proteins in Enoki and Reishi mushrooms. J Agric Food Chem 2008;56:3160-6.
39. Shi Y, Sun J, He H, Guo H, Zhang S. Hepatoprotective effects of Ganoderma lucidum peptides against D-galactosamine-induced liver injury in mice. J Ethnopharmacol 2008;117:415-9.
40. Wang HX, Ng TB. A laccase from the medicinal mushroom Ganoderma lucidum. Appl Microbiol Biotechnol 2006;72:508-13.
41. Wang H, Ng TB. Ganodermin, an antifungal protein from fruiting bodies of the medicinal mushroom Ganoderma lucidum. Peptides 2006;27:27-30.
42. Gao JJ, Nakamura N, Min BS, Hirakawa A, Zuo F, Hattori M. Quantitative determination of bitter principles in specimens of Ganoderma lucidum using high-performance liquid chromatography and its application to the evaluation of ganoderma products. Chem Pharm Bull 2004;52:688-95.
43. Yue GG, Fung KP, Leung PC, Lau CB. Comparative studies on the immunomodulatory and antitumor activities of the different parts of fruiting body of Ganoderma lucidum and Ganoderma spores. Phytother Res 2008;22:1282-91.
44. Yuen JW, Gohel MD. The dual roles of Ganoderma antioxidants on urothelial cell DNA under carcinogenic attack. J Ethnopharmacol 2008;118:324-30.
45. Wang PY, Wang SZ, Lin SQ, Lin ZB. Comparison of the immunomodulatory effects of spore polysaccharides and broken spore polysaccharides isolated from Ganoderma lucidum on murine splenic lymphocytes and peritoneal macrophages in vitro. Beijing Da Xue Xue Bao 2005;37:569-74.
46. Dubois M, Gilles KA, Hamilton JK, Rebers PA, Smith F. Colorimetric method for determination of sugars and related substances. Anal Chem 1956;28:350-6.
47. Blumenkrantz N, Asboe-Hansen G. New method for quantitative determination of uronic acid. Anal Biochem 1973;54:484-9.
48. Chen YXM, Gong XF. Microwave-assisted extraction used for the isolation of total triterpenoid saponins from Ganoderma atrum. J Food Eng 2007;81:162-70.
49. The United States Pharmacopeia 29/ The National Formulary 24. MD: The United States Pharmacopeial Convention; 2006.
50. ดาราวรรณ วนะชิวนาวิน, อนงค์ เพียรกิจกรรม, อังคณา ฉายประเสริฐ, พันธ์พบ เลิศฉายต่วน, อัญชลี ตั้งตรงจิตร, พิสิฏธ์ ชินบุตร. Ganoderma lucidum: a cause of pseudoparasitosis. Southeast Asian J Trop Med Public Health 2006;37:1099-102.