Anticancer potential of the Zanthoxylum genus: A review of phytochemistry and bioactivity

Pham Cao Bach, Tran Thi Tuyen, Trinh Anh Vien, Pham Thi Hong Minh, Pham Quoc Long, Nguyen Thi Hong Van
Author affiliations

Authors

  • Pham Cao Bach \(^1\) Institute of Natural Product Chemistry (INPC), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet street, Nghia Do, Ha Noi 10072, Viet Nam https://orcid.org/0000-0003-0999-4534
  • Tran Thi Tuyen \(^1\) Institute of Natural Product Chemistry (INPC), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet street, Nghia Do, Ha Noi 10072, Viet Nam
  • Trinh Anh Vien \(^2\) Department of Examination and Quality Assurance of Education, Hanoi Medical University-Thanh Hoa Campus, Quang Trung 3, Dong Ve, Thanh Hoa 40130, Viet Nam
  • Pham Thi Hong Minh \(^1\) Institute of Natural Product Chemistry (INPC), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet street, Nghia Do, Ha Noi 10072, Viet Nam
    \(^3\) Graduate University of Science and Technology (GUST), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet street, Nghia Do, Ha Noi 10072, Viet Nam
  • Pham Quoc Long \(^4\) Laboratory of Biophysics, Institute for Advanced Study in Technology, Ton Duc Thang University, 19 Nguyen Huu Tho, Tan Hung, Ho Chi Minh City 70000, Viet Nam
    \(^5\) Faculty of Pharmacy, Ton Duc Thang University, 19 Nguyen Huu Tho, Tan Hung, Ho Chi Minh City 70000, Viet Nam
  • Nguyen Thi Hong Van \(^1\) Institute of Natural Product Chemistry (INPC), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet street, Nghia Do, Ha Noi 10072, Viet Nam
    \(^3\) Graduate University of Science and Technology (GUST), Vietnam Academy of Science and Technology (VAST), 18 Hoang Quoc Viet street, Nghia Do, Ha Noi 10072, Viet Nam
    https://orcid.org/0000-0003-4152-1630

DOI:

https://doi.org/10.15625/2525-2518/22121

Keywords:

Zanthoxylum, anticancer, traditional use, extract, essential oil, secondary metabolites

Abstract

The Zanthoxylum genus, belonging to the Rutaceae family, comprises over 250 species and is widely distributed across Asia, Africa, Europe, and the Americas. These species have been appreciated their significance as both spices and medicinal plants with broad therapeutic applications, especially for cancer treatment. Zanthoxylum species via Z. nitidum, Z. armatum, Z. chalybeum, Z. bungeanum, Z. piperitum, Z. simulans, Z. capense, Z. schinifolium, and Z. zanthoxyloides were a rich source of cytotoxic components, including crude extracts, essential oils, secondary metabolite compounds, such as alkaloids, flavonoids, lignans, and coumarins that showed potential anticancer agents through many different mechanisms. However, there are some reports on the safety/toxicology of some Zanthoxylum species, and advice about using them for a long time must be narrowly supervised, as well as further toxicity investigations to access their safety before in vivo trials.

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References

1. Amponsah I. K., Opoku-Kwabi D., Armah F. A., Addotey J. N., Turkson B. K., Kontoh E. Q. - A Systematic Review of Medicinal Plants and Their Compounds Validated as Agents for the Management of Sickle Cell Disease. Nat. Prod. Commun., 19(9) (2024) https://doi.org/10.1177/1934578x241265889.

2. Cui Y., Wu L., Cao R., Xu H., Xia J., Wang Z. P., Ma J. - Antitumor functions and mechanisms of nitidine chloride in human cancers. J. Cancer, 11(5) (2020) 1250-1256. https://doi.org/10.7150/jca.37890.

3. Okagu I. U., Ndefo J. C., Aham E. C., Udenigwe C. C. - Zanthoxylum Species: A Review of Traditional Uses, Phytochemistry and Pharmacology in Relation to Cancer, Infectious Diseases and Sickle Cell Anemia. Front. Pharmacol., 12 (2021) 713090. https://doi.org/10.3389/fphar.2021.713090.

4. Wen J., Xiang Q., Guo J., Zhang J., Yang N., Huang Y., Chen Y., Hu T., Rao C. - Pharmacological activities of Zanthoxylum L. plants and its exploitation and utilization. Heliyon, 10(12) (2024) e33207. https://doi.org/10.1016/j.heliyon.2024.e33207.

5. Mutinda E. S., Kimutai F., Mkala E. M., Waswa E. N., Odago W. O., Nanjala C., Ndungu C. N., Gichua M. K., Njire M. M., Gituru R. W., Hu G. W. - Ethnobotanical uses, phytochemistry and pharmacology of pantropical genus Zanthoxylum L. (Rutaceae): An update. J. Ethnopharmacol., 303 (2023) 115895. https://doi.org/10.1016/j.jep.2022.115895.

6. Guillaumin A. - Rutacées. In: Flore générale de l'Indo-Chine. Masson, Paris (1911).

7. Chi V. V. - Dictionary of Vietnamese medicinal plants. Medical Publishing House, Vietnam (1997).

8. Ho P. H. - Cây cỏ Việt Nam: An illustrated Flora of VietNam. Tre Publishing House, Vietnam (2003).

9. Loi D. T. - Vietnamese medicinal plants and herbs. Medical Publishing House, Vietnam (2004).

10. Guillaumin A. - Rutacées. In: Supplément à la Flore générale de l'Indo-Chine. Masson, Paris (1946).

11. Ha B. T., Nguyen N. T., Lien N. T. H. - Taxonomical study on Zanthoxylum L. (Rutaceae) in Vietnam. VNU J. Sci. Nat. Sci. Technol., 26(2S) (2010) 101-110.

12. Ha B. T., Lien N. T. H., Quyen N. V., Dung V. T., Tung N. V. - Proceeding of the 4th National scientific conference on biological research and teaching in Vietnam, Publishing House for Science and Technology, (2020) 16-20.

13. Satria D., Silalahi J., Haro G., Ilyas S., Hasibuan P. A. Z. - Cell Cycle Inhibition of Ethylacetate Fraction of Zanthoxylum Acanthopodium DC. Fruit against T47D Cells. Open Access Maced. J. Med. Sci., 7(5) (2019) 726-729. https://doi.org/10.3889/oamjms.2019.178.

14. Syari D. M., Rosidah R., Hasibuan P. A. Z., Haro G., Satria D. - Evaluation of Cytotoxic Activity Alkaloid Fractions of Zanthoxylum acanthopodium DC. Fruits. Open Access Maced. J. Med. Sci., 7(22) (2019) 3745-3747. https://doi.org/10.3889/oamjms.2019.495.

15. Satria D., Silalahi J., Haro G., Ilyas S., Hasibuan Z. P. A. - Chemical analysis and cytotoxic activity of n-hexane fraction of Zanthoxylum acanthopodium DC. fruits. Rasayan J. Chem., 12(02) (2019) 803-808. https://doi.org/10.31788/rjc.2019.1225180.

16. Adrian, Syahputra R. A., Juwita N. A., Astyka R., Lubis M. F. - Andaliman (Zanthoxylum acanthopodium DC.) a herbal medicine from North Sumatera, Indonesia: Phytochemical and pharmacological review. Heliyon, 9(5) (2023) e16159. https://doi.org/10.1016/j.heliyon.2023.e16159.

17. Diep T. T., Dung L. V., Trung P. V., Hoai N. T., Thao D. T., Uyen N. T. T., Linh T. T. H., Ha T. H. N., Truc H. T. - Chemical Composition, Antimicrobial, Nitric Oxide Inhibition and Cytotoxic Activity of Essential Oils from Zanthoxylum acanthopodium DC. Leaves and Stems from Vietnam. Chem. Biodivers., 20(8) (2023) e202300649. https://doi.org/10.1002/cbdv.202300649.

18. Chou S. T., Chan H. H., Peng H. Y., Liou M. J., Wu T. S. - Isolation of substances with antiproliferative and apoptosis-inducing activities against leukemia cells from the leaves of Zanthoxylum ailanthoides Sieb. & Zucc. Phytomedicine, 18(5) (2011) 344-348. https://doi.org/10.1016/j.phymed.2010.08.018.

19. Chou S. T., Peng H. Y., Chang C. T., Yang J. S., Chung H. K., Yang S. T., Wood W. G., Chung J. G. - Zanthoxylum ailanthoides Sieb and Zucc. extract inhibits growth and induces cell death through G2/M-phase arrest and activation of apoptotic signals in colo 205 human colon adenocarcinoma cells. Anticancer Res., 31(5) (2011) 1667-1676.

20. Ju Y., Still C. C., Sacalis J. N., Li J., Ho C. T. - Cytotoxic coumarins and lignans from extracts of the northern prickly ash (Zanthoxylum americanum). Phytother. Res., 15(5) (2001) 441-443. https://doi.org/10.1002/ptr.686.

21. Alam F., Najum us Saqib Q., Waheed A. - Cytotoxic activity of extracts and crude saponins from Zanthoxylum armatum DC. against human breast (MCF-7, MDA-MB-468) and colorectal (Caco-2) cancer cell lines. BMC Complement. Altern. Med., 17(1) (2017) 368. https://doi.org/10.1186/s12906-017-1882-1.

22. Alam F., Najum us Saqib Q. - Evaluation of Zanthoxylum armatum Roxb for in vitro biological activities. J. Tradit. Complement. Med., 7(4) (2017) 515-518. https://doi.org/10.1016/j.jtcme.2017.01.006.

23. Mukhija M., Lal Dhar K., Nath Kalia A. - Bioactive Lignans from Zanthoxylum alatum Roxb. stem bark with cytotoxic potential. J. Ethnopharmacol., 152(1) (2014) 106-112. https://doi.org/10.1016/j.jep.2013.12.039.

24. Singh T. D., Meitei H. T., Sharma A. L., Robinson A., Singh L. S., Singh T. R. - Anticancer properties and enhancement of therapeutic potential of cisplatin by leaf extract of Zanthoxylum armatum DC. Biol. Res., 48(1) (2015) 46. https://doi.org/10.1186/s40659-015-0037-4.

25. Phuyal N., Jha P. K., Raturi P. P., Rajbhandary S. - Zanthoxylum armatum DC.: Current knowledge, gaps and opportunities in Nepal. J. Ethnopharmacol., 229 (2019) 326-341. https://doi.org/10.1016/j.jep.2018.08.010.

26. Islam A., Sayeed A., Bhuiyan M. S. A., Mosaddik M. A., Islam M. A. U., Astaq Mondal Khan G. R. M. - Antimicrobial activity and cytotoxicity of Zanthoxylum budrunga. Fitoterapia, 72(4) (2001) 428-430. https://doi.org/10.1016/s0367-326x(00)00336-1.

27. Sandjo L. P., Kuete V., Tchangna R. S., Efferth T., Ngadjui B. T. - Cytotoxic Benzophenanthridine and Furoquinoline Alkaloids from Zanthoxylum buesgenii (Rutaceae). Chem. Cent. J., 8(1) (2014) 61. https://doi.org/10.1186/s13065-014-0061-4.

28. Zhang M., Wang J., Zhu L., Li T., Jiang W., Zhou J., Peng W., Wu C. - Zanthoxylum bungeanum Maxim. (Rutaceae): A Systematic Review of Its Traditional Uses, Botany, Phytochemistry, Pharmacology, Pharmacokinetics, and Toxicology. Int. J. Mol. Sci., 18(10) (2017) https://doi.org/10.3390/ijms18102172.

29. Zhang Y., Dong H., Zhang J., Zhang L. - Inhibitory effect of hyperoside isolated from Zanthoxylum bungeanum leaves on SW620 human colorectal cancer cells via induction of the p53 signaling pathway and apoptosis. Mol. Med. Rep., 16(2) (2017) 1125-1132. https://doi.org/10.3892/mmr.2017.6710.

30. Bodede O., Shaik S., Singh M., Moodley R. - Phytochemical Analysis with Antioxidant and Cytotoxicity Studies of the Bioactive Principles from Zanthoxylum capense (Small Knobwood). Anticancer Agents Med. Chem., 17(4) (2017) 627-634. https://doi.org/10.2174/1871520616666160627091939.

31. Luo X., Pires D., Ainsa J. A., Gracia B., Mulhovo S., Duarte A., Anes E., Ferreira M. J. - Antimycobacterial evaluation and preliminary phytochemical investigation of selected medicinal plants traditionally used in Mozambique. J. Ethnopharmacol., 137(1) (2011) 114-120. https://doi.org/10.1016/j.jep.2011.04.062.

32. da Silva F. B., Santos N. O. D., Pascon R. C., Vallim M. A., Figueiredo C. R., Martins R. C. C., Sartorelli P. - Chemical Composition and In Vitro Cytotoxic and Antimicrobial Activities of the Essential Oil from Leaves of Zanthoxylum monogynum St. Hill (Rutaceae). Medicines (Basel), 4(2) (2017) https://doi.org/10.3390/medicines4020031.

33. Omosa L. K., Mbogo G. M., Korir E., Omole R., Seo E. J., Yenesew A., Heydenreich M., Midiwo J. O., Efferth T. - Cytotoxicity of fagaramide derivative and canthin-6-one from Zanthoxylum (Rutaceae) species against multidrug resistant leukemia cells. Nat. Prod. Res., 35(4) (2021) 579-586. https://doi.org/10.1080/14786419.2019.1587424.

34. Waiganjo B., Moriasi G., Onyancha J., Elias N., Muregi F. - Antiplasmodial and Cytotoxic Activities of Extracts of Selected Medicinal Plants Used to Treat Malaria in Embu County, Kenya. J. Parasitol. Res., 2020 (2020) 8871375. https://doi.org/10.1155/2020/8871375.

35. Anywar G., Kakudidi E., Byamukama R., Mukonzo J., Schubert A., Oryem-Origa H., Jassoy C. - A Review of the Toxicity and Phytochemistry of Medicinal Plant Species Used by Herbalists in Treating People Living With HIV/AIDS in Uganda. Front. Pharmacol., 12 (2021) 615147. https://doi.org/10.3389/fphar.2021.615147.

36. Ross S. A., Sultana G. N., Burandt C. L., ElSohly M. A., Marais J. P., Ferreira D. - Syncarpamide, a new antiplasmodial (+)-norepinephrine derivative from Zanthoxylum syncarpum. J. Nat. Prod., 67(1) (2004) 88-90. https://doi.org/10.1021/np030417t.

37. Boehme A. K., Noletto J. A., Haber W. A., Setzer W. N. - Bioactivity and chemical composition of the leaf essential oils of Zanthoxylum rhoifolium and Zanthoxylum setulosum from Monteverde, Costa Rica. Nat. Prod. Res., 22(1) (2008) 31-36. https://doi.org/10.1080/14786410601130224.

38. Wouatsa N. A. V., Misra L. N., Venkatesh R. K., Darokar M. P., Tchoumbougnang F. - Zantholic acid, a new monoterpenoid from Zanthoxylum zanthoxyloides. Nat. Prod. Res., 27(21) (2013) 1994-1998. https://doi.org/10.1080/14786419.2013.811662.

39. Ngoumfo R. M., Jouda J. B., Mouafo F. T., Komguem J., Mbazoa C. D., Shiao T. C., Choudhary M. I., Laatsch H., Legault J., Pichette A., Roy R. - In vitro cytotoxic activity of isolated acridones alkaloids from Zanthoxylum leprieurii Guill. et Perr. Bioorg. Med. Chem., 18(10) (2010) 3601-3605. https://doi.org/10.1016/j.bmc.2010.03.040.

40. Misra L. N., Wouatsa N. A., Kumar S., Kumar R. V., Tchoumbougnang F. - Antibacterial, cytotoxic activities and chemical composition of fruits of two Cameroonian Zanthoxylum species. J. Ethnopharmacol., 148(1) (2013) 74-80. https://doi.org/10.1016/j.jep.2013.03.069.

41. Obakiro S. B., Kiprop A., Kowino I., Kigondu E., Odero M. P., Omara T., Bunalema L. - Ethnobotany, ethnopharmacology, and phytochemistry of traditional medicinal plants used in the management of symptoms of tuberculosis in East Africa: a systematic review. Trop. Med. Health, 48 (2020) 68. https://doi.org/10.1186/s41182-020-00256-1.

42. Chen Z. F., Liu Y. C., Liu L. M., Wang H. S., Qin S. H., Wang B. L., Bian H. D., Yang B., Fun H. K., Liu H. G., Liang H., Orvig C. - Potential new inorganic antitumour agents from combining the anticancer traditional Chinese medicine (TCM) liriodenine with metal ions, and DNA binding studies. Dalton Trans., (2) (2009) 262-272. https://doi.org/10.1039/b813363h.

43. Hu J., Shi X., Mao X., Chen J., Li H. - Cytotoxic mannopyranosides of indole alkaloids from Zanthoxylum nitidum. Chem. Biodivers., 11(6) (2014) 970-974. https://doi.org/10.1002/cbdv.201300381.

44. Liu H., Feng J., Feng K., Lai M. - Optimization of the extraction conditions and quantification by RP-LC analysis of three alkaloids in Zanthoxylum nitidum roots. Pharm. Biol., 52(2) (2014) 255-261. https://doi.org/10.3109/13880209.2013.826244.

45. Lu Q., Ma R., Yang Y., Mo Z., Pu X., Li C. - Zanthoxylum nitidum (Roxb.) DC: Traditional uses, phytochemistry, pharmacological activities and toxicology. J. Ethnopharmacol., 260 (2020) 112946. https://doi.org/10.1016/j.jep.2020.112946.

46. Wang C. F., Fan L., Tian M., Du S. S., Deng Z. W., Feng J. B., Wang Y. Y., Su X. - Cytotoxicity of benzophenanthridine alkaloids from the roots of Zanthoxylum nitidum (Roxb.) DC. var. fastuosum How ex Huang. Nat. Prod. Res., 29(14) (2015) 1380-1383. https://doi.org/10.1080/14786419.2014.1002090.

47. Kaigongi M. M., Lukhoba C. W., Yaouba S., Makunga N. P., Githiomi J., Yenesew A. - In Vitro Antimicrobial and Antiproliferative Activities of the Root Bark Extract and Isolated Chemical Constituents of Zanthoxylum paracanthum Kokwaro (Rutaceae). Plants (Basel), 9(7) (2020) https://doi.org/10.3390/plants9070920.

48. Park C., Choi E. O., Hwangbo H., Lee H., Jeong J. W., Han M. H., Moon S. K., Yun S. J., Kim W. J., Kim G. Y., Hwang H. J., Choi Y. H. - Induction of apoptotic cell death in human bladder cancer cells by ethanol extract of Zanthoxylum schinifolium leaf, through ROS-dependent inactivation of the PI3K/Akt signaling pathway. Nutr. Res. Pract., 16(3) (2022) 330-343. https://doi.org/10.4162/nrp.2022.16.3.330.

49. Park Y. S., Nam G. H., Jo K. J., Kawk H. W., Kim S. Y., Kim Y. M. - Extract from Zanthoxylum piperitum Induces Apoptosis of AGS Gastric Cancer Cells Through Akt/MDM2/p53 Signaling Pathway. Chin. J. Integr. Med., 27(10) (2021) 752-759. https://doi.org/10.1007/s11655-021-3486-8.

50. Lee J., Lee S. J., Lim K. T. - Preventive effects of ZPDC glycoprotein (24 kDa) on hepatotoxicity induced by mercury chloride in vitro and in vivo. Cell Biochem. Funct., 32(6) (2014) 520-529. https://doi.org/10.1002/cbf.3046.

51. Maduka T. O., Ikpa C. B. C. - Zanthoxylum rhetsa (Roxb.) DC.: A Systemic Review of its Ethnomedicinal Properties, Phytochemistry and Pharmacology. World News Nat. Sci., 37 (2021) 41-57.

52. Ahsan M., Haque M. R., Hossain M. B., Islam S. N., Gray A. I., Hasan C. M. - Cytotoxic dimeric quinolone-terpene alkaloids from the root bark of Zanthoxylum rhetsa. Phytochemistry, 103 (2014) 8-12. https://doi.org/10.1016/j.phytochem.2014.03.008.

53. da Silva T. B., Costa C. O., Galvao A. F., Bomfim L. M., Rodrigues A. C., Mota M. C., Dantas A. A., Dos Santos T. R., Soares M. B., Bezerra D. P. - Cytotoxic potential of selected medicinal plants in northeast Brazil. BMC Complement. Altern. Med., 16 (2016) 199. https://doi.org/10.1186/s12906-016-1166-1.

54. Li W., Sun Y. N., Yan X. T., Yang S. Y., Kim E. J., Kang H. K., Kim Y. H. - Coumarins and lignans from Zanthoxylum schinifolium and their anticancer activities. J. Agric. Food Chem., 61(45) (2013) 10730-10740. https://doi.org/10.1021/jf403479c.

55. Wang C., Wan J., Mei Z., Yang X. - Acridone alkaloids with cytotoxic and antimalarial activities from Zanthoxylum simulans Hance. Pharmacogn. Mag., 10(37) (2014) 73-76. https://doi.org/10.4103/0973-1296.126669.

56. Ozkan M., Mutiso P. B., Nahar L., Liu P., Brown S., Wang W., Sarker S. D. - Zanthoxylum usambarense (Engl.) Kokwaro (Rutaceae) extracts inhibit the growth of the breast cancer cell lines MDA-MB-231 and MCF-7, but not the brain tumour cell line U251 in vitro. Phytother. Res., 27(5) (2013) 787-790. https://doi.org/10.1002/ptr.4775.

57. Kassim O. O., Copeland R. L., Kenguele H. M., Nekhai S., Ako-Nai K. A., Kanaan Y. M. - Antiproliferative activities of Fagara xanthoxyloides and Pseudocedrela kotschyi against prostate cancer cell lines. Anticancer Res., 35(3) (2015) 1453-1458.

58. Ogunbolude Y., Ibrahim M., Elekofehinti O. O., Adeniran A., Abolaji A. O., Rocha J. B., Kamdem J. P. - Effects of Tapinanthus globiferus and Zanthoxylum zanthoxyloides extracts on human leukocytes in vitro. J. Intercult. Ethnopharmacol., 3(4) (2014) 167-172. https://doi.org/10.5455/jice.20140826110059.

59. Kumar S., Muller K. - Inhibition of keratinocyte growth by different Nepalese zanthoxylum species. Phytother. Res., 13(3) (1999) 214-217. https://doi.org/10.1002/(SICI)1099-1573(199905)13:3<214::AID-PTR431>3.0.CO;2-2.

60. Simanullang R. H., Situmorang P. C., Herlina M., Noradina, Silalahi B., Manurung S. S. - Histological changes of cervical tumours following Zanthoxylum acanthopodium DC treatment, and its impact on cytokine expression. Saudi J. Biol. Sci., 29(4) (2022) 2706-2718. https://doi.org/10.1016/j.sjbs.2021.12.065.

61. Tian Y., Zhang C., Guo M. - Comparative study on alkaloids and their anti-proliferative activities from three Zanthoxylum species. BMC Complement. Altern. Med., 17(1) (2017) 460. https://doi.org/10.1186/s12906-017-1966-y.

62. Epifano F., Curini M., Marcotullio M. C., Genovese S. - Searching for novel cancer chemopreventive plants and their products: the genus Zanthoxylum. Curr. Drug Targets, 12(13) (2011) 1895-1902. https://doi.org/10.2174/138945011798184128.

63. Tseng T. H., Wang C. J., Lee Y. J., Shao Y. C., Shen C. H., Lee K. C., Tung S. Y., Kuo H. C. - Suppression of the Proliferation of Huh7 Hepatoma Cells Involving the Downregulation of Mutant p53 Protein and Inactivation of the STAT 3 Pathway with Ailanthoidol. Int. J. Mol. Sci., 23(9) (2022) https://doi.org/10.3390/ijms23095102.

64. Afzal M., Qais F. A., Abduh N. A. Y., Christy M., Ayub R., Alarifi A. - Identification of bioactive compounds of Zanthoxylum armatum as potential inhibitor of pyruvate kinase M2 (PKM2): Computational and virtual screening approaches. Heliyon, 10(5) (2024) e27361. https://doi.org/10.1016/j.heliyon.2024.e27361.

65. Islam M. K., Acharzo A. K., Saha S., Hossain H., Shilpi J. A., Das A. K., Biswas N. N. - Bioactivity studies on Zanthoxylum budrunga wall (Rutaceae) root bark. Clin. Phytosci., 4(24) (2018) https://doi.org/10.1186/s40816-018-0084-9.

66. Khan I. N., Sarker M. I., Almamun A., Mazumder K., Bhuiya M. A. M., Mannan A. - Cytotoxic and thrombolytic activity of ethanolic extract of Zanthoxylum budrunga (Fam: Rutaceae) leaves. Eur. J. Sci. Res., 66(2) (2011) 303-310.

67. Islam A., Sayeed A., Islam M. A. U., Astaq Mondal Khan G. R. M., Biswas M. H. U., Bhuiyan M. S. A. - A Flavonone from Leaves of Zanthoxylum budrunga: its In vitro Antimicrobial Activity and Cytotoxic Evaluation. J. Med. Sci., 1(4) (2001) 209-213. https://doi.org/10.3923/jms.2001.209.213.

68. Islam M. A., Sayeed M. A., Islam M. A., Khan G. R. M. A. M., Mosaddik M. A., Bhuiyan M. S. A. - Terpenes from bark of Zanthoxylum budrunga and their cytotoxic activities. Rev. Latinoam. Quim., 30(1) (2002) 24-28.

69. Meng X. H., Chai T., Shi Y. P., Yang J. L. - Bungsteroid A: One Unusual C(34) Pentacyclic Steroid Analogue from Zanthoxylum bungeanum Maxim. J. Org. Chem., 85(16) (2020) 10806-10812. https://doi.org/10.1021/acs.joc.0c01312.

70. Chen Z., Tan L., Feng X., Singab A. N., Lei Z., Liu X. - Hydroxy-gamma-sanshool from Zanthoxylum bungeanum (prickly ash) induces apoptosis of human colorectal cancer cell by activating P53 and Caspase 8. Front. Nutr., 9 (2022) 914638. https://doi.org/10.3389/fnut.2022.914638.

71. Li K., Zhou R., Wang Jia W., Li Z., Li J., Zhang P., Xiao T. - Zanthoxylum bungeanum essential oil induces apoptosis of HaCaT human keratinocytes. J. Ethnopharmacol., 186 (2016) 351-361. https://doi.org/10.1016/j.jep.2016.03.054.

72. Pang W., Liu S., He F., Li X., Saira B., Zheng T., Chen J., Dong K., Pei X. F. - Anticancer activities of Zanthoxylum bungeanum seed oil on malignant melanoma. J. Ethnopharmacol., 229 (2019) 180-189. https://doi.org/10.1016/j.jep.2018.10.012.

73. Wang W., Pang W., Yan S., Zheng X., Han Q., Yao Y., Jin L., Zhang C. - Zanthoxylum bungeanum seed oil inhibits tumorigenesis of human melanoma A375 by regulating CDC25A/CyclinB1/CDK1 signaling pathways in vitro and in vivo. Front. Pharmacol., 14 (2023) 1165584. https://doi.org/10.3389/fphar.2023.1165584.

74. Seoposengwe K., van Tonder J. J., Steenkamp V. - In vitro neuroprotective potential of four medicinal plants against rotenone-induced toxicity in SH-SY5Y neuroblastoma cells. BMC Complement. Altern. Med., 13 (2013) 353. https://doi.org/10.1186/1472-6882-13-353.

75. Mansoor T. A., Borralho P. M., Luo X., Mulhovo S., Rodrigues C. M., Ferreira M. J. - Apoptosis inducing activity of benzophenanthridine-type alkaloids and 2-arylbenzofuran neolignans in HCT116 colon carcinoma cells. Phytomedicine, 20(10) (2013) 923-929. https://doi.org/10.1016/j.phymed.2013.03.026.

76. Mansoor T. A., Borralho P. M., Luo X., Mulhovo S., Rodrigues C. M., Ferreira M. J. - 6-Acetonyldihydrochelerythrine Is a Potent Inducer of Apoptosis in HCT116 and SW620 Colon Cancer Cells. J. Nat. Prod., 77(8) (2014) 1825-1830. https://doi.org/10.1021/np500161n.

77. Nibret E., Ashour M. L., Rubanza C. D., Wink M. - Screening of some Tanzanian medicinal plants for their trypanocidal and cytotoxic activities. Phytother. Res., 24(6) (2010) 945-947. https://doi.org/10.1002/ptr.3066.

78. Dzoyem J. P., Guru S. K., Pieme C. A., Kuete V., Sharma A., Khan I. A., Saxena A. K., Vishwakarma R. A. - Cytotoxic and antimicrobial activity of selected Cameroonian edible plants. BMC Complement. Altern. Med., 13 (2013) 78. https://doi.org/10.1186/1472-6882-13-78.

79. Wouatsa V. N., Misra L., Kumar S., Prakash O., Khan F., Tchoumbougnang F., Venkatesh R. K. - Aromatase and glycosyl transferase inhibiting acridone alkaloids from fruits of Cameroonian Zanthoxylum species. Chem. Cent. J., 7 (2013) 125. https://doi.org/10.1186/1752-153X-7-125.

80. Dupuy L. O. A., Bonilla V. J. A., Murillo R., Taylor P., Abad M. J., González L., Johanna J. A. - Efecto in vitro de los terpenos lupeol y casearina G sobre células sanguíneas y tumorales. Rev. Med. Chile, 141(9) (2013) 1150-1157. https://doi.org/10.4067/S0034-98872013000900007.

81. Diep T. T., Dung L. V., Trung P. V., Thao D. T., Hoai N. T., Uyen N. T. T., Linh T. T. H., Truc H. T., Tran L. T. T., Ngoc V. T. B. - Chemical Composition, Anti-Inflammatory and Cytotoxic Activities of Essential Oils from Zanthoxylum myriacanthum Wall. ex Hook. f. Fruits, Leaves and Stems Collected in Lam Dong Province. J. Med. Mater. Hanoi, 28(6) (2023) 343-351.

82. Phuong T. H., Quan P. M., Bach P. C., Tuyen T. T., Nga N. P., Cuc N. T., Thao D. T., Van N. T. H. - Nitidine Isolated from the Bark of Zanthoxylum myriacanthum and its Effects on NTERA-2 Cancer Stem Cells. Planta Med., (EFirst) (2025) https://doi.org/10.1055/a-2654-6627.

83. Yang C. H., Cheng M. J., Lee S. J., Yang C. W., Chang H. S., Chen I. S. - Secondary metabolites and cytotoxic activities from the stem bark of Zanthoxylum nitidum. Chem. Biodivers., 6(6) (2009) 846-857. https://doi.org/10.1002/cbdv.200800107.

84. Liu Y. C., Chen Z. F., Liu L. M., Peng Y., Hong X., Yang B., Liu H. G., Liang H., Orvig C. - Divalent later transition metal complexes of the traditional chinese medicine (TCM) liriodenine: coordination chemistry, cytotoxicity and DNA binding studies. Dalton Trans., (48) (2009) 10813-10823. https://doi.org/10.1039/B912553A.

85. Chen Z. F., Liu Y. C., Peng Y., Hong X., Wang H. H., Zhang M. M., Liang H. - Synthesis, characterization, and in vitro antitumor properties of gold(III) compounds with the traditional Chinese medicine (TCM) active ingredient liriodenine. J. Biol. Inorg. Chem., 17(2) (2012) 247-261. https://doi.org/10.1007/s00775-011-0846-z.

86. Chen J., Wang J., Lin L., He L., Wu Y., Zhang L., Yi Z., Chen Y., Pang X., Liu M. - Inhibition of STAT3 signaling pathway by nitidine chloride suppressed the angiogenesis and growth of human gastric cancer. Mol. Cancer Ther., 11(2) (2012) 277-287. https://doi.org/10.1158/1535-7163.MCT-11-0648.

87. Kim L. H., Khadka S., Shin J. A., Jung J. Y., Ryu M. H., Yu H. J., Lee H. N., Jang B., Yang I. H., Won D. H., Kwon H. J., Jeong J. H., Hong S. D., Cho N. P., Cho S. D. - Nitidine chloride acts as an apoptosis inducer in human oral cancer cells and a nude mouse xenograft model via inhibition of STAT3. Oncotarget, 8(53) (2017) 91306-91315. https://doi.org/10.18632/oncotarget.20444.

88. Liu L. M., Lin P., Yang H., Dang Y. W., Chen G. - Gene profiling of HepG2 cells following nitidine chloride treatment: An investigation with microarray and Connectivity Mapping. Oncol. Rep., 41(6) (2019) 3244-3256. https://doi.org/10.3892/or.2019.7091.

89. Fang Z., Tang Y., Jiao W., Xing Z., Guo Z., Wang W., Xu Z., Liu Z. - Nitidine chloride induces apoptosis and inhibits tumor cell proliferation via suppressing ERK signaling pathway in renal cancer. Food Chem. Toxicol., 66 (2014) 210-216. https://doi.org/10.1016/j.fct.2014.01.049.

90. Li W., Yin H., Bardelang D., Xiao J., Zheng Y., Wang R. - Supramolecular formulation of nitidine chloride can alleviate its hepatotoxicity and improve its anticancer activity. Food Chem. Toxicol., 109(Pt 2) (2017) 923-929. https://doi.org/10.1016/j.fct.2017.02.022.

91. Liu J., Zhang Q., Ye Y., Li W., Qiu J., Liu J., Zhan R., Chen W., Yu Q. - Angoline: a selective IL-6/STAT3 signaling pathway inhibitor isolated from Zanthoxylum nitidum. Phytomedicine, 21(8-9) (2014) 1088-1091. https://doi.org/10.1016/j.phymed.2014.04.001.

92. Fan C. W., Luo L., Li M. S., Gu Y. Q., Fang Y. L., Qin F., Wang H. S. - Sesquilignans PD from Zanthoxylum nitidum var. tomentosum exerts antitumor effects via the ROS/MAPK pathway in liver cancer cells. J. Asian Nat. Prod. Res., (2024) 1-13. https://doi.org/10.1080/10286020.2024.2371032.

93. Qin F., Luo L., Chen Y., Wei G., Wei C. C., Yang X. H., Fang Y. L., Wang H. S. - A new phenylpropanoic acid congener from Zanthoxylum nitidum. Nat. Prod. Res., 38(14) (2024) 2404-2410. https://doi.org/10.1080/14786419.2023.2176490.

94. Omosa L. K., Nchiozem-Ngnitedem V. A., Mukavi J., Okoko B. A., Nyaboke H. O., Hashim I., Matundura J. O., Efferth T., Spiteller M. - Cytotoxic alkaloids from the root of Zanthoxylum paracanthum (mildbr) Kokwaro. Nat. Prod. Res., 36(10) (2022) 2518-2525. https://doi.org/10.1080/14786419.2021.1913586.

95. Nozaki R., Kono T., Bochimoto H., Watanabe T., Oketani K., Sakamaki Y., Okubo N., Nakagawa K., Takeda H. - Zanthoxylum fruit extract from Japanese pepper promotes autophagic cell death in cancer cells. Oncotarget, 7(43) (2016) 70437-70446. https://doi.org/10.18632/oncotarget.11926.

96. Nagata T., Toume K., Long L. X., Hirano K., Watanabe T., Sekine S., Okumura T., Komatsu K., Tsukada K. - Anticancer effect of a Kampo preparation Daikenchuto. J. Nat. Med., 70(3) (2016) 627-633. https://doi.org/10.1007/s11418-016-0989-x.

97. Ahsan M., Zaman T. A., Hasan C. M., Ito C., Islam S. K. N. - Constituents and cytotoxicity of Zanthoxylum rhesta stem bark. Fitoterapia, 71(6) (2000) 697-700. https://doi.org/10.1016/S0367-326X(00)00214-8.

98. Mallya R., Bhitre M. J. - Cytotoxic Activity and Initiation of Apoptosis via Intrinsic Pathway in Jurkat Cells by Leaf Extract of Zanthoxylum rhetsa DC. Nutr. Cancer, 73(9) (2021) 1768-1779. https://doi.org/10.1080/01635581.2020.1808231.

99. Lookpan T., Voravuthikunchai S. P., Sitthisuk P., Poorahong W., Watanapokasin R., Chakthong S. - A new alkaloid and a new benzaldehyde derivative from the twig of Zanthoxylum rhetsa (Roxb.) DC. Nat. Prod. Res., 38(3) (2024) 463-469. https://doi.org/10.1080/14786419.2022.2127708.

100. Van N. T. H., Tuyen T. T., Nghi D. H., Quan P. M., Bach P. C., Hiep D. H., Lam D. T., Minh P. T. H. - A new benzophenanthridine alkaloid from stem bark of Zanthoxylum rhetsa and its biological activities. Nat. Prod. Res., (2023) 1-13. https://doi.org/10.1080/14786419.2023.2297261.

101. da Costa J. G., Campos A. R., Brito S. A., Pereira C. K., Souza E. O., Rodrigues F. F. - Biological screening of araripe basin medicinal plants using Artemia salina Leach and pathogenic bacteria. Pharmacogn. Mag., 6(24) (2010) 331-334. https://doi.org/10.4103/0973-1296.71792.

102. da Silva S. L., Figueiredo P. M., Yano T. - Cytotoxic evaluation of essential oil from Zanthoxylum rhoifolium Lam. leaves. Acta Amazon., 37(2) (2007) 281-286. https://doi.org/10.1590/s0044-59672007000200015.

103. Chon S. U., Heo B. G., Park Y. S., Kim D. K., Gorinstein S. - Total phenolics level, antioxidant activities and cytotoxicity of young sprouts of some traditional Korean salad plants. Plant Foods Hum. Nutr., 64(1) (2009) 25-31. https://doi.org/10.1007/s11130-008-0092-x.

104. Min B. K., Hyun D. G., Jeong S. Y., Kim Y. H., Ma E. S., Woo M. H. - A new cytotoxic coumarin, 7-[(E)-3',7'-dimethyl-6'-oxo-2',7'-octadienyl] oxy coumarin, from the leaves of Zanthoxylum schinifolium. Arch. Pharm. Res., 34(5) (2011) 723-726. https://doi.org/10.1007/s12272-011-0504-6.

105. Jun D. Y., Kim J. S., Park H. S., Han C. R., Fang Z., Woo M. H., Rhee I. K., Kim Y. H. - Apoptogenic activity of auraptene of Zanthoxylum schinifolium toward human acute leukemia Jurkat T cells is associated with ER stress-mediated caspase-8 activation that stimulates mitochondria-dependent or -independent caspase cascade. Carcinogenesis, 28(6) (2007) 1303-1313. https://doi.org/10.1093/carcin/bgm028.

106. Wang C. F., Fan L., Tian M., Qi X. S., Liu J. X., Feng J. B., Du S. S., Su X., Wang Y. Y. - Radiosensitizing effect of schinifoline from Zanthoxylum schinifolium Sieb et Zucc on human non-small cell lung cancer A549 cells: a preliminary in vitro investigation. Molecules, 19(12) (2014) 20128-20138. https://doi.org/10.3390/molecules191220128.

107. Paik S. Y., Koh K. H., Beak S. M., Paek S. H., Kim J. A. - The Essential Oils from Zanthoxylum schinifolium Pericarp Induce Apoptosis of HepG2 Human Hepatoma Cells through Increased Production of Reactive Oxygen Species. Biol. Pharm. Bull., 28(5) (2005) 802-807. https://doi.org/10.1248/bpb.28.802.

108. Walker T. M., Vogler B., Moriarity D. M., Haber W. A., Setzer W. N. - A phytochemical investigation of Zanthoxylum setulosum. Nat. Prod. Commun., 6(12) (2011) 1807-1808.

109. Chen I. S., Wu S. J., Tsai I. L. - Chemical and bioactive constituents from Zanthoxylum simulans. J. Nat. Prod., 57(9) (1994) 1206-1211. https://doi.org/10.1021/np50111a003.

110. Ahn C., Lee J. H., Park M. J., Kim J. W., Yang J., Yoo Y. M., Jeung E. B. - Cytostatic effects of plant essential oils on human skin and lung cells. Exp. Ther. Med., 19(3) (2020) 2008-2018. https://doi.org/10.3892/etm.2020.8460.

111. Acheampong D. O., Baffour I. K., Atsu Barku V. Y., Addo J. K., Essuman M. A., Boye A. - Zanthoxylum zanthoxyloides Alkaloidal Extract Improves CCl(4)-Induced Hepatocellular Carcinoma-Like Phenotypes in Rats. Evid. Based Complement. Altern. Med., 2021 (2021) 3804379. https://doi.org/10.1155/2021/3804379.

112. Andima M., Coghi P. S., Yang L. J., Wong V. K. W., Ngule C. M., Heydenreich M., Ndakala A. J., Yenesew A., Derese S. - Antiproliferative Activity of Secondary Metabolites from Zanthoxylum zanthoxyloides Lam: In vitro and in silico Studies. Pharmacogn. Commun., 10(1) (2020) 44-51. https://doi.org/10.5530/pc.2020.1.8.

113. Fu Y. H., Guo J. M., Xie Y. T., Hua J., Dai Y. Y., Zhang W., Lin T. C., Liu Y. P. - Structural characterization, antiproliferative and anti-inflammatory activities of alkaloids from the roots of Zanthoxylum austrosinense. Bioorg. Chem., 102 (2020) 104101. https://doi.org/10.1016/j.bioorg.2020.104101.

114. Ferreira M. E., Cebrian-Torrejon G., Corrales A. S., Vera de Bilbao N., Rolon M., Gomez C. V., Leblanc K., Yaluf G., Schinini A., Torres S., Serna E., Rojas de Arias A., Poupon E., Fournet A. - Zanthoxylum chiloperone leaves extract: first sustainable Chagas disease treatment. J. Ethnopharmacol., 133(3) (2011) 986-993. https://doi.org/10.1016/j.jep.2010.11.032.

115. Garcia I. A., Pansa M. F., Pacciaroni A. D. V., Garcia M. E., Gonzalez M. L., Oberti J. C., Bocco J. L., Carpinella M. C., Barboza G. E., Nicotra V. E., Soria G. - Synthetic Lethal Activity of Benzophenanthridine Alkaloids From Zanthoxylum coco Against BRCA1-Deficient Cancer Cells. Front. Pharmacol., 11 (2020) 593845. https://doi.org/10.3389/fphar.2020.593845.

116. Setzer W. N., Schmidt J. M., Eiter L. C. - The Leaf Oil Composition of Zanthoxylum fagara (L.) Sarg. from Monteverde, Costa Rica, and its Biological Activities. J. Essent. Oil Res., 17(3) (2005) 333-335. https://doi.org/10.1080/10412905.2005.9698923.

117. Mbaveng A. T., Damen F., Celik I., Tane P., Kuete V., Efferth T. - Cytotoxicity of the crude extract and constituents of the bark of Fagara tessmannii towards multi-factorial drug resistant cancer cells. J. Ethnopharmacol., 235 (2019) 28-37. https://doi.org/10.1016/j.jep.2019.01.031.

118. Chen J. J., Fang H. Y., Duh C. Y., Chen I. S. - New indolopyridoquinazoline, benzo[c]phenanthridines and cytotoxic constituents from Zanthoxylum integrifoliolum. Planta Med., 71(5) (2005) 470-475. https://doi.org/10.1055/s-2005-864144.

119. Pachon G., Rasoanaivo H., Azqueta A., Rakotozafy J. C., Raharisololalao A., De Cerain A. L., De Lapuente J., Borras M., Moukha S., Centelles J. J., Creppy E. E., Cascante M. - Anticancer effect of a new benzophenanthridine isolated from Zanthoxylum madagascariense (Rutaceline). In Vivo, 21(2) (2007) 417-422.

120. Chen J. J., Huang H. Y., Duh C. Y., Chen I. S. - Cytotoxic Constituents from the Stem Bark of Zanthoxylum Pistaciiflorum. J. Chin. Chem. Soc., 51(3) (2004) 659-663. https://doi.org/10.1002/jccs.200400099.

121. Silva T. C. C., de Faria Lopes G. P., de J. Menezes-Filho N., de Oliveira D. M., Pereira E., Pitanga B. P. S., Dos Santos Costa R., da Silva Velozo E., Freire S. M., Clarencio J., Borges H. L., Rehen S. K., Moura-Neto V., Costa S. L. - Specific Cytostatic and Cytotoxic Effect of Dihydrochelerythrine in Glioblastoma Cells: Role of NF-kappaB/beta-catenin and STAT3/IL-6 Pathways. Anticancer Agents Med. Chem., 18(10) (2018) 1386-1393. https://doi.org/10.2174/1871520618666180412122101.

122. Adebayo S. A., Dzoyem J. P., Shai L. J., Eloff J. N. - The anti-inflammatory and antioxidant activity of 25 plant species used traditionally to treat pain in southern African. BMC Complement. Altern. Med., 15 (2015) 159. https://doi.org/10.1186/s12906-015-0669-5.

123. Mofor C. T., Zofou D., Nangmo L., Boyom F. F., Fokou E., Titanji V. P. K., Amvam-Zollo P. H. - Phytochemical screening, antiplasmodial activity against multi-drug resistant parasites, cytotoxicity and antioxidant profiling of extracts from Fagara macrophylla and Eremomastax speciosa. Int. J. Indig. Herb. Drug, 2(2) (2017) 1-8.

124. de la Torre Rodriguez Y. C., Martinez Estrada F. R., Flores Suarez A. E., Waksman de Torres N., Salazar Aranda R. - Larvicidal and cytotoxic activities of extracts from 11 native plants from northeastern Mexico. J. Med. Entomol., 50(2) (2013) 310-313. https://doi.org/10.1603/me12056.

125. Ntchapda F., Maguirgue K., Kemeta A. D. R., Momeni J., Djedouboum A., Dimo T. - Acute Toxicity Studies of the Stem Bark Extract of Zanthoxylum heitzii A. & P. (Rutaceae) on Haematological Parameters, and Body Temperature. Int. J. Pharma Res. Health Sci., 3(2) (2015) 630-642.

126. Yang N., Zhang J., Guo J., Xiang Q., Huang Y., Wen J., Liu Q., Hu T., Chen Y., Rao C. - Revealing the mechanism of Zanthoxylum armatum DC. extract-induced liver injury in mice based on lipidomics. J. Ethnopharmacol., 319(Pt 1) (2024) 117086. https://doi.org/10.1016/j.jep.2023.117086.

127. Zhang J., Guo J., Yang N., Huang Y., Wen J., Xiang Q., Liu Q., Chen Y., Hu T., Rao C. - Zanthoxylum armatum DC fruit ethyl acetate extract site induced hepatotoxicity by activating endoplasmic reticulum stress and inhibiting autophagy in BRL-3A models. J. Ethnopharmacol., 319(Pt 2) (2024) 117245. https://doi.org/10.1016/j.jep.2023.117245.

128. Guo J., Wen J., Xiang Q., Huang Y., Hu T., Rao C. - Study on SH-SY5Y autophagy inhibition and apoptosis induced by methanol extract of Zanthoxylum armatum DC. based on mTOR signal pathway. Toxicol. Res. (Camb.), 13(1) (2024) tfae013. https://doi.org/10.1093/toxres/tfae013.

129. Guo J., Yang N., Zhang J., Huang Y., Xiang Q., Wen J., Chen Y., Hu T., Qiuyan L., Rao C. - Neurotoxicity study of ethyl acetate extract of Zanthoxylum armatum DC. on SH-SY5Y based on ROS mediated mitochondrial apoptosis pathway. J. Ethnopharmacol., 319(Pt 3) (2024) 117321. https://doi.org/10.1016/j.jep.2023.117321.

130. Xiang Q., Wen J., Zhou Z., Dai Q., Huang Y., Yang N., Guo J., Zhang J., Ren F., Zhou X., Rao C., Chen Y. - Effect of hydroxy-alpha-sanshool on lipid metabolism in liver and hepatocytes based on AMPK signaling pathway. Phytomedicine, 132 (2024) 155849. https://doi.org/10.1016/j.phymed.2024.155849.

131. Prakash B., Singh P., Mishra P. K., Dubey N. K. - Safety assessment of Zanthoxylum alatum Roxb. essential oil, its antifungal, antiaflatoxin, antioxidant activity and efficacy as antimicrobial in preservation of Piper nigrum L. fruits. Int. J. Food Microbiol., 153(1-2) (2012) 183-191. https://doi.org/10.1016/j.ijfoodmicro.2011.11.007.

132. Luo X., Pires D., Ainsa J. A., Gracia B., Duarte N., Mulhovo S., Anes E., Ferreira M. J. - Zanthoxylum capense constituents with antimycobacterial activity against Mycobacterium tuberculosis in vitro and ex vivo within human macrophages. J. Ethnopharmacol., 146(1) (2013) 417-422. https://doi.org/10.1016/j.jep.2013.01.013.

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25-04-2026

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Bach, P. C., Tuyen, T. T., Vien, T. A., Minh, P. T. H., Long, P. Q., & Van, N. T. H. (2026). Anticancer potential of the Zanthoxylum genus: A review of phytochemistry and bioactivity. Vietnam Journal of Science and Technology, 64(2), 213–240. https://doi.org/10.15625/2525-2518/22121

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