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30.03.2023

Medicinal Mushroom Supplements in Cancer: A Systematic Review of Clinical Studies

verfasst von: Santhosshi Narayanan, Aline Rozman de Mores, Lorenzo Cohen, Mohammed Moustapha Anwar, Felippe Lazar, Rachel Hicklen, Gabriel Lopez, Peiying Yang, Eduardo Bruera

Erschienen in: Current Oncology Reports | Ausgabe 6/2023

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Abstract

Purpose of Review

Patients seek clinical guidance on mushroom supplements that can be given alongside conventional treatments, but most research on such fungi has been preclinical. The current systematic review focused on clinical studies of mushrooms in cancer care conducted in the past 10 years. We searched Medline (Ovid), Embase (Ovid), Scopus (Wiley), and Cochrane Library to identify all mushroom studies conducted in humans published from January 2010 through December 2020. Two authors independently assessed papers for inclusion.

Recent Findings

Of 136 clinical studies identified by screening 2349, 39 met inclusion criteria. The studies included 12 different mushroom preparations. A survival benefit was reported using Huaier granules (Trametes robiniophila Murr) in 2 hepatocellular carcinoma studies and 1 breast cancer study. A survival benefit was also found in 4 gastric cancer studies using polysaccharide-K (polysaccharide-Kureha; PSK) in the adjuvant setting. Eleven studies reported a positive immunological response. Quality-of-life (QoL) improvement and/or reduced symptom burden was reported in 14 studies using various mushroom supplements. Most studies reported adverse effects of grade 2 or lower, mainly nausea, vomiting, diarrhea, and muscle pain. Limitations included small sample size and not using randomized controlled trial design.

Summary

Many of the reviewed studies were small and observational. Most showed favorable effects of mushroom supplements in reducing the toxicity of chemotherapy, improving QoL, favorable cytokine response, and possibly better clinical outcomes. Nevertheless, the evidence is inconclusive to recommend the routine use of mushrooms for cancer patients. More trials are needed to explore mushroom use during and after cancer treatment.

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Crawford K. National survey reveals surprising number of Americans believe alternative therapies can cure cancer. ASCO News Releases. 2018. https://www.asco.org/about-asco/press-center/news-releases/national-survey-reveals-surprising-number-americans-believe. Accessed August 24,2022.

Clarke TC, Black LI, Stussman BJ, Barnes PM, Nahin RL. Trends in the use of complementary health approaches among adults: United States, 2002–2012. Natl Health Stat Report. 2015;79:1–16.

Mao JJ, Palmer SC, Straton JB, et al. Cancer survivors with unmet needs were more likely to use complementary and alternative medicine. J Cancer Surviv. 2008;2:116–24.PubMedCrossRef

•• Ba DM, Ssentongo P, Beelman RB, Muscat J, Gao X, Richie JP. Higher mushroom consumption is associated with lower risk of cancer: a systematic review and meta-analysis of observational studies. Adv Nutr. 2021;12(5):1691–704. This recent systematic review showed that higher dietary mushroom lowers the risk of cancer, especially breast cancer.PubMedPubMedCentralCrossRef

Li J, Zou L, Chen W, et al. Dietary mushroom intake may reduce the risk of breast cancer: evidence from a meta-analysis of observational studies. PLoS One. 2014;9(4):e93437.PubMedPubMedCentralCrossRef

Lee DH, Yang M, Keum N, Giovannucci EL, Sun Q, Chavarro JE. Mushroom consumption and risk of total and site-specific cancer in two large U.S. prospective cohorts. Cancer Prev Res (Phila). 2019;12(8):517–26.PubMedCrossRef

Barbieri A, Quagliariello V, Del Vecchio V, et al. Anticancer and anti-inflammatory properties of Ganoderma lucidum extract effects on melanoma and triple-negative breast cancer treatment. Nutrients. 2017;9:210.PubMedPubMedCentralCrossRef

Wang W, Wang X, Li C, et al. Huaier suppresses breast cancer progression via linc00339/miR-4656/CSNK2B signaling pathway. Front Oncol. 2019;9:1195.PubMedPubMedCentralCrossRef

Seo H, Song J, Kim M, Han DW, Park HJ, Song M. Cordyceps militaris grown on germinated soybean suppresses kras-driven colorectal cancer by inhibiting the RAS/ERK pathway. Nutrients. 2018;11:20.PubMedPubMedCentralCrossRef

10.

Satria D, Amen Y, Niwa Y, Ashour A, Allam AE, Shimizu K. Lucidumol D, a new lanostane-type triterpene from fruiting bodies of Reishi (Ganoderma lingzhi). Nat Prod Res. 2019;33:189–95.PubMedCrossRef

11.

Hisamochi A, Kage M, Arinaga T, et al. Drug-induced liver injury associated with Agaricus blazei Murill which is very similar to autoimmune hepatitis. Clin J Gastroenterol. 2013;6:139–44.PubMedCrossRef

12.

Kikuchi Y, Seta K, Ogawa Y, et al. Chaga mushroom-induced oxalate nephropathy. Clin Nephrol. 2014;81:440–4.PubMedCrossRef

13.

• Loquai C, Dechent D, Garzarolli M, et al. Risk of interactions between complementary and alternative medicine and medication for comorbidities in patients with melanoma. Med Oncol. 2016;33:52. This study reported the elevated risk of interactions when natural products and supplements are used alongside conventional cancer treatment.PubMedCrossRef

14.

Loquai C, Schmidtmann I, Garzarolli M, et al. Interactions from complementary and alternative medicine in patients with melanoma. Melanoma Res. 2017;27(3):238–42.PubMedCrossRef

15.

Hanselin MR, Vande Griend JP, Linnebur SA. INR elevation with maitake extract in combination with warfarin. Ann Pharmacother. 2010;44:223–4.PubMedCrossRef

16.

103rd US Congress. Dietary Supplement Health and Education Act of 1994 (DSHEA). Public Law 103–417. 10–25–1994.

17.

White CM. Dietary supplements pose real dangers to patients. Ann Pharmacother. 2020;54:815–9.PubMedCrossRef

18.

Ito G, Tanaka H, Ohira M, et al. Correlation between efficacy of PSK postoperative adjuvant immunochemotherapy for gastric cancer and expression of MHC class I. Exp Ther Med. 2012;3(6):925–30.PubMedPubMedCentralCrossRef

19.

Torkelson CJ, Sweet E, Martzen MR, et al. Phase 1 clinical trial of Trametes versicolor in women with breast cancer. ISRN Oncol. 2012;2012:251632.PubMedPubMedCentral

20.

Deng G, Lin H, Seidman A, et al. A phase I/II trial of a polysaccharide extract from Grifola frondosa (Maitake mushroom) in breast cancer patients: immunological effects. J Cancer Res Clin Oncol. 2009;135:1215–21.PubMedPubMedCentralCrossRef

21.

Witt CM, Balneaves LG, Cardoso MJ, et al. 2017 A comprehensive definition for integrative oncology. J Natl Cancer Inst Monogr. 2017;52:lgx012.

22.

Frenkel M, Cohen L. Effective communication about the use of complementary and integrative medicine in cancer care. J Altern Complement Med. 2014;20(1):12–8.PubMedPubMedCentralCrossRef

23.

Lee RT, Greenlee H. Don’t ask, don’t tell: it’s time to talk about complementary, alternative, and integrative medicine with our patients. Cancer. 2020;126(13):2968–70.PubMedCrossRef

24.

Nakazato H, Koike A, Saji S, Ogawa N, Sakamoto J. Efficacy of immunochemotherapy as adjuvant treatment after curative resection of gastric cancer. Study Group of Immunochemotherapy with PSK for Gastric Cancer. Lancet. 1994;343(8906):1122–6.PubMedCrossRef

25.

Oba K, Teramukai S, Kobayashi M, Matsui T, Kodera Y, Sakamoto J. Efficacy of adjuvant immunochemotherapy with polysaccharide K for patients with curative resections of gastric cancer. Cancer Immunol Immunother. 2007;56(6):905–11.PubMedCrossRef

26.

Toge T, Yamaguchi Y. Protein-bound polysaccharide increases survival in resected gastric cancer cases stratified with a preoperative granulocyte and lymphocyte count. Oncol Rep. 2000;7(5):1157–61.PubMed

27.

Yoshitani S, Takashima S. Efficacy of postoperative UFT (tegafur/uracil) plus PSK therapies in elderly patients with resected colorectal cancer. Cancer Biother Radiopharm. 2009;24(1):35–40.PubMed

28.

Zhang Y, Wang X, Chen T. Efficacy of Huaier granule in patients with breast cancer. Clin Transl Oncol. 2019;21:588–95.PubMedCrossRef

29.

Zhao GS, Liu Y, Zhang Q, et al. Transarterial chemoembolization combined with Huaier granule for the treatment of primary hepatic carcinoma: safety and efficacy. Medicine (Baltimore). 2017;96:e7589.PubMedCrossRef

30.

Zhou L, Pan LC, Zheng YG, et al. Novel strategy of sirolimus plus thymalfasin and Huaier granule on tumor recurrence of hepatocellular carcinoma beyond the UCSF criteria following liver transplantation: a single center experience. Oncol Lett. 2018;16:4407–17.PubMedPubMedCentral

31.

•• Chen Q, Chen XP. Adjuvant Huaier granule for hepatocellular carcinoma after curative resection: a phase IV, multicenter, randomized, and parallel-group controlled clinical trial. J Hepatol. 2017;66(suppl 1)S622. This large multi-center randomised controlled clinical trial showed survival benefit of Huaier granule, a mushroom supplement, in hepatocellular cancer.

32.

Qi J, Xie FJ, Liu S, et al. Huaier granule combined with tegafur gimeracil oteracil potassium promotes stage IIb gastric cancer prognosis and induces gastric cancer cell apoptosis by regulating Livin. Biomed Res Int. 2020;2020:2403595.PubMedPubMedCentralCrossRef

33.

Akagi J, Baba H. PSK may suppress CD57(+) T cells to improve survival of advanced gastric cancer patients. Int J Clin Oncol. 2010;15:145–52.PubMedCrossRef

34.

Tanaka H, Muguruma K, Ohira M, et al. Impact of adjuvant immunochemotherapy using protein-bound polysaccharide-K on overall survival of patients with gastric cancer. Anticancer Res. 2012;32:3427–33.PubMed

35.

Fukuchi M, Mochiki E, Ishiguro T, et al. Improved efficacy by addition of protein-bound polysaccharide K to adjuvant chemotherapy for advanced gastric cancer. Anticancer Res. 2016;36:4237–41.PubMed

36.

Hsu JT, Hsu CS, Le PH, et al. Immunochemotherapy benefits in gastric cancer patients stratified by programmed death-1 ligand-1. J Surg Res. 2017;211:30–8.PubMedCrossRef

37.

Namikawa T, Fukudome I, Ogawa M, et al. Clinical efficacy of protein-bound polysaccharide K in patients with gastric cancer undergoing chemotherapy with an oral fluoropyrimidine (S-1). Eur J Surg Oncol. 2015;41:795–800.PubMedCrossRef

38.

Okuno K, Aoyama T, Oba K, et al. Randomized phase III trial comparing surgery alone to UFT + PSK for stage II rectal cancer (JFMC38 trial). Cancer Chemother Pharmacol. 2018;81:65–71.PubMedCrossRef

39.

Ahn MS, Kang SY, Lee HW, et al. 5-Fluorouracil, mitomycin-c, and polysaccharide-k versus uracil-ftorafur and polysaccharide-K as adjuvant chemoimmunotherapy for patients with locally advanced gastric cancer with curative resection. Onkologie. 2013;36:421–6.PubMed

40.

Yoshino S, Nishikawa K, Morita S, et al. Randomised phase III study of S-1 alone versus S-1 plus lentinan for unresectable or recurrent gastric cancer (JFMC36-0701). Eur J Cancer. 2016;65:164–71.PubMedCrossRef

41.

Miyake Y, Nishimura J, Kato T, et al. Phase III trial comparing UFT + PSK to UFT + LV in stage IIB, III colorectal cancer (MCSGO-CCTG). Surg Today. 2018;48:66–72.PubMedCrossRef

42.

Lee SH, Hwang HK, Kang CM, Lee WJ. Potential impact of Phellinus linteus on adherence to adjuvant treatment after curative resection of pancreatic ductal adenocarcinoma: outcomes of a propensity score-matched analysis. Integr Cancer Ther. 2019;18:1534735418816825.PubMedCrossRef

43.

Yanagimoto H, Satoi S, Yamamoto T, et al. Alleviating effect of active hexose correlated compound (AHCC) on chemotherapy-related adverse events in patients with unresectable pancreatic ductal adenocarcinoma. Nutr Cancer. 2016;68:234–40.PubMedCrossRef

44.

Yoshimura K, Kamoto T, Ogawa O, et al. Medical mushrooms used for biochemical failure after radical treatment for prostate cancer: an open-label study. Int J Urol. 2010;17:548–54.PubMedCrossRef

45.

Sumiyoshi Y, Hashine K, Kakehi Y, et al. Dietary administration of mushroom mycelium extracts in patients with early stage prostate cancers managed expectantly: a phase II study. Jpn J Clin Oncol. 2010;40:967–72.PubMedCrossRef

46.

Tsai MY, Hung YC, Chen YH, et al. A preliminary randomised controlled study of short-term Antrodia cinnamomea treatment combined with chemotherapy for patients with advanced cancer. BMC Complement Altern Med. 2016;16:322.PubMedPubMedCentralCrossRef

47.

Ali NKM, Saeed HA, Othman RT. Immunostimulatory and anti-inflammatory effect of Ganoderma lucidum on breast cancer patients. Asia Pacific J Cancer Biol. 2019;3:51–7.

48.

Suzuki N, Takimoto Y, Suzuki R, et al. Efficacy of oral administration of Lentinula eododes mycelia extract for breast cancer patients undergoing postoperative hormone therapy. Asian Pac J Cancer Prev. 2013;14:3469–72.PubMedCrossRef

49.

Zhao H, Zhang Q, Zhao L, Huang X, Wang J, Kang X. Spore powder of Ganoderma lucidum improves cancer-related fatigue in breast cancer patients undergoing endocrine therapy: a pilot clinical trial. Evid Based Complement Alternat Med. 2012;2012:809614.PubMedCrossRef

50.

Nagashima Y, Maeda N, Yamamoto S, Yoshino S, Oka M. Evaluation of host quality of life and immune function in breast cancer patients treated with combination of adjuvant chemotherapy and oral administration of Lentinula edodes mycelia extract. Onco Targets Ther. 2013;6:853–9.PubMedPubMedCentralCrossRef

51.

Nagashima Y, Yoshino S, Yamamoto S, et al. Lentinula edodes mycelia extract plus adjuvant chemotherapy for breast cancer patients: results of a randomized study on host quality of life and immune function improvement. Mol Clin Oncol. 2017;7:359–66.PubMedPubMedCentralCrossRef

52.

Suknikhom W, Lertkhachonsuk R, Manchana T. The effects of active hexose correlated compound (AHCC) on levels of CD4+ and CD8+ in patients with epithelial ovarian cancer or peritoneal cancer receiving platinum based chemotherapy. Asian Pac J Cancer Prev. 2017;18:633–8.PubMedPubMedCentral

53.

Chochi K, Ichikura T, Majima T, et al. The increase of CD57+ T cells in the peripheral blood and their impaired immune functions in patients with advanced gastric cancer. Oncol Rep. 2003;10:1443–8.PubMed

54.

Sadahiro S, Suzuki T, Maeda Y, et al. Effects of preoperative immunochemoradiotherapy and chemoradiotherapy on immune responses in patients with rectal adenocarcinoma. Anticancer Res. 2010;30:993–9.PubMed

55.

Yamashita K, Sakuramoto S, Mieno H, et al. Preoperative administration of polysaccharide Kureha and reduced plasma transforming growth factor-β in patients with advanced gastric cancer: a randomized clinical trial. Mol Clin Oncol. 2015;3:471–8.PubMedPubMedCentralCrossRef

56.

Wang JL, Bi Z, Zou JW, Gu XM. Combination therapy with lentinan improves outcomes in patients with esophageal carcinoma. Mol Med Rep. 2012;5:745–8.PubMed

57.

Wang XE, Wang YH, Zhou Q, et al. Immunomodulatory effect of lentinan on aberrant T subsets and cytokines profile in non-small cell lung cancer patients. Pathol Oncol Res. 2020;26:499–505.PubMedCrossRef

58.

Twardowski P, Kanaya N, Frankel P, et al. A phase I trial of mushroom powder in patients with biochemically recurrent prostate cancer: roles of cytokines and myeloid-derived suppressor cells for Agaricus bisporus-induced prostate-specific antigen responses. Cancer. 2015;121:2942–50.PubMedCrossRef

59.

Tangen JM, Tierens A, Caers J, et al. Immunomodulatory effects of the Agaricus blazei Murrill-based mushroom extract AndoSan in patients with multiple myeloma undergoing high dose chemotherapy and autologous stem cell transplantation: a randomized, double blinded clinical study. Biomed Res Int. 2015;2015:718539.PubMedPubMedCentralCrossRef

60.

Ito T, Urushima H, Sakaue M, et al. Reduction of adverse effects by a mushroom product, active hexose correlated compound (AHCC) in patients with advanced cancer during chemotherapy–the significance of the levels of HHV-6 DNA in saliva as a surrogate biomarker during chemotherapy. Nutr Cancer. 2014;66:377–82.PubMedCrossRef

61.

Ohno S, Sumiyoshi Y, Hashine K, Shirato A, Kyo S, Inoue M. Quality of life improvements among cancer patients in remission following the consumption of Agaricus blazei Murill mushroom extract. Complement Ther Med. 2013;21:460–7.PubMedCrossRef

62.

Costa Fortes R, LacorteRecôva V, Lima Melo A, CarvalhoGarbiNovaes MR. Life quality of postsurgical patients with colorectal cancer after supplemented diet with Agaricus sylvaticus fungus. Nutr Hosp. 2010;25:586–96.PubMed

63.

Hangai S, Iwase S, Kawaguchi T, et al. Effect of active hexose-correlated compound in women receiving adjuvant chemotherapy for breast cancer: a retrospective study. J Altern Complement Med. 2013;19:905–10.PubMedPubMedCentralCrossRef

64.

Ohno S, Sumiyoshi Y, Hashine K, Shirato A, Kyo S, Inoue M. Phase I clinical study of the dietary supplement, Agaricus blazei murill, in cancer patients in remission. Evid Based Complement Alternat Med. 2011;2011:192381.PubMedPubMedCentralCrossRef

65.

Guo LY, Zhang SY, Chen C, Zeng HX, Li FY, Xu QX. Lentinan combined with cisplatin and paclitaxel in the treatment of patients with ovarian cancer with ascites. Eur J Gynaecol Oncol. 2018;39:615–20.

66.

Higashi D, Seki K, Ishibashi Y, et al. The effect of lentinan combination therapy for unresectable advanced gastric cancer. Anticancer Res. 2012;32:2365–8.PubMed

67.

Valadares F, GarbiNovaes MR, Cañete R. Effect of Agaricus sylvaticus supplementation on nutritional status and adverse events of chemotherapy of breast cancer: a randomized, placebo-controlled, double-blind clinical trial. Indian J Pharmacol. 2013;45:217–22.PubMedPubMedCentralCrossRef

68.

Shreya S, Kumar DN, Mohapatra D, et al. Tracing the anti-cancer mechanism of Pleurotus osteratus by the integrative approach of network pharmacology and experimental studies. Appl Biochem Biotechnol. 2023;195(1):152–71.PubMedCrossRef

69.

Cheng S, Castillo V, Sliva D. CDC20 associated with cancer metastasis and novel mushroom-derived CDC20 inhibitors with antimetastatic activity. Int J Oncol. 2019;54(6):2250–6.PubMed

70.

Chen S, Li X, Yong T, et al. Cytotoxic lanostane-type triterpenoids from the fruiting bodies of Ganoderma lucidum and their structure-activity relationships. Oncotarget. 2017;8(6):10071–84.PubMedCrossRef

71.

Chihara G, Hamuro J, Maeda Y, Arai Y, Fukuoka F. Fractionation and purification of the polysaccharides with marked antitumor activity, especially lentinan, from Lentinus edodes (Berk.) Sing. (an edible mushroom). Cancer Res. 1970;30(11):2776–81.PubMed

72.

Deng S, Zhang G, Kuai J, et al. Lentinan inhibits tumor angiogenesis via interferon γ and in a T cell independent manner [published correction appears in J ExpClin Cancer Res. 2021 Nov 18;40(1):366]. J Exp Clin Cancer Res. 2018;37:260.

73.

Du YC, Chang FR, Wu TY, et al. Antileukemia component, dehydroeburicoic acid from Antrodia camphorata induces DNA damage and apoptosis in vitro and in vivo models. Phytomedicine. 2012;19(8–9):788–96.PubMedCrossRef

74.

Fu J, Wei C, Cheng J, et al. Cordycepin inhibits breast cancer migration and invasion by targeting epithelial to mesenchymal transition-inducing transcription factors (EMT-TFs) [abstract]. Cancer Res. 2018;78(13_Supplement):2039.

75.

Han CK, Chiang HC, Lin CY, et al. Comparison of immunomodulatory and anticancer activities in different strains of Tremella fuciformis Berk. Am J Chin Med. 2015;43:1637–55.PubMedCrossRef

76.

Hsu WH, Qiu WL, Tsao SM, et al. Effects of WSG, a polysaccharide from Ganoderma lucidum, on suppressing cell growth and mobility of lung cancer. Int J Biol Macromol. 2020;165(Pt A):1604–13.PubMedCrossRef

77.

Roda E, De Luca F, Di Iorio C, et al. Novel medicinal mushroom blend as a promising supplement in integrative oncology: a multi-tiered study using 4 T1 Triple-negative mouse breast cancer model. Int J Mol Sci. 2020;21:3479.PubMedPubMedCentralCrossRef

78.

Winder M, Bulska-Będkowska W, Chudek J. The use of Hericium erinaceus and Trametes versicolor extracts in supportive treatment in oncology. Acta Pharm. 2021;71:1–16.PubMedCrossRef

79.

Sweet ES, Standish LJ, Goff BA, Andersen MR. Adverse events associated with complementary and alternative medicine use in ovarian cancer patients. Integr Cancer Ther. 2013;12(6):508–16.PubMedCrossRef

80.

Lee RT, Barbo A, Lopez G, et al. National survey of US oncologists’ knowledge, attitudes, and practice patterns regarding herb and supplement use by patients with cancer. J Clin Oncol. 2014;32:4095–101.PubMedPubMedCentralCrossRef

81.

Hou YN, Chimonas S, Gubili J, et al. Integrating herbal medicine into oncology care delivery: development, implementation, and evaluation of a novel program. Support Care Cancer. 2023;31(2):128.PubMedPubMedCentralCrossRef

Titel: Medicinal Mushroom Supplements in Cancer: A Systematic Review of Clinical Studies
verfasst von: Santhosshi Narayanan
Aline Rozman de Mores
Lorenzo Cohen
Mohammed Moustapha Anwar
Felippe Lazar
Rachel Hicklen
Gabriel Lopez
Peiying Yang
Eduardo Bruera
Publikationsdatum: 30.03.2023
Verlag: Springer US
Erschienen in: Current Oncology Reports / Ausgabe 6/2023
Print ISSN: 1523-3790
Elektronische ISSN: 1534-6269
DOI: https://doi.org/10.1007/s11912-023-01408-2

Springer Medizin

Medicinal Mushroom Supplements in Cancer: A Systematic Review of Clinical Studies