Anticancer effect of berberine based on experimental animal models of various cancers: a systematic review and meta-analysis

Xu, Jianhao; Long, Yuming; Ni, Liwei; Yuan, Xuya; Yu, Na; Wu, Runhong; Tao, Jialong; Zhang, Yusong

doi:10.1186/s12885-019-5791-1

Table 1 Characteristics of prospective studies on BBR

From: Anticancer effect of berberine based on experimental animal models of various cancers: a systematic review and meta-analysis

Author, year, country	Species, strain, gender, age	Model cell line	Experiment				Control	Outcome
Author, year, country	Species, strain, gender, age	Model cell line	Dosage	Frequency	Adnimistration	Duration	Control	type	mean0	Sd0	n0	mean1	Sd1	n1	p value
Breast cancer
Elisa Pierpaoli, 2015, Italy [10]	mice, FVB/N, F, 4w	SK-BR-3	2.5 mg/kg	biw	ip	32.5w	DMSO	VD	16.81	7.24	10	12.09	1.98	10	0.07
Yuwan Zhao, 2017, China [11]	mice, BALB/c, F, 6w	MDA-MB-231	100 mg/kg	tiw	po	3w	DMSO	TV	2.70	0.18	7	0.68	0.08	7	< 0.01
Yuwan Zhao, 2017, China [11]	mice, BALB/c, F, 6w	MDA-MB-231	100 mg/kg	tiw	po	3w	DMSO	BW	24.40	0.69	7	22.48	0.81	7	< 0.01
Alaa Refaat, 2013, Japan [12]	mice, BALB/c, F, 6w	4 T1	100 mg/kg	qd	po	4.3w	CMC	TW	0.21	0.01	6	0.15	0.01	6	< 0.01
Sangmin Kim, 2018, Korea [13]	mice, Balb/c, F, 6-8w	MDA-MB-231	0.1% BBR in the drinking water	Daily free intake	po	6.6w	–	TV	0.42	0.18	5	0.21	0.08	5	0.05
Kalyani Chowdary Karnam, 2017, India [14]	rats, SD, F, 6.4–8.3w	Induced by DMBA	50 mg/kg [pretreatment]	tiw	po	4w	Corn oil	TV	3.79	0.90	6	0.63	0.30	6	< 0.01
			50 mg/kg [pretreatment]					TW	9.64	0.90	6	3.80	0.99	6	< 0.01
			50 mg/kg [posttreatment]					TV	3.79	0.90	6	1.31	0.60	6	< 0.01
			50 mg/kg [posttreatment]					TW	9.64	0.90	6	5.71	1.32	6	< 0.01
Elisa Damiani, 2015, Italy [15]	miceFVB/NF4w	HER2/neu transgenic mice	2.5 mg/kg	biw	ip	NR	Sterile saline	VD	16.77	5.31	7	11.07	1.75	9	0.03
Ke Su, 2016, China [16]	mice, Balb/c, F, 6w	MDA-MB-231	10 mg/kg	q4d	ip	3w	DMSO	TV	0.59	0.27	6	0.27	0.12	6	0.02
								TW	0.50	0.11	6	0.29	0.06	6	< 0.01
								BW	22.59	7.31	6	19.10	3.71	6	0.32
Liver cancer
Guan-Yu Wang, 2009, China [17]	mice, Balb/c, M, 6w	HEPG2	40 mg/kg	qd	ip	1.4w	Saline	TV	3.31	0.38	5	2.21	0.22	6	< 0.01
			40 mg/kg					BW	3.13	0.43	5	4.62	0.41	6	< 0.01
			80 mg/kg					TV	3.31	0.38	5	1.43	0.13	5	< 0.01
			80 mg/kg					BW	3.13	0.43	5	3.74	0.36	5	0.04
Jing Li, 2015, Canada [18]	mice, Balb/c, NR, 6-8w	H22	50 mg/kg	qd	po	2w	Water	TV	4.24	0.56	10	0.33	0.35	10	< 0.01
Chi Man Tsang, 2015, China [19]	mice, NR, NR, NR	MHCC-97 L-luciferase	10 mg/kg	qod	ip	5w	Saline	TV	1.00	0.05	7	0.21	0.03	7	< 0.01
Chi Man Tsang, 2015, China [19]	mice, NR, NR, NR	MHCC-97 L-luciferase	10 mg/kg	qod	ip	5w	Saline	VD	12.58	2.94	7	2.18	1.29	7	< 0.01
Colon cancer
Norio Iizuka, 2002, Japan [20]	mice, Balb/c, M, 6w	Colon26/clone 20	0.1% BBR in the driNRing water	Daily free intake	po	2w	–	TW	0.22	0.15	9	0.25	0.12	9	0.65
			0.1% BBR in the driNRing water					BW	18.20	1.50	9	18.40	1.80	9	0.80
			0.2% BBR in the driNRing water					TW	0.22	0.15	9	0.25	0.15	9	0.68
			0.2% BBR in the driNRing water					BW	18.20	1.50	9	22.20	1.50	9	< 0.01
			0.4% BBR in the driNRing water					TW	0.22	0.15	9	0.24	0.18	9	0.80
			0.4% BBR in the driNRing water					BW	18.20	1.50	9	20.90	4.20	9	0.10
H Ruan, 2017, China [21]	mice, Balb/c, NR, 6-7w	KM12C/shCtrl	10 mg/kg	qd	ip	2w	DMSO	TV	1.26	0.97	6	0.79	0.53	6	0.32
H Ruan, 2017, China [21]	mice, Balb/c, NR, 6-7w	KM12C/shRXRα	10 mg/kg	qd	ip	2w	DMSO	TV	1.54	0.92	6	1.40	0.46	6	0.76
Yuchen Cai, 2013, Japan [22]	mice, Balb/c, NR, 5w	HT-29	10 mg/kg	qd	po	2w	Sterile water	TV	6.11	3.01	10	4.33	2.42	10	0.16
			10 mg/kg					BW	6.60	3.60	10	4.90	3.20	10	0.28
			30 mg/kg					TV	6.11	3.01	10	4.09	1.76	10	0.08
			30 mg/kg					BW	6.60	3.60	10	3.90	2.70	10	0.07
			50 mg/kg					TV	6.11	3.01	10	3.34	1.31	11	0.01
			50 mg/kg					BW	6.60	3.60	10	3.60	2.50	11	0.04
nasopharyngeal carcinoma
Chao Wang, 2017, China [23]	mice, NOD/SCID, F, 8w	HONE-1	10 mg/kg	tiw	ip	3w	DMSO	TV	0.58	0.06	5	0.10	0.03	5	< 0.01
Chao Wang, 2017, China [23]	mice, NOD/SCID, F, 8w	HONE-1	10 mg/kg	tiw	ip	3w	DMSO	TW	0.15	0.01	5	0.02	0.01	5	< 0.01
Chi Man Tsang, 2013, China [24]	mice, NR, M, 6-8w	C666–1	5 mg/kg	qod	ip	6w	DMSO	TV	0.15	0.05	5	0.04	0.03	5	< 0.01
Chi Man Tsang, 2013, China [24]	mice, NR, M, 6-8w	C666–1	10 mg/kg	qod	ip	6w	DMSO	TV	0.15	0.05	5	0.02	0.02	4	< 0.01
Lung cancer
Michael A. James, 2011, Missouri [25]	mice, Balb/c, M, 4-6w	A549	1800 ppm	Daily free intake	po	4w	DMSO	TV	0.06	0.02	3	0.02	0.02	4	0.05
Michael A. James, 2011, Missouri [25]	mice, Balb/c, M, 4-6w	A549	5400 ppm	Daily free intake	po	4w	DMSO	TV	0.06	0.02	3	0.01	0.01	2	0.04
Santosh K. Katiyar, 2009, Alabama [26]	mice, Balb/c, F, 6-7w	A549	50 mg/kg	qd	po	7w	PBS	TV	1.40	0.07	10	0.99	0.04	10	< 0.01
			50 mg/kg					TW	2.32	0.27	10	2.02	0.30	10	0.03
			100 mg/kg					TV	1.40	0.07	10	0.60	0.03	10	< 0.01
			100 mg/kg					TW	2.32	0.27	10	1.16	0.21	10	< 0.01
			200 mg/kg					TV	1.40	0.07	10	0.30	0.06	10	< 0.01
			200 mg/kg					TW	2.32	0.27	10	0.62	0.09	10	< 0.01
		H1299	50 mg/kg					TV	1.59	0.10	10	1.36	0.05	10	< 0.01
			50 mg/kg					TW	2.71	0.31	10	2.36	0.29	10	0.02
			100 mg/kg					TV	1.59	0.10	10	1.05	0.05	10	< 0.01
			100 mg/kg					TW	2.71	0.31	10	1.82	0.29	10	< 0.01
			200 mg/kg					TV	1.59	0.10	10	0.61	0.02	10	< 0.01
			200 mg/kg					TW	2.71	0.31	10	1.15	0.10	10	< 0.01
Gastric cancer
Junxiong Wang, 2016, China [27]	mice, Balb/c, F, 5w	BGC823	50 mg/kg	qd	po	4w	NR	TV	2.28	0.24	3	0.73	0.13	3	< 0.01
								TW	1.37	0.37	3	0.32	0.08	3	< 0.01
								BW	2.51	0.69	3	0.10	0.46	3	< 0.01
Hongli Li, 2016, China [28]	mice, Balb/c, M, 4w	MGC803	15 mg/kg	qd	po	3.3w	NR	TV	0.85	0.29	6	0.44	0.09	6	0.02
Hongli Li, 2016, China [28]	mice, Balb/c, M, 4w	MGC803	15 mg/kg	qd	po	3.3w	NR	TW	0.68	0.18	6	0.42	0.07	6	< 0.01
Neuroepithelial tumor
Juan Wang, 2015, China [29]	miceBalb/cNN	–	100 mg/kg	qd	po	3w	NR	TV	0.04	0.02	8	0.02	0.00	8	0.05
Yuxue Sun, 2018, China [30]	miceBalb/cN6-8w	C6	10 mg/kg	qd	ip	1w	DMSO	TV	0.77	0.22	7	0.35	0.06	7	< 0.01
Endometrial carcinoma
Yu Wang, 2018, China [31]	mice, Balb/c, NR, 6w	HEC-1-A	50 mg/kg	qd	po	4w	DMSO	TV	1.01	0.13	6	0.65	0.06	6	< 0.01
Yu Wang, 2018, China [31]	mice, Balb/c, NR, 6w	HEC-1-A	100 mg/kg	qd	po	4w	DMSO	TV	1.01	0.13	6	0.34	0.04	6	< 0.01
Esophageal cancer
Kewei Ren, 2016, China [32]	mice, Balb/c, M, 6-8w	Eca9706	20 mg/kg	qd	po	7w	DMSO	TV	6.37	0.25	5	5.05	0.60	5	< 0.01
Kewei Ren, 2016, China [32]	mice, Balb/c, M, 6-8w	Eca9706	20 mg/kg	qd	po	7w	DMSO	TW	2.66	0.29	5	1.82	0.21	5	< 0.01
Tongue squamous cell carcinima
Yung-Tsuan Ho, 2009, China [33]	mice, Balb/c, F, 6w	SCC-4	10 mg/kg	q4d	ip	4w	DMSO	TV	0.18	0.06	6	0.03	0.02	6	< 0.01
Yung-Tsuan Ho, 2009, China [33]	mice, Balb/c, F, 6w	SCC-4	10 mg/kg	q4d	ip	4w	DMSO	TW	0.26	0.16	6	0.12	0.09	6	0.11
Cholangiocarcinoma
Nattapong Puthdee, 2013, Japan [34]	hamster, Syrian, M, 4-5w	Ham-1	10 mg/kg	qd	po	3w	sterile water	TW	0.70	0.18	5	0.67	0.11	5	0.79
Sarcoma
Lei Zhang, 2012, China [35]	mice, Kunming, NR, 6w	S180	30 mg/kg	qd	ip	NR	NR	TW	2.20	0.93	10	1.26	0.54	9	0.02
Lei Zhang, 2012, China [35]	mice, Kunming, NR, 6w	S180	30 mg/kg	qd	ip	NR	NR	BW	2.71	2.20	10	−2.54	3.24	9	< 0.01

Mean0: mean value in control group (cm³ for tumor volume, g for tumor weight and body weight, mm/mm² for vessel density); Sd0: standard difference in control group; N0: sample size in control group; Mean1: mean in berberine group; Sd1: standard difference in berberine group; N1: sample size in berberine group; M: male; F: femle; NR: non reported; TV: tumor volume; TW: tumor weight; VD: vessel density; BW: body weight

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