Anti-nociceptive effect of black seed oil on an animal model of chronic constriction injury

Sayyed Alireza Talaei , Hamid Reza Banafshe, Alireza Moravveji, Mohammad Shabani, Shiva Shirazi Tehrani, Alireza Abed

Abstract


Background and purpose: Traditionally, Nigella sativa L. has been known as a medical intervention to treat numerous diseases. This study aimed at investigating the antihyperalgesic effect of black seed oil (BSO) in an experimental model of neuropathic pain.

Experimental approach: Chronic constriction injury (CCI) was performed under anesthesia. The sciatic nerve was ligated with four loose ties. Two separate protocols were used to administer BSO. In chronic treatment, rats were given daily doses of BSO (250, 500, and 1000 mg/kg p.o.) from the 1st day until the 21st post-CCI day. While, in acute treatment, BSO (250, 500, and 1000 mg/kg p.o.) was administered only on the 7th, 14th, and 21st days. CCI and sham groups were given almond oil according to the same schedule. Behavioral scores were determined by evaluation of the paw withdrawal in the plantar, Von Frey, and acetone tests, on the 7th, 14th, and 21st days.

Findings/Results: Our results showed that CCI leads to significant allodynia and hyperalgesia in the ipsilateral paw after surgery. Chronic administration of BSO (500 and 1000 mg/kg) obviously attenuated heat hyperalgesia and mechanical allodynia. However, daily administration of BSO did not alter cold allodynia. Nevertheless, when BSO was administered, 30 min before the pain assessment tests, hypersensitivity was not improved in the treated animals.

Conclusion and implications: These results demonstrated BSO can inhibit neuropathic pain progression and suggests a potential use of BSO to manage hyperalgesia and allodynia. However, additional research is necessary to approve BSO effectiveness, in neuropathic pain conditions.


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References


Falzon CC, Balabanova A. Phytotherapy: an introduction to herbal medicine. Prim Care. 2017;44(2):217-227. DOI: 10.1016/j.pop.2017.02.001.

Ahmad A, Husain A, Mujeeb M, Khan SA, Najmi AK, Siddique NA, et al. A review on therapeutic potential of Nigella sativa: a miracle herb. Asian Pac J Trop Biomed. 2013;3(5):337-352. DOI: 10.1016/S2221-1691(13)60075-1.

Kooti W, Hasanzadeh-Noohi Z, Sharafi-Ahvazi N, Asadi-Samani M, Ashtary-Larky D. Phytochemistry, pharmacology, and therapeutic uses of black seed (Nigella sativa). Chin J Nat Med. 2016;14(10):732-745. DOI: 10.1016/S1875-5364(16)30088-7.

Amin B, Heravi Taheri MM, Hosseinzadeh H. Effects of intraperitoneal thymoquinone on chronic neuropathic pain in rats. Planta Med. 2014;80(15):1269-1277. DOI: 10.1055/s-0034-1383062.

Abdel-Fattah AM, Matsumoto K, Watanabe H. Antinociceptive effects of Nigella sativa oil and its major component, thymoquinone, in mice. Eur J Pharmacol. 2000;400(1):89-97. DOI: 10.1016/s0014-2999(00)00340-x.

Bordoni L, Fedeli D, Nasuti C, Maggi F, Papa F, Wabitsch M, et al. Antioxidant and anti-inflammatory properties of Nigella sativa oil in human pre-adipocytes. Antioxidants (Basel). 2019;8(2):51-63. DOI: 10.3390/antiox8020051.

Hajhashemi V, Ghannadi A, Jafarabadi H. Black cumin seed essential oil, as a potent analgesic and antiinflammatory drug. Phytother Res. 2004;18(3):195-199. DOI: 10.1002/ptr.1390.

Szok D, Tajti J, Nyári A, Vécsei L. Therapeutic approaches for peripheral and central neuropathic pain. Behav Neurol. 2019;2019:1-13. DOI: 10.1155/2019/8685954.

Baron R, Binder A, Wasner G. Neuropathic pain: diagnosis, pathophysiological mechanisms, and treatment. Lancet Neurol. 2010;9(8):807-819. DOI: 10.1016/S1474-4422(10)70143-5.

Finnerup NB, Kuner R, Jensen TS. Neuropathic pain: from mechanisms to treatment. Physiol Rev. 2021;101(1):259-301. DOI: 10.1152/physrev.00045.2019.

Xu L, Zhang Y, Huang Y. Advances in the treatment of neuropathic pain. Adv Exp Med Biol. 2016;904:117-129. DOI: 10.1007/978-94-017-7537-3_9.

Hajhashemi V, Banafshe HR, Minaiyan M, Mesdaghinia A, Abed A. Antinociceptive effects of venlafaxine in a rat model of peripheral neuropathy: role of alpha2-adrenergic receptors. Eur J Pharmacol. 2014;738:230-236.DOI: 10.1016/j.ejphar.2014.04.046.

Medeiros P, Dos Santos IR, Júnior IM, Palazzo E, da Silva JA, Machado HR, et al. An adapted chronic constriction injury of the sciatic nerve produces sensory, affective, and cognitive impairments: a peripheral mononeuropathy model for the study of comorbid neuropsychiatric disorders associated with neuropathic pain in rats. Pain Med. 2021;22(2): 338-351. DOI: 10.1093/pm/pnaa206.

Abed AR, Abed A, Banafshe HR, Malekabad ES, Gorgani-Firuzjaee S, Dadashi AR. Effect of biotin supplementation on neuropathic pain induced by chronic constriction of the sciatic nerve in the rat. Res Pharm Sci. 2021;16(3):250-259. DOI: 10.4103/1735-5362.314823.

Banafshe HR, Khoshnoud MJ, Abed A, Saghazadeh M, Mesdaghinia A. Vitamin D supplementation attenuates the behavioral scores of neuropathic pain in rats. Nutr Neurosci. 2019;22(10):700-705. DOI: 10.1080/1028415X.2018.1435485.

Banafshe HR, Hajhashemi V, Minaiyan M, Mesdaghinia A, Abed A. Antinociceptive effects of maprotiline in a rat model of peripheral neuropathic pain: possible involvement of opioid system. Iran J Basic Med Sci. 2015; 18(8):752-757. PMCID: PMC4633457.

Abed A, Hajhashemi V, Banafshe HR, Minaiyan M, Mesdaghinia A. Venlafaxine attenuates heat hyperalgesia independent of adenosine or opioid system in a rat model of peripheral neuropathy. Iran J Pharm Res. 2015;14(3):843-850. PMCID: PMC4518112.

Abed A, Khoshnoud MJ, Taghian M, Aliasgharzadeh M, Mesdaghinia A. Quetiapine reverses paclitaxel-induced neuropathic pain in mice: role of alpha2- adrenergic receptors. Iran J Basic Med Sci. 2017;20(11):1182-1188. DOI: 10.22038/IJBMS.2017.9500.

Naji-Esfahani H, Vaseghi G, Safaeian L, Pilehvarian AA, Abed A, Rafieian-Kopaei M. Gender differences in a mouse model of chemotherapy-induced neuropathic pain. Lab Anim. 2016;50(1):15-20 DOI: 10.1177/0023677215575863.

Hamidi GA, Jafari-Sabet M, Abed A, Mesdaghinia A, Mahlooji M, Banafshe HR. Gabapentin enhances anti-nociceptive effects of morphine on heat, cold, and mechanical hyperalgesia in a rat model of neuropathic pain. Iran J Basic Med Sci. 2014;17(10):753-759. PMCID: PMC4340982.

Amin B, Hajhashemi V, Hosseinzadeh H. Minocycline potentiates the anti-hyperalgesic effect of ceftriaxone in CCI-induced neuropathic pain in rats. Res Pharm Sci. 2015;10(1):34-42. PMCID: PMC4578210.

Chen SH, Huang TC, Wang JY, Wu CC, Hsueh YY. Controllable forces for reproducible chronic constriction injury mimicking compressive neuropathy in rat sciatic nerve. J Neurosci Methods. 2020;335:108615,1-37. DOI: 10.1016/j.jneumeth.2020.108615.

Heinricher MM. Pain modulation and the transition from acute to chronic pain. Adv Exp Med Biol. 2016;904:105-115. DOI: 10.1007/978-94-017-7537-3_8.

Hung CY, Tan CH. TRP Channels in nociception and pathological pain. Adv Exp Med Biol. 2018; 1099:13-27.DOI: 10.1007/978-981-13-1756-9_2.

Jensen TS, Finnerup NB. Allodynia and hyperalgesia in neuropathic pain: clinical manifestations and mechanisms. Lancet Neurol. 2014;13(9):924-935.DOI: 10.1016/S1474-4422(14)70102-4.

Amin B, Hosseinzadeh H. Black cumin (Nigella sativa) and its active constituent, thymoquinone: an overview on the analgesic and anti-inflammatory effects. Planta Med. 2016;82(1-2):8-16. DOI: 10.1055/s-0035-1557838.

Al-Ghamdi MS. The anti-inflammatory, analgesic and antipyretic activity of Nigella sativa. J Ethnopharmacol. 2001;76(1):45-48. DOI: 10.1016/s0378-8741(01)00216-1.

De Sousa DP, Nóbrega FFF, Santos CCMP, Benedito RB, Vieira YW, Uliana MP, et al. Antinociceptive activity thymoquinone and its structural analogues: a structure-activity relationship study. Trop J Pharm Res. 2012;11(4):605-610.DOI: 10.4314/tjpr.v11i4.11.

Bashir MU, Qureshi HJ. Analgesic effect of Nigella sativa seeds extract on experimentally induced pain in albino mice. J Coll Physicians Surg Pak. 2010;20(7):464-467.PMID: 20642947.

Atlante A, Calissano P, Bobba A, Azzariti A, Marra E, Passarella S. Cytochrome c is released from mitochondria in a reactive oxygen species (ROS)-dependent fashion and can operate as a ROS scavenger and as a respiratory substrate in cerebellar neurons undergoing excitotoxic death. J Biol Chem. 2000;275(47):37159-37166. DOI: 10.1074/jbc.M002361200.

AA Farooqui, WY Ong, LA Horrocks. Neurochemical Aspects of Excitotoxicity. Springer, New York, NY, USA, 2008. pp: 21-35. DOI: org/10.1007/978-0-387-73023-3.

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):413-417.DOI: 10.1111/jnc.12830.

Alkhalaf MI, Hussein RH, Hamza A. Green synthesis of silver nanoparticles by Nigella sativa extract alleviates diabetic neuropathy through anti-inflammatory and antioxidant effects. Saudi J Biol Sci. 2020;27(9):2410-2419. DOI: 10.1016/j.sjbs.2020.05.005.

Vafaee F, Hosseini M, Hassanzadeh Z, Edalatmanesh MA, Sadeghnia HR, Seghatoleslam M, et al. The effects of Nigella sativa hydro-alcoholic extract on memory and brain tissues oxidative damage after repeated seizures in rats. Iran J Pharm Res. 2015;14(2):547-557. PMCID: PMC4403072.

Ozugurlu F, Sahin S, Idiz N, Akyol O, Ilhan A, Yigitoglu R, et al. The effect of Nigella sativa oil against experimental allergic encephalomyelitis via nitric oxide and other oxidative stress parameters. Cell Mol Biol (Noisy-le-grand). 2005;51(3):337-342. PMID: 16191402.

Kamal A, Arif JM, Ahmad IZ. Potential of Nigella sativa L. seed during different phases of germination on inhibition of bacterial growth. J Biotech Pharm Res. 2010;1: 9-13.

Singh S, Das SS, Singh G, Schuff C, de Lampasona MP, Catalan CAN. Composition, in vitro antioxidant and antimicrobial activities of essential oil and oleoresins obtained from black cumin seeds (Nigella sativa L.). BioMed Res Int. 2014;2014:1-10.DOI: 10.1155/2014/918209.

El-Mahmoudy A, Matsuyama H, Borgan MA, Shimizu Y, El-Sayed MG, Minamoto N, et al. Thymoquinone suppresses expression of inducible nitric oxide synthase in rat macrophages. Int Immunopharmacol. 2002;2(11):1603-1611. DOI: 10.1016/s1567-5769(02)00139-x.

Lei X, Liu M, Yang Z, Ji M, Guo X, Dong W. Thymoquinone prevents and ameliorates dextran sulfate sodium-induced colitis in mice. Dig Dis Sci. 2012; 57(9):2296-2303.DOI: 10.1007/s10620-012-2156-x.

Norouzi F, Hosseini M, Abareshi A, Beheshti F, Khazaei M, Shafei MN, et al. Memory enhancing effect of Nigella sativa hydro-alcoholic extract on lipopolysaccharide-induced memory impairment in rats. Drug Chem Toxicol. 2019;42(3):270-279. DOI: 10.1080/01480545.2018.1447578.

Hosseinzadeh H, Parvardeh S, Nassiri-Asl M, Mansouri MT. Intracerebroventricular administration of thymoquinone, the major constituent of Nigella sativa seeds, suppresses epileptic seizures in rats. Med Sci Monit. 2005;11(4):BR106-BR110.PMID: 15795687.

Gilhotra N, Dhingra D. Thymoquinone produced antianxiety-like effects in mice through modulation of GABA and NO levels. Pharmacol Rep. 2011;63(3):660-669.DOI: 10.1016/s1734-1140(11)70577-1.

Enna SJ, McCarson KE. The role of GABA in the mediation and perception of pain. Adv Pharmacol. 2006;54:1-27. DOI: 10.1016/s1054-3589(06)54001-3.

Ossipov MH, Morimura K, Porreca F. Descending pain modulation and chronification of pain. Curr Opin Support Palliat Care. 2014;8(2):143-151. DOI: 10.1097/SPC.0000000000000055.

Perveen T, Haider S, Zuberi NA, Saleem S, Sadaf S, Batool Z. Increased 5-HT levels following repeated administration of Nigella sativa L. (black seed) oil produce antidepressant effects in rats. Sci Pharm. 2014;82(1):161-170. DOI:10.3797/scipharm.1304-19.


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