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Medicinal plants and their isolated phytochemicals for the management of chemotherapy-induced neuropathy: therapeutic targets and clinical perspective

  • Vahideh Oveissi
  • Mahboobe Ram
  • Roodabeh Bahramsoltani
  • Farnaz Ebrahimi
  • Roja Rahimi
  • Rozita Naseri
  • Tarun Belwal
  • Hari Prasad Devkota
  • Zahra Abbasabadi
  • Mohammad Hosein FarzaeiEmail author
Review Article

Abstract

Background

Chemotherapy, as one of the main approaches of cancer treatment, is accompanied with several adverse effects, including chemotherapy-induced peripheral neuropathy (CIPN). Since current methods to control the condition are not completely effective, new treatment options should be introduced. Medicinal plants can be suitable candidates to be assessed regarding their effects in CIPN. Current paper reviews the available preclinical and clinical studies on the efficacy of herbal medicines in CIPN.

Methods

Electronic databases including PubMed, Scopus, and Cochrane library were searched with the keywords “neuropathy” in the title/abstract and “plant”, “extract”, or “herb” in the whole text. Data were collected from inception until April 2018.

Results

Plants such as chamomile (Matricaria chamomilla L.), sage (Salvia officinalis L.), cinnamon (Cinnamomum cassia (L.) D. Don), and sweet flag (Acorus calamus L.) as well as phytochemicals like matrine, curcumin, and thioctic acid have demonstrated beneficial effects in animal models of CIPN via prevention of axonal degeneration, decrease in total calcium level, improvement of endogenous antioxidant defense mechanisms such as superoxide dismutase and reduced glutathione, and regulation of neural cell apoptosis, nuclear factor-ĸB, cyclooxygenase-2, and nitric oxide signaling. Also, five clinical trials have evaluated the effect of herbal products in patients with CIPN.

Conclusions

There are currently limited clinical evidence on medicinal plants for CIPN which shows the necessity of future mechanistic studies, as well as well-designed clinical trial for further confirmation of the safety and efficacy of herbal medicines in CIPN.

Graphical abstract

Schematic mechanisms of medicinal plants to prevent chemotherapy-induced neuropathy: NO: nitric oxide, TNF: tumor necrosis factor, PG: prostaglandin, NF-ĸB: nuclear factor kappa B, LPO: lipid peroxidation, ROS: reactive oxygen species, COX: cyclooxygenase, IL: interleukin, ERK: extracellular signal-related kinase, X: inhibition, ↓: induction.

Keywords

Pain Neuropathy Phytotherapy Chemotherapeutic agents Inflammation Phytochemicals Medicinal plants Clinical studies 

Notes

Compliance with ethical standards

Conflict of interest

Authors declare that they have no conflicts of interest.

References

  1. 1.
    Hughes RAC. Peripheral neuropathy. Br Med J. 2002;324(7335):466–9.CrossRefGoogle Scholar
  2. 2.
    Martyn CN, Hughes RA. Epidemiology of peripheral neuropathy. J Neurol Neurosurg Psychiatry. 1997;62(4):310–8.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Fuller G. Diagnosing and managing mononeuropathies. Clin Med (Lond). 2004;4(2):113–7.CrossRefGoogle Scholar
  4. 4.
    Cascella M. Chemotherapy-induced peripheral neuropathy: limitations in current prophylactic strategies and directions for future research. Curr Med Res Opin. 2017;33(6):981–4.CrossRefPubMedGoogle Scholar
  5. 5.
    Malik B, Stillman M. Chemotherapy-induced peripheral neuropathy. Curr Neurol Neurosci Rep. 2008;8(1):56–65.CrossRefPubMedGoogle Scholar
  6. 6.
    Wolf S, Barton D, Kottschade L, Grothey A, Loprinzi C. Chemotherapy-induced peripheral neuropathy: prevention and treatment strategies. Eur J Cancer. 2008;44(11):1507–15.CrossRefPubMedGoogle Scholar
  7. 7.
    Brzeziński K. Chemotherapy-induced peripheral neuropathy. Part II. Prevention. Contemp Oncol (Pozn). 2012;16(3):258–61.Google Scholar
  8. 8.
    Seretny M, Currie GL, Sena ES, Ramnarine S, Grant R, MacLeod MR, et al. Incidence, prevalence, and predictors of chemotherapy-induced peripheral neuropathy: a systematic review and meta-analysis. Pain. 2014;155(12):2461–70.CrossRefPubMedGoogle Scholar
  9. 9.
    Wong R, Sagar S. Acupuncture treatment for chemotherapy-induced peripheral neuropathy–a case series. Acupunct Med. 2006;24(2):87–91.CrossRefPubMedGoogle Scholar
  10. 10.
    Quasthoff S, Hartung HP. Chemotherapy-induced peripheral neuropathy. J Neurol. 2002;249(1):9–17.CrossRefPubMedGoogle Scholar
  11. 11.
    Albers JW, Chaudhry V, Cavaletti G, Donehower RC. Interventions for preventing neuropathy caused by cisplatin and related compounds. Cochrane Database Syst Rev. 2014;(3):Cd005228.Google Scholar
  12. 12.
    Bahramsoltani R, Farzaei MH, Farahani MS, Rahimi R. Phytochemical constituents as future antidepressants: a comprehensive review. Rev Neurosci. 2015;26(6):699–719.CrossRefPubMedGoogle Scholar
  13. 13.
    Farzaei MH, Shahpiri Z, Mehri MR, Bahramsoltani R, Rezaei M, Raeesdana A, et al. Medicinal plants in neurodegenerative diseases: perspective of traditional Persian medicine. Curr Drug Metab. 2018;19(5):429–42.CrossRefPubMedGoogle Scholar
  14. 14.
    Shahpiri Z, Bahramsoltani R, Hosein Farzaei M, Farzaei F, Rahimi R. Phytochemicals as future drugs for Parkinson’s disease: a comprehensive review. Rev Neurosci. 2016;27(6):651–68.CrossRefPubMedGoogle Scholar
  15. 15.
    Abad ANA, Nouri MHK, Gharjanie A, Tavakoli F. Effect of Matricaria chamomilla Hydroalcoholic extract on cisplatin-induced neuropathy in mice. Chin J Nat Med. 2011;9(2):126–31.Google Scholar
  16. 16.
    Abad ANA, Nouri MHK, Tavakkoli F. Effect of Salvia officinalis hydroalcoholic extract on vincristine-induced neuropathy in mice. Chin J Nat Med. 2011;9(5):354–8.Google Scholar
  17. 17.
    Ameyaw EO, Woode E, Boakye-Gyasi E, Abotsi WKM, Kyekyeku JO, Adosraku RK. Anti-Allodynic and anti-hyperalgesic effects of an ethanolic extract and xylopic acid from the fruits of Xylopia aethiopica in murine models of neuropathic pain. Pharm Res. 2014;6(2):172–9.Google Scholar
  18. 18.
    Nabavi SF, Khan H, D'onofrio G, Šamec D, Shirooie S, Dehpour AR, et al. Apigenin as neuroprotective agent: of mice and men. Pharmacol Res. 2018;128:359–65.CrossRefPubMedGoogle Scholar
  19. 19.
    Amoateng P, Adjei S, Osei-Safo D, Kukuia KKE, Kretchy IA, Sarkodie JA, et al. Analgesic effects of a hydro-ethanolic whole plant extract of Synedrella nodiflora (L.) Gaertn in paclitaxel-induced neuropathic pain in rats. BMC Res Notes. 2017;10(1):226.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Andoh T, Kato M, Kitamura R, Mizoguchi S, Uta D, Toume K, et al. Prophylactic administration of an extract from Plantaginis semen and its major component aucubin inhibits mechanical allodynia caused by paclitaxel in mice. J Tradit Complement Med. 2016;6(3):305–8.CrossRefPubMedPubMedCentralGoogle Scholar
  21. 21.
    Boakye-Gyasi E, Kasanga EA, Biney RP, Abotsi WKM, Mensah KB, Woode E. Ameliorative effects of ethanolic leaf extract of Palisota hirsuta K. Schum (Commelinaceae) on vincristine-induced neuropathic pain in rats. J Applied Pharmaceut Sci. 2014;4(11):35–41.Google Scholar
  22. 22.
    Cho ES, Yi JM, Park JS, Lee YJ, Lim CJ, Bang OS, et al. Aqueous extract of Lithospermi radix attenuates oxaliplatin-induced neurotoxicity in both in vitro and in vivo models. BMC Complement Altern Med. 2016;16(1):419.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Di Cesare ML, Pacini A, Micheli L, Femia AP, Maresca M, Zanardelli M, et al. Astragali radix: could it be an adjuvant for oxaliplatin-induced neuropathy? Sci Rep. 2017;7:42021.CrossRefGoogle Scholar
  24. 24.
    Iliya HA, Abotsi WKM, Benneh C, Woode E. Maerua angolensis extract reduces allodynia and hyperalgesia in a mouse model of vincristine-induced peripheral neuropathy. J Applied Pharmaceut Sci. 2016;6(5):124–30.CrossRefGoogle Scholar
  25. 25.
    Jung Y, Lee JH, Kim W, Yoon SH, Kim SK. Anti-allodynic effect of Buja in a rat model of oxaliplatin-induced peripheral neuropathy via spinal astrocytes and pro-inflammatory cytokines suppression. BMC Complement Altern Med. 2017;17(1).  https://doi.org/10.1186/s12906-017-1556-z.
  26. 26.
    Kaur G, Jaggi AS, Singh N. Exploring the potential effect of Ocimum sanctum in vincristine-induced neuropathic pain in rats. J Brachial Plex Peripher Nerve Inj. 2010;5(1).Google Scholar
  27. 27.
    Kim C, Lee JH, Kim W, Li D, Kim Y, Lee K, et al. The Suppressive Effects of Cinnamomi Cortex and Its Phytocompound Coumarin on Oxaliplatin-Induced Neuropathic Cold Allodynia in Rats. Molecules. 2016;21(9).Google Scholar
  28. 28.
    Lee JS, Kim YT, Jeon EK, Won HS, Cho YS, Ko YH. Effect of green tea extracts on oxaliplatin-induced peripheral neuropathy in rats. BMC Complement Altern Med. 2012;12:124.CrossRefPubMedPubMedCentralGoogle Scholar
  29. 29.
    Lee KH, Rhee KH. Anti-nociceptive effect of agrimonia eupatoria extract on a cisplatin-induced neuropathic model. Afr J Tradit Complement Altern Med. 2016;13(5):139–44.PubMedPubMedCentralGoogle Scholar
  30. 30.
    Muthuraman A, Singh N. Attenuating effect of hydroalcoholic extract of Acorus calamus in vincristine-induced painful neuropathy in rats. J Nat Med. 2011;65(3–4):480–7.CrossRefPubMedGoogle Scholar
  31. 31.
    Muthuraman A, Singh N, Jaggi AS. Protective effect of Acorus calamus L. in rat model of vincristine induced painful neuropathy: an evidence of anti-inflammatory and anti-oxidative activity. Food Chem Toxicol. 2011;49(10):2557–63.CrossRefPubMedGoogle Scholar
  32. 32.
    Park HJ, Lee HG, Kim YS, Lee JY, Jeon JP, Park C, et al. Ginkgo biloba extract attenuates hyperalgesia in a rat model of vincristine-induced peripheral neuropathy. Anesth Analg. 2012;115(5):1228–33.CrossRefPubMedGoogle Scholar
  33. 33.
    Nawaz NUA, Saeed M, Rauf K, Usman M, Arif M, Ullah Z, et al. Antinociceptive effectiveness of Tithonia tubaeformis in a vincristine model of chemotherapy-induced painful neuropathy in mice. Biomed Pharmacother. 2018;103:1043–51.CrossRefPubMedGoogle Scholar
  34. 34.
    Woode E, Boakey-Giasi E, Ainooson GK, Ansah C, Duwiejua M. Anti-nociceptive effects and the mechanism of Palisota hirsuta K. Schum. Leaf extract in murine models. Int J Pharmacol. 2009;5(2):101–13.CrossRefGoogle Scholar
  35. 35.
    Kahng J, Kim TK, Chung EY, Kim YS, Moon JY. The effect of thioctic acid on allodynia in a rat vincristine-induced neuropathy model. J Int Med Res. 2015;43(3):350–5.CrossRefPubMedGoogle Scholar
  36. 36.
    Al Moundhri MS, Al-Salam S, Al Mahrouqee A, Beegam S, Ali BH. The effect of curcumin on oxaliplatin and cisplatin neurotoxicity in rats: some behavioral, biochemical, and histopathological studies. J Med Toxicol. 2013;9(1):25–33.CrossRefPubMedGoogle Scholar
  37. 37.
    Dutra RC, Bicca MA, Segat GC, Silva KABS, Motta EM, Pianowski LF, et al. The antinociceptive effects of the tetracyclic triterpene euphol in inflammatory and neuropathic pain models: the potential role of PKCε. Neuroscience. 2015;303:126–37.CrossRefPubMedGoogle Scholar
  38. 38.
    Azevedo MI, Pereira AF, Nogueira RB, Rolim FE, Brito GA, Wong DV, et al. The antioxidant effects of the flavonoids rutin and quercetin inhibit oxaliplatin-induced chronic painful peripheral neuropathy. Mol Pain. 2013;9:53.CrossRefPubMedPubMedCentralGoogle Scholar
  39. 39.
    Gong SS, Li YX, Zhang MT, Du J, Ma PS, Yao WX, et al. Neuroprotective effect of Matrine in mouse model of vincristine-induced neuropathic pain. Neurochem Res. 2016;41(11):3147–59.CrossRefPubMedGoogle Scholar
  40. 40.
    Dun L, Li Y, Xu Y, Zhou R, Ma L, Jin S, et al. Antinociceptive effect of matrine on vincristine-induced neuropathic pain model in mice. Neurol Sci. 2014;35(6):815–21.CrossRefGoogle Scholar
  41. 41.
    Babu A, Prasanth KG, Balaji B. Effect of curcumin in mice model of vincristine-induced neuropathy. Pharm Biol. 2015;53(6):838–48.CrossRefPubMedGoogle Scholar
  42. 42.
    Andoh T, Kobayashi N, Uta D, Kuraishi Y. Prophylactic topical paeoniflorin prevents mechanical allodynia caused by paclitaxel in mice through adenosine A1 receptors. Phytomedicine. 2017;25:1–7.CrossRefPubMedGoogle Scholar
  43. 43.
    Guo Y, Jones D, Palmer JL, Forman A, Dakhil SR, Velasco MR, et al. Oral alpha-lipoic acid to prevent chemotherapy-induced peripheral neuropathy: a randomized, double-blind, placebo-controlled trial. Support Care Cancer. 2014;22(5):1223–31.CrossRefPubMedGoogle Scholar
  44. 44.
    Desideri I, Francolini G, Becherini C, Terziani F, Delli Paoli C, Olmetto E, et al. Use of an alpha lipoic, methylsulfonylmethane and bromelain dietary supplement (opera((R))) for chemotherapy-induced peripheral neuropathy management, a prospective study. Med Oncol. 2017;34(3):46.CrossRefPubMedGoogle Scholar
  45. 45.
    Kaku H, Kumagai S, Onoue H, Takada A, Shoji T, Miura F, et al. Objective evaluation of the alleviating effects of Goshajinkigan on peripheral neuropathy induced by paclitaxel/carboplatin therapy: a multicenter collaborative study. Exp Ther Med. 2012;3(1):60–5.CrossRefPubMedGoogle Scholar
  46. 46.
    Lynch ME, Cesar-Rittenberg P, Hohmann AG. A double-blind, placebo-controlled, crossover pilot trial with extension using an oral mucosal cannabinoid extract for treatment of chemotherapy-induced neuropathic pain. J Pain Symptom Manag. 2014;47(1):166–73.CrossRefGoogle Scholar
  47. 47.
    Yoshida N, Hosokawa T, Ishikawa T, Yagi N, Kokura S, Naito Y, et al. Efficacy of goshajinkigan for oxaliplatin-induced peripheral neuropathy in colorectal cancer patients. J Oncol. 2013;2013:139740.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    McWhinney SR, Goldberg RM, McLeod HL. Platinum neurotoxicity pharmacogenetics. Mol Cancer Ther. 2009;8(1):10–6.CrossRefPubMedPubMedCentralGoogle Scholar
  49. 49.
    Poklar N, Pilch DS, Lippard SJ, Redding EA, Dunham SU, Breslauer KJ. Influence of cisplatin intrastrand crosslinking on the conformation, thermal stability, and energetics of a 20-mer DNA duplex. Proc Natl Acad Sci U S A. 1996;93(15):7606–11.CrossRefPubMedPubMedCentralGoogle Scholar
  50. 50.
    Rudd GN, Hartley JA, Souhami RL. Persistence of cisplatin-induced DNA interstrand crosslinking in peripheral blood mononuclear cells from elderly and young individuals. Cancer Chemother Pharmacol. 1995;35(4):323–6.  https://doi.org/10.1007/bf00689452.CrossRefPubMedGoogle Scholar
  51. 51.
    Windebank AJ, Grisold W. Chemotherapy-induced neuropathy. J Peripher Nerv Syst. 2008;13(1):27–46.CrossRefPubMedGoogle Scholar
  52. 52.
    Tanner KD, Levine JD, Topp KS. Microtubule disorientation and axonal swelling in unmyelinated sensory axons during vincristine-induced painful neuropathy in rat. J Comp Neurol. 1998;395(4):481–92.CrossRefPubMedGoogle Scholar
  53. 53.
    Hagiwara H, Sunada Y. Mechanism of taxane neurotoxicity. Breast Cancer. 2004;11(1):82–5.CrossRefPubMedGoogle Scholar
  54. 54.
    Broyl A, Corthals SL, Jongen JL, van der Holt B, Kuiper R, de Knegt Y, et al. Mechanisms of peripheral neuropathy associated with bortezomib and vincristine in patients with newly diagnosed multiple myeloma: a prospective analysis of data from the HOVON-65/GMMG-HD4 trial. Lancet Oncol. 2010;11(11):1057–65.CrossRefPubMedGoogle Scholar
  55. 55.
    Chaudhry V, Cornblath D, Corse A, Freimer M, Simmons-O’Brien E, Vogelsang G. Thalidomide-induced neuropathy. Neurology. 2002;59(12):1872–5.CrossRefPubMedGoogle Scholar
  56. 56.
    Ferrero-Miliani L, Nielsen O, Andersen P, Girardin S. Chronic inflammation: importance of NOD2 and NALP3 in interleukin-1β generation. Clin Exp Immunol. 2007;147(2):227–35.PubMedPubMedCentralGoogle Scholar
  57. 57.
    Siegal T, Haim N. Cisplatin-induced peripheral neuropathy. Frequent off-therapy deterioration, demyelinating syndromes, and muscle cramps. Cancer. 1990;66(6):1117–23.CrossRefPubMedGoogle Scholar
  58. 58.
    Ding YQ, Kaneko T, Nomura S, Mizuno N. Immunohistochemical localization of μ-opioid receptors in the central nervous system of the rat. J Comp Neurol. 1996;367(3):375–402.CrossRefPubMedGoogle Scholar
  59. 59.
    Obara I, Makuch W, Spetea M, Schutz J, Schmidhammer H, Przewlocki R, et al. Local peripheral antinociceptive effects of 14-O-methyloxymorphone derivatives in inflammatory and neuropathic pain in the rat. Eur J Pharmacol. 2007;558(1–3):60–7.CrossRefPubMedGoogle Scholar
  60. 60.
    Bujalska M, Makulska-Nowak H. Bradykinin receptors antagonists and nitric oxide synthase inhibitors in vincristine and streptozotocin induced hyperalgesia in chemotherapy and diabetic neuropathy rat model. Neuro Endocrinol Lett. 2009;30(1):144–52.PubMedGoogle Scholar
  61. 61.
    Yajima Y, Narita M, Usui A, Kaneko C, Miyatake M, Narita M, et al. Direct evidence for the involvement of brain-derived neurotrophic factor in the development of a neuropathic pain-like state in mice. J Neurochem. 2005;93(3):584–94.CrossRefPubMedGoogle Scholar
  62. 62.
    Castrillo A, de Las HB, Hortelano S, Rodriguez B, Villar A, Bosca L. Inhibition of the nuclear factor kappa B (NF-kappa B) pathway by tetracyclic kaurene diterpenes in macrophages. Specific effects on NF-kappa B-inducing kinase activity and on the coordinate activation of ERK and p38 MAPK. J Biol Chem. 2001;276(19):15854–60.CrossRefPubMedGoogle Scholar
  63. 63.
    Aley KO, Levine JD. Role of protein kinase a in the maintenance of inflammatory pain. J Neurosci. 1999;19(6):2181–6.CrossRefPubMedGoogle Scholar
  64. 64.
    Coderre TJ. Contribution of protein kinase C to central sensitization and persistent pain following tissue injury. Neurosci Lett. 1992;140(2):181–4.CrossRefPubMedGoogle Scholar
  65. 65.
    McQuay H, Tramer M, Nye B, Carroll D, Wiffen P, Moore R. A systematic review of antidepressants in neuropathic pain. Pain. 1996;68(2–3):217–27.CrossRefPubMedGoogle Scholar
  66. 66.
    Sindrup SH, Jensen TS. Efficacy of pharmacological treatments of neuropathic pain: an update and effect related to mechanism of drug action. Pain. 1999;83(3):389–400.CrossRefPubMedGoogle Scholar
  67. 67.
    Uhm JH, Yung WK. Neurologic complications of cancer therapy. Curr Treat Options Neurol. 1999;1(5):428–37.CrossRefPubMedGoogle Scholar
  68. 68.
    Millan MJ. Descending control of pain. Prog Neurobiol. 2002;66(6):355–474.CrossRefPubMedGoogle Scholar
  69. 69.
    Zhao X, Xu Y, Zhao Q, Chen C-R, Liu A-M, Huang Z-L. Curcumin exerts antinociceptive effects in a mouse model of neuropathic pain: descending monoamine system and opioid receptors are differentially involved. Neuropharmacology. 2012;62(2):843–54.CrossRefPubMedGoogle Scholar
  70. 70.
    Tracey DJ, Cunningham JE, Romm MA. Peripheral hyperalgesia in experimental neuropathy: mediation by α2-adrenoreceptors on post-ganglionic sympathetic terminals. Pain. 1995;60(3):317–27.CrossRefPubMedGoogle Scholar
  71. 71.
    Woode E, Ameyaw E, Ainooson G, Abotsi W, Gyasi E, Kyekyeku J. Analgesic effects of an ethanol extract of the fruits of xylopia aethiopica and xylopic acid in murine models of pain: possible mechanism (s). Pharmacologia. 2013;4(4):285–300.CrossRefGoogle Scholar
  72. 72.
    Warwick RA, Hanani M. The contribution of satellite glial cells to chemotherapy-induced neuropathic pain. Eur J Pain. 2013;17(4):571–80.CrossRefPubMedGoogle Scholar
  73. 73.
    Cavaletti G, Alberti P, Frigeni B, Piatti M, Susani E. Chemotherapy-induced neuropathy. Curr Treat Options Neurol. 2011;13(2):180–90.CrossRefPubMedGoogle Scholar
  74. 74.
    Hassler SN, Johnson KM, Hulsebosch CE. Reactive oxygen species and lipid peroxidation inhibitors reduce mechanical sensitivity in a chronic neuropathic pain model of spinal cord injury in rats. J Neurochem. 2014;131(4):413–7.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Bánhegyi G, Baumeister P, Benedetti A, Dong D, Fu Y, Lee AS, et al. Endoplasmic reticulum stress. Ann N Y Acad Sci. 2007;1113(1):58–71.CrossRefPubMedGoogle Scholar
  76. 76.
    Ranpariya VL, Parmar SK, Sheth NR, Chandrashekhar VM. Neuroprotective activity of Matricaria recutita against fluoride-induced stress in rats. Pharm Biol. 2011;49(7):696–701.CrossRefPubMedGoogle Scholar
  77. 77.
    Chandrashekhar VM, Ranpariya VL, Ganapaty S, Parashar A, Muchandi AA. Neuroprotective activity of Matricaria recutita Linn against global model of ischemia in rats. J Ethnopharmacol. 2010;127(3):645–51.CrossRefPubMedGoogle Scholar
  78. 78.
    Grundmann O, Phipps SM, Zadezensky I, Butterweck V. Salvia divinorum and salvinorin a: an update on pharmacology and analytical methodology. Planta Med. 2007;73(10):1039–46.CrossRefPubMedGoogle Scholar
  79. 79.
    Iuvone T, De Filippis D, Esposito G, D'Amico A, Izzo AA. The spice sage and its active ingredient rosmarinic acid protect PC12 cells from amyloid-beta peptide-induced neurotoxicity. J Pharmacol Exp Ther. 2006;317(3):1143–9.CrossRefPubMedGoogle Scholar
  80. 80.
    Adaramoye OA, Popoola BO, Farombi EO. Effects of Xylopia aethiopica (Annonaceae) fruit methanol extract on gamma-radiation-induced oxidative stress in brain of adult male Wistar rats. Acta Biol Hung. 2010;61(3):250–61.CrossRefPubMedGoogle Scholar
  81. 81.
    Amoateng P, Adjei S, Osei-Safo D, Ameyaw EO, Ahedor B, N'Guessan BB, et al. A hydro-ethanolic extract of Synedrella nodiflora (L.) Gaertn ameliorates hyperalgesia and allodynia in vincristine-induced neuropathic pain in rats. J Basic Clin Physiol Pharmacol. 2015;26(4):383–94.CrossRefPubMedGoogle Scholar
  82. 82.
    Xue HY, Gao GZ, Lin QY, Jin LJ, Xu YP. Protective effects of aucubin on H2O2 -induced apoptosis in PC12 cells. Phytother Res. 2012;26(3):369–74.PubMedGoogle Scholar
  83. 83.
    Xue HY, Lu YN, Fang XM, Xu YP, Gao GZ, Jin LJ. Neuroprotective properties of aucubin in diabetic rats and diabetic encephalopathy rats. Mol Biol Rep. 2012;39(10):9311–8.CrossRefPubMedGoogle Scholar
  84. 84.
    Xue HY, Jin L, Jin LJ, Li XY, Zhang P, Ma YS, et al. Aucubin prevents loss of hippocampal neurons and regulates antioxidative activity in diabetic encephalopathy rats. Phytother Res. 2009;23(7):980–6.CrossRefPubMedGoogle Scholar
  85. 85.
    Benneh CK, Biney RP, Tandoh A, Ampadu FA, Adongo DW, Jato J, et al. Maerua angolensis DC. (Capparaceae) Stem Bark Extract Protects against Pentylenetetrazole-Induced Oxidative Stress and Seizures in Rats. Evid Based Complement Alternat Med. 2018;2018:9684138.CrossRefPubMedPubMedCentralGoogle Scholar
  86. 86.
    Benneh CK, Biney RP, Adongo DW, Mante PK, Ampadu FA, Tandoh A, et al. Anxiolytic and antidepressant effects of Maerua angolensis DC. Stem Bark Extract in Mice. Depress Res Treat. 2018;2018:1537371.PubMedPubMedCentralGoogle Scholar
  87. 87.
    Azi IH, Boakye-Gyasi E, Donatus AW, Agyei AF, Woode E. Antinociceptive activity of various solvent extracts of Maerua angolensis DC stem bark in rodents. J Phytopharmacol. 2014;3(1):1–8.Google Scholar
  88. 88.
    Venuprasad MP, Hemanth Kumar K, Khanum F. Neuroprotective effects of hydroalcoholic extract of Ocimum sanctum against H2O2 induced neuronal cell damage in SH-SY5Y cells via its antioxidative defence mechanism. Neurochem Res. 2013;38(10):2190–200.CrossRefPubMedGoogle Scholar
  89. 89.
    Yanpallewar SU, Rai S, Kumar M, Acharya SB. Evaluation of antioxidant and neuroprotective effect of Ocimum sanctum on transient cerebral ischemia and long-term cerebral hypoperfusion. Pharmacol Biochem Behav. 2004;79(1):155–64.CrossRefPubMedGoogle Scholar
  90. 90.
    Momtaz S, Hassani S, Khan F, Ziaee M, Abdollahi M. Cinnamon, a promising prospect towards Alzheimer's disease. Pharmacol Res. 2018;130:241–58.CrossRefPubMedGoogle Scholar
  91. 91.
    Madhavadas S, Subramanian S. Cognition enhancing effect of the aqueous extract of Cinnamomum zeylanicum on non-transgenic Alzheimer's disease rat model: biochemical, histological, and behavioural studies. Nutr Neurosci. 2017;20(9):526–37.CrossRefPubMedGoogle Scholar
  92. 92.
    Bae WY, Choi JS, Jeong JW. The Neuroprotective Effects of Cinnamic Aldehyde in an MPTP Mouse Model of Parkinson's Disease. Int J Mol Sci. 2018;19(2).Google Scholar
  93. 93.
    Chen YF, Wang YW, Huang WS, Lee MM, Wood WG, Leung YM, et al. Trans-Cinnamaldehyde, an essential oil in cinnamon powder, ameliorates cerebral ischemia-induced brain injury via inhibition of Neuroinflammation through attenuation of iNOS, COX-2 expression and NFκ-B signaling pathway. NeuroMolecular Med. 2016;18(3):322–33.CrossRefPubMedGoogle Scholar
  94. 94.
    Chen SQ, Wang ZS, Ma YX, Zhang W, Lu JL, Liang YR, et al. Neuroprotective Effects and Mechanisms of Tea Bioactive Components in Neurodegenerative Diseases. Molecules. 2018;23(3).Google Scholar
  95. 95.
    Kakuda T. Neuroprotective effects of the green tea components theanine and catechins. Biol Pharm Bull. 2002;25(12):1513–8.CrossRefPubMedGoogle Scholar
  96. 96.
    Lee KY, Hwang L, Jeong EJ, Kim SH, Kim YC, Sung SH. Effect of neuroprotective flavonoids of Agrimonia eupatoria on glutamate-induced oxidative injury to HT22 hippocampal cells. Biosci Biotechnol Biochem. 2010;74(8):1704–6.CrossRefPubMedGoogle Scholar
  97. 97.
    Muthuraman A, Singh N. Neuroprotective effect of saponin rich extract of Acorus calamus L. in rat model of chronic constriction injury (CCI) of sciatic nerve-induced neuropathic pain. J Ethnopharmacol. 2012;142(3):723–31.CrossRefPubMedGoogle Scholar
  98. 98.
    Mo ZT, Fang YQ, He YP, Zhang S. β-Asarone protects PC12 cells against OGD/R-induced injury via attenuating Beclin-1-dependent autophagy. Acta Pharmacol Sin. 2012;33(6):737–42.CrossRefPubMedPubMedCentralGoogle Scholar
  99. 99.
    Yang X, Zheng T, Hong H, Cai N, Zhou X, Sun C, et al. Neuroprotective effects of Ginkgo biloba extract and Ginkgolide B against oxygen-glucose deprivation/reoxygenation and glucose injury in a new in vitro multicellular network model. Front Med. 2018;12(3):307–18.CrossRefPubMedGoogle Scholar
  100. 100.
    Taliyan R, Sharma PL. Protective effect and potential mechanism of Ginkgo biloba extract EGb 761 on STZ-induced neuropathic pain in rats. Phytother Res. 2012;26(12):1823–9.CrossRefPubMedGoogle Scholar
  101. 101.
    Cole GM, Teter B, Frautschy SA. Neuroprotective effects of curcumin. Adv Exp Med Biol. 2007;595:197–212.CrossRefPubMedPubMedCentralGoogle Scholar
  102. 102.
    Agthong S, Kaewsema A, Charoensub T. Curcumin ameliorates functional and structural abnormalities in cisplatin-induced neuropathy. Exp Neurobiol. 2015;24(2):139–45.  https://doi.org/10.5607/en.2015.24.2.139.CrossRefPubMedPubMedCentralGoogle Scholar
  103. 103.
    Bahramsoltani R, Rahimi R, Farzaei MH. Pharmacokinetic interactions of curcuminoids with conventional drugs: a review. J Ethnopharmacol. 2017;209:1–12.  https://doi.org/10.1016/j.jep.2017.07.022.CrossRefPubMedGoogle Scholar
  104. 104.
    Zheng M, Liu C, Fan Y, Shi D, Zhang Y. Protective effects of Paeoniflorin against MPP(+)-induced neurotoxicity in PC12 cells. Neurochem Res. 2016;41(6):1323–34.CrossRefPubMedGoogle Scholar
  105. 105.
    Gu X, Cai Z, Cai M, Liu K, Liu D, Zhang Q, et al. Protective effect of paeoniflorin on inflammation and apoptosis in the cerebral cortex of a transgenic mouse model of Alzheimer's disease. Mol Med Rep. 2016;13(3):2247–52.CrossRefPubMedGoogle Scholar
  106. 106.
    Wang D, Wong HK, Feng YB, Zhang ZJ. Paeoniflorin, a natural neuroprotective agent, modulates multiple anti-apoptotic and pro-apoptotic pathways in differentiated PC12 cells. Cell Mol Neurobiol. 2013;33(4):521–9.CrossRefPubMedGoogle Scholar
  107. 107.
    Costa LG, Garrick JM, Roquè PJ, Pellacani C. Mechanisms of neuroprotection by quercetin: counteracting oxidative stress and more. Oxidative Med Cell Longev. 2016;2016:2986796.Google Scholar
  108. 108.
    Dutra RC, Simão da Silva KA, Bento AF, Marcon R, Paszcuk AF, Meotti FC, et al. Euphol, a tetracyclic triterpene produces antinociceptive effects in inflammatory and neuropathic pain: the involvement of cannabinoid system. Neuropharmacology. 2012;63(4):593–605.CrossRefPubMedGoogle Scholar
  109. 109.
    Soleymani S, Bahramsoltani R, Rahimi R, Abdollahi M. Clinical risks of St John's wort (Hypericum perforatum) co-administration. Expert Opin Drug Metab Toxicol. 2017;13(10):1047–62.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Vahideh Oveissi
    • 1
    • 2
  • Mahboobe Ram
    • 3
  • Roodabeh Bahramsoltani
    • 4
  • Farnaz Ebrahimi
    • 5
  • Roja Rahimi
    • 4
  • Rozita Naseri
    • 6
  • Tarun Belwal
    • 7
  • Hari Prasad Devkota
    • 8
    • 9
  • Zahra Abbasabadi
    • 10
  • Mohammad Hosein Farzaei
    • 10
    • 11
    Email author
  1. 1.Faculty of PharmacyTehran University of Medical SciencesTehranIran
  2. 2.PhytoPharmacology Interest Group (PPIG)Universal Scientific Education and Research Network (USERN)TehranIran
  3. 3.Student Research Committee, Faculty of PharmacyMashhad University of Medical SciencesMashhadIran
  4. 4.Department of Traditional Pharmacy, School of Persian MedicineTehran University of Medical SciencesTehranIran
  5. 5.Pharmacy Students’ Research Committee, School of PharmacyIsfahan University of Medical SciencesIsfahanIran
  6. 6.Faculty of MedicineKermanshah University of Medical SciencesKermanshahIran
  7. 7.G. B. Pant National Institute of Himalayan Environment and Sustainable DevelopmentAlmoraIndia
  8. 8.School of PharmacyKumamoto UniversityKumamotoJapan
  9. 9.Program for Leading Graduate Schools, Health life science: Interdisciplinary and Glocal Oriented (HIGO) ProgramKumamoto UniversityKumamotoJapan
  10. 10.Pharmaceutical Sciences Research Center, Health InstituteKermanshah University of Medical SciencesKermanshahIran
  11. 11.Medical Biology Research CenterKermanshah University of Medical SciencesKermanshahIran

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