Potential of Indonesian Herbal as an Anti-Cancer Therapy: A Systemic Review of in vitro Studies

Figures & data

Table 1 Risk of Bias Assessment Results and Quality of Articles Reviewed Using OHAT Tools

		Risk of Bias Question								Overall Risk of Bias
		Randomization	Allocation Concealment	Blinded Study	Missing Outcome Data	Exposure Characterization	Outcome Assessment	Outcome Reported	Other Bias	Score	Tier	Conclusion
Review	Fatmawati, dkk.^Citation13	+2	+2	+2	+1	+2	+2	+2	+1	+1,75	1	Low Risk of Bias
	Fertilita, dkk.^Citation14	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Suhendar U.^Citation15	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Ibrahim A.A., dkk.^Citation16	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Widyanto R.M., dkk.^Citation17	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Abdullah M, dkk.^Citation18	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Bhanuwati AV and Pakpahan A.^Citation19	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Ramandhita AP, dkk.^Citation20	+2	+2	+2	+1	+2	+2	+2	+1	+1,75	1	Low Risk of Bias
	Tulloh NRA and Andriane Y.^Citation21	+2	+2	+2	+1	+2	+2	+2	+1	+1,75	1	Low Risk of Bias
	Astuti Y, et al^Citation22	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Fathani IJ and Miladiyah I.^Citation23	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Mutiah R.^Citation24	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Susilowati, dkk.^Citation25	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Novitasari D, dkk.^Citation26	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Anwar R, et al^Citation2	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Anwar R, et al^Citation6	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Anwar R, et al^Citation7	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Anwar R, et al^Citation27	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Lestari W, et al^Citation28	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Wihadmadyatami H, et al^Citation29	+2	+2	+2	+2	+2	+2	+2	+1	+1,875	1	Low Risk of Bias
	Lutfia A, et al^Citation30	−1	+2	+2	+2	+2	+2	+2	+1	+1,5	1	Low Risk of Bias
	Hasan AEZ, et al^Citation31	−1	+2	+2	+2	+2	+2	+2	+1	+1,5	1	Low Risk of Bias
	Nugraha AS, et al^Citation11	+2	+2	+2	+2	−1	+2	+2	+1	+1,5	1	Low Risk of Bias

Notes: ; ;

Figure 1 Flowchart of the Article Search Process based on the PRISMA-SR Guidelines.

Table 2 Characteristic and Comparison Result of Researched Article

No.	Author	Year	Quality of Journal	Herbal Plant	Origin of Herbal Plant	Model System	Type of Cancer	Method Assay	Mechanism of Action	Result	Conclusion
1.	Fatmawati, dkk.^Citation13	2018	National Accredited	Annona muricata (Soursop) Note: Ethanol extract	Semarang	MCF-7 cell	Breast cancer	MTT Assay	Soursop leaf extract causes some cancer cells to damage the defense mechanism against ROS so that they cannot use additional anti-oxidants for the repair process causing a buildup of free radicals in cancer cells which has the effect of triggering apoptosis in cancer cells	The IC50 value obtained in MCF-7 cells was 44.94 μg/mL	Soursop extract is selective cytotoxic against MCF-7 breast cancer cells
2.	Fertilita, dkk.^Citation14	2020	S2	Annona muricata (Soursop) Note: Ethanol extract	East Java	T47D cell	Breast cancer	MTT Assay	Decreases BCL2 protein regulation, increases Bax, inhibits mitochondrial I complexes, and inhibits NADH ubiquinone-oxidase on the plasma membrane of cancer cells causing apoptosis	The IC50 value of Annona muricata leaf ethanol extract against T47D cancer cells was 109.91±3.04 μg/mL	Soursop (Annona muricata) leaf ethanol extract has the potential to inhibit the proliferation of T47D cancer cells
3.	Suhendar U.^Citation15	2018	S3	Annona muricata (Soursop) Note: Ethanol extract	Sukasirna (Cianjur I), Sukasarana (Cianjur II), Ciherang (Cianjur III), Coral Pakpak (Sukabumi I), Coral Pakpak (Sukabumi II), and Sukasari (Sukabumi III)	MCF-7 cell	Breast cancer	MTT Assay	Inhibits the proliferation of cancer cells	Cianjur I’s IC50 value was 24.72; Cianjur 2 of 17.26; Sukabumi 1 of 22.39; Sukabumi 2 of 12.05; Sukabumi 3 by 19.49	All extracts exhibit cytotoxic activity against MCF-7 cancer cells. Cianjur III soursop leaf extract has the highest IC50 value, which is 9.12 μg/mL
4.	Ibrahim A.A., dkk^Citation16	2020	S3	Annona muricata (Soursop) Note: Ethanol extract	Kota Batu (East Java)	MCF-7 cell	Breast cancer	MTT Assay	Stop the cell cycle in phase G1 and decrease the number of cells in phase S by decreasing the expression of cyclin D1, an important regulatory protein in the cell cycle	IC50 value of soursop leaf ethanol extract (Annona muricata) against MCF-7 cancer cells is 117.87 μg/mL	Annona muricata leaf ethanol extract is effective in inhibiting the growth of MCF-7 breast cancer cells
5.	Widyanto R.M., dkk.^Citation17	2019	S2	Annona muricata (Soursop) Note: Soursop fruit extract	Materia Medika (East Java)	HeLa cell	Cervix cancer	MTT Assay	–	IC50 value of soursop juice in HeLa cells is 2522.33 μg/mL	Soursop juice has very low anti-oxidant activity and has no potential as an anti-cancer against HeLa cells in vitro.
6.	Abdullah M, dkk.^Citation18	2019	S2	Annona muricata (Soursop) Note: Ethanol extract	West Java	HT-29 cell	Colorectal cancer	MTT Assay	Inhibits the activity of cyclin protein D1	CC50 soursop leaf ethanol extract is 278 μg/mL	Soursop leaf ethanol extract may decrease the viability of HT-29 colon cancer cells
7.	Bhanuwati AV and Pakpahan A.^Citation19	2022	S1	Annona muricata (Soursop) Note: Ethanol extract; Fractions of ethanol, ethyl acetate, and n-hexane	Bandung (West Java)	HSC-3 cell	Oral Squamous Cell Carcinoma	CCK-8 assay	Reduces cancer cell growth by interfering with the G1/S and G2/M phases of the cell cycle	The IC50 value of A. muricata ethyl acetate fraction extract against HSC-3 cancer cell is 76.66 μg/mL; IC50 value of n-hexane fraction extract is 84.14 μg/mL; and IC50 value of ethanol fraction extract is 101,32 μg/mL	The ethanol, ethyl acetate, and hexane fractions of Annona muricata leaf extract have moderate cytotoxic activity
8.	Ramandhita AP, Yuniarti L, Hanum L^Citation20	2022	National Accredited	Annona muricata (Soursop) Note: Ethanol extract	Lembang (West Bandung)	HepG2 cell	Liver cancer	MTT Assay	Nanoparticles trigger easier cellular internalization through the pores of the endothelium to reach the cancer cells and more quickly or efficiently due to the charge on the surface of the nanoparticles which causes electrostatic bonds with cancer cells to be stronger	IC50 value of soursop leaf extract alginate nanoparticles against HepG2 liver cancer cell is 14.5 μg/mL	Alginate nanoparticles of soursop leaf extract have a high cytotoxic activity against HepG2 cancer cell
9.	Tulloh NRA and Andriane Y^Citation21	2022	National Accredited	Annona muricata (Soursop) Note: Ethanol extract	–	HTB183 cell	Lung cancer	MTT Assay	Nanoparticles trigger easier cellular internalization through the pores of the endothelium to reach the cancer cells and more quickly or efficiently due to the charge on the surface of the nanoparticles which causes electrostatic bonds with cancer cells to be stronger	IC50 value of soursop leaf extract alginate nanoparticles against HTB183 lung cancer cell is 31,261 278 μg/mL	Soursop leaf extract alginate nanoparticles have a moderate cytotoxic activity against HTB183 cancer cell
10.	Astuti Y, et al^Citation22	2022	S3	Annona muricata (Soursop) Note: Ethanol extract	Tawangmangu	Widr cell	Colorectal cancer	MTT Assay	Induces cell viability loss, morphological changes, membrane mitochondrial potential loss, and cell termination in the G0/G1 phase	The IC50 value of soursop leaf ethanol extract against Widr cells ranges from 0.03124–0.5 μg/mL at a dosage range of 33.125–450 ug/mL	Soursop leaf ethanol extract against Widr cancer cells has a high cytotoxic activity
11.	Hasan AEZ, et al^Citation31	2022	Q1	Annona muricata (Soursop) Note: Ethyl acetate extract endophytic mushroom of Soursop leaf	Sukabumi, Cianjur, Garut	HeLa cell	Cervix cancer	MTT Assay	Inhibits cell proliferation	All three endophytic mushroom extracts (Sir-CA1, Sir-G2, and Sir-SM2) showed IC values of <30 lg mL	All three endophytic mushroom extracts (Sir-CA1, Sir-G2, and Sir-SM2) have cytotoxic effects against HeLa cancer cell
12.	Nugraha AS, et al^Citation11	2019	Q3	Annona muricata (Soursop) Note: Methanol extract; alkaloid fraction; bioactive compound of coclaurine, reticuline, argentinine, atherosperminine, xylopine	Malang	HL-60, A549, HepG2 cell	Leukemia, lung, and liver cancer	MTT Assay	Inhibits cell proliferation	The IC50 value of xylopine bioactive compound of Annona muricata root extract against cancer cells HL-60, A549, and HepG2 is between 20–80 μg/mL	Xylopine bioactive compound of Annona muricata root extract has the highest cytotoxic effect among other compounds against HL-60, A549, and HepG2 cancer cell
13.	Fathani IJ and Miladiyah I^Citation23	2021	S2	Calophyllum spp. (Nyamplung) Note: Ethanol extract	–	Widr cell	Colorectal cancer	MTT Assay	Nyamplung fruit extract inhibits cancer cells through apoptosis and non apoptosis mechanisms (reducing NO production, cytoskeleton disintegration, and stimulation of cell death by autophagy).	The IC50 value of Nyamplung fruit shell ethanol extract in WiDr cell is 42.47 μg / mL, while the IC50 value of Nyamplung seed ethanol extract is 1030.41 μg / mL	Nyamplung seed ethanol extract is not cytotoxic to WiDr colorectal cancer cells, while Nyamplung fruit shell ethanol extract is moderately cytotoxic
14.	Mutiah R.^Citation24	2019	S5	Dendrophthoe pentandra (Benalu Cengkeh) Note: Ethanol extract	Kediri, Pekalongan, Sumatra and Kalimantan	T47D cell	Breast cancer	MTT Assay	Dendrophthoe pentandra ethanol extract inhibits proliferation of T47D cancer cell	Dendrophthoe pentandra ethanol extract from Kalimantan has IC50 value of 287.39 μg/mL, from Kediri of 304.79 μg/mL, from Pekalongan of 4646.34 μg/mL, and from Sumatra of 540.91 μg/mL	Extract from Kediri and Kalimantann have anti cancer effect against T47D cancer cell. Extract from Kalimantan has better cytotoxic effect than from Kediri against T47D cancer cell
15.	Susilowati, dkk.^Citation25	2022	S4	Dendrophthoe pentandra (Benalu Cengkeh) Note: Ethanol extract	Tawangmangu	HeLa cell	Cervix cancer	MTT Assay	Cytotoxic activity of ethanol extract parasite clove leaf against HeLa cell suspected to be able to go through cell cycle pathways as well as apoptosis	Ethanol extract of parasite clove leaf against HeLa cells showed an IC50 value of 43.90 μg/mL	Ethanol extract of parasite clove leaf with flavonoid compound has active moderate cytotoxic activity against HeLa cervical cancer cell
16.	Novitasari D, dkk^Citation26	2018	S2	Hedyotis corymbosa L. (Rumput Mutiara) Note: Ethanol extract	–	4T1 cell	Breast cancer	MTT Assay	Ethanol extract Hedyotis corymbosa L. inhibits cell proliferation and modulating signaling pathway such as FoxM1 expression, STAT3, Jun N-terminal kinase, dan NF-κB in anti-cancer activity; inhibits cancer invasion by inhibiting activity of MMP-9; and inhibits cancer cell migration	Ethanol extract Hedyotis corymbosa L. has IC50 value of 400 µg/mL	Ethanol extract Hedyotis corymbosa L. has anti-cancer effect against 4T1 cancer cell
17.	Anwar R, et al^Citation2	2018	S2	Altingia excelsa (Rasamala) Note: Methanol extract; ethyl acetate fraction; bioactive compound of Kaempferol and Quarcetin	Wayang Windu (Pengalengan, West Java)	SP-C1 cell	Tongue cancer	MTT Assay	Inhibits cell proliferation of SP-C1 cancer cell	Kamepferol compound IC50 value of Rasamala leaf extract is 2.50 μM; while quercetin IC50 value of Rasamala leaf extract is 2.31 μM	Quarcetin has higher cytotoxic effect than kaempferol of Rasamala leaf extract, however all of them have high cytotoxic activity
18.	Anwar R, et al^Citation6	2018	S3	Altingia excelsa (Rasamala) Note: Ethyl acetate extract; A-E fraction; bioactive compound of kaempferol and quarcetin	Wayang Windu (Pengalengan, West Java)	SP-C1 cell	Tongue cancer	MTT Assay	Inhibits cell proliferation of SP-C1 cancer cell by reducting proto onkogen c-myc expression	IC50 value of ethyl acetate extract against SP-C1 cell is 12.85 μg/mL, has a highest cytotoxic effect than others. IC50 value of quarcetin bioactive is 0.70 μg/mL, has a higher cytotoxic activity than kaempferol compound	Ethyl acetate extract, water extract, quarcetin and kaempferol compounds of Rasamala leaf (Altingia excelsa) has high cytotoxic activity against SP-C1 cancer cell
19.	Anwar R, et al^Citation7	2019	S4	Altingia excelsa (Rasamala) Note: Ethyl acetate extract; A-E fraction; bioactive compound of 3.4-dihidroksi benzoic acid, gallic acid, apigenin	Wayang Windu (Pengalengan, West Java)	SP-C1 cell	Tongue cancer	MTT Assay	Inhibits cell proliferation of SP-C1 cancer cell	The compound 3.4-dihydroxy benzoic acid, gallic acid, and apigenin from ethyl acetic extract of Altingia excelsa (Rasamala) against SP-C1 cancer cells had IC50 values of 75.41 μg/mL, 17.92 μg/mL, and 12.96 μg/mL	These three compounds are secondary metabolites of Rasamala leaves that can inhibit the proliferation of human tongue cancer cells in vitro.
20.	Anwar R, et al^Citation27	2021	S3	Altingia excelsa (Rasamala) Note: Methanol extract; ethyl acetate, n-hexane, and water fraction; bioactive compound of kaempferol and quarcetin	Wayang Windu (Pengalengan, West Java)	SP-C1 cell	Tongue cancer	MTT Assay	Kaempferol dan quercetin induces apoptosis can relate with MAPK cascade in inhibiting p90RSK activity, which p90RSK is inhibiting pro-apoptotic BAD. Increased apoptosis leads to increased activity of caspase-8 and −9.	The IC50 values of kaempferol and quarcetin from acetylacetate extract Rasamala leaf are 0.72 μg/mL and 0.70 μg/mL. The bioactive compounds of kaempferol and quercetin induce increased caspase-8 and −9 activity	The kaempferol and quarcetin compounds of acetylacetic extract Rasamala leaf can inhibit the proliferation of human SP-C1 tongue cancer cells in vitro
21.	Lestari W, et al^Citation28	2019	S1	Myrmecodia pendans (sarang semut) Note: Aqua extract	Bintuni (West Papua)	HSC-3 cell	Oral Squamous Cell Carcinoma	Flow cytometric analysis and qRT-PCR	Inhibits cell proliferation of SP-C1 cancer cell	The IC50 value of kaempferol from Rasamala leaf extract is 2.50 μM; while the IC50 quarcetin value of Rasamala leaf extract is 2.31 μM	Quarcetin has a higher cytotoxic effect than kaempferol in Rasamala leaf extract, but both have a high cytotoxic effect
22.	Wihadmadyatami H, et al^Citation29	2019	Q1	Ocimum sanctum Linn. (Basil) Note: Ethanol extract	Tawangmangu	Sel A549	Lung adenocarcinoma	MTT assay, Caspase-Glo 3/7 assay	Decrease cell viability and proliferation, increase intracellular ROS, affect SOD and GPx activity, so that increase apoptosis in A549 cell	Adhesion and viability examination showed that EEOS improved cell attachment and decreased cell viability at EEOS concentration of 100 ug/mL, EEOS induced apoptosis in A549 cells, EEOS showed a significant increase in ROS, EEOS showed an increase in expression levels of caspase-3, while this substance decreased the activity of the anti-apoptotic Bcl-2 protein	Ethanol extract Ocimum sanctum gives anti-cancer activity
23.	Lutfia A, et al^Citation30	2021	Q1	Zingiber griffithii (Tepus) Note: Ethyl acetate extract	Tahura Tongkoh Bukit Barisan (North Sumatra)	Viz. Panc-1, NBT-T2, HCT116 cell	Pancreas, gallbladder, and colon cancer	MTT Assay	Increased apoptosis	The IC50 values of compound 1 (Terpenoid-Alkaloids) against Panc-1, NBT-T2, and HCT116 cells are 0.05, 0.75, and 0.05 ppm; IC50 values for compound 2 (Sesterterpenoids) against Panc-1, NBT-T2, and HCT116 cells are 0.71, 0.30, and 0.67 ppm	Extract from the endophytic mushroom Hypomontagnella monticulosa Zg15SU and its host Zingiber griffithii Baker provides a high anticancer effect

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