REVIEW ARTICLE

Meta-analysis of Ginkgo biloba Preparation for the Treatment

of Alzheimer's Disease
Ziwei Liao, MM, Liping Cheng, MM, Xiaoxue Li, MM, Miaomiao Zhang, MM,
Sha Wang, MM, and Ruimin Huo, MM

Several systematic reviews have been performed on the use of

Objective: The objective of this study was to investigate the efficacy Ginkgo biloba in treating cognitive impairment and dementia.3–7
and safety of Ginkgo biloba preparation for the treatment of Alzheimer However, most of them enrolled patients with mixed cognitive
disease (AD). impairment (including mild cognitive impairment and other
Methods: Both English (PubMed, Embase, Cochrane Library databases,
Downloaded from http://journals.lww.com/clinicalneuropharm by BhDMf5ePHKbH4TTImqenVICwrFV2Grwd+oUXZ6nGCYZXyGiR4fwN7kUhCQZBkKMHXyhtLRk1VVM= on 07/18/2020

memory loss) or dementia (including AD, vascular dementia, or

and the Cochrane Controlled Trials Register) and Chinese (WanFang, mixed dementia), or they compared Ginkgo biloba and other drugs.
Chinese Biomedical, CNKI, and VIP databases) databases were system- This meta-analysis assessed the efficacy and safety of Ginkgo
atically and independently searched by 2 authors from their inception until biloba by extracting data from selected randomized controlled trials
July 3, 2019. All relevant studies included AD patients who were treated (RCTs) published in both English and Chinese language journals.
with Ginkgo biloba. The efficacy and safety of the medicine were used
as the main measurement index.
Results: Seven studies (N = 939) were identified and analyzed. When METHODS
compared with placebo, Ginkgo biloba showed exact validity in cognitive
function and global clinical assessment (cognitive function section: risk Selection Criteria
ratio = 1.98, 95% confidence interval = 1.52–2.59, Z = 5.12, P < 0.001;
according to Clinical Global Impression Change: odds ratio = 3.119,
According to the PICOS acronym, the following selection
95% confidence interval = 2.206–4.410, Z = 6.44, P < 0.001). Adverse
criteria were used:
events were mild.
Conclusions: Ginkgo biloba preparation has reliable efficacy of cognitive (1) Participants (P): Participants diagnosed with any one of the
function and global clinical assessment and safety in the treatment of AD.
following criteria as AD were included, regardless of severity
and disease course: (a) the Diagnostic and Statistical Manual
Key Words: Alzheimer disease, Ginkgo biloba, meta-analysis, of Mental Disorder III or IVor (b) the National Institute of Neu-
randomized controlled trial rological and Communicative Disorder and Stroke-Alzheimer
(Clin Neuropharm 2020;43: 93–99) Disease and Related Disorder Association.
(2) Intervention (I) and Comparison (C): Ginkgo biloba ver-
sus placebo or other single drug + Ginkgo biloba versus other
A lzheimer disease (AD) is a neurodegenerative disease and the
most common cause of dementia. Its characteristic symptoms
include difficulties with memory, language, problem solving, and
single drugs.
(3) Outcomes (O): At least one of the following items is in-
other cognitive skills that affect a person's ability to perform cluded: (a) efficacy and (b) the adverse events of the drug.
everyday activities. It is related to age, family history, and apo- (4) Study design (S): Randomized placebo-controlled, trials.
lipoproteins E (APOE)-e4 gene.1 A total of 5.7 million Americans Languages include Chinese and English.
of all ages were estimated to be living with Alzheimer dementia in
2018. One in 10 people (10%) 65 years and older has Alzheimer Exclusion Criteria
dementia.2 Alzheimer disease not only seriously affects the qual- Repeated publication; lack of access to the full text; case re-
ity of life of patients but also brings a heavy burden to the family ports, reviews, and systematic evaluation; inability to extract data;
and society. animal experiments; and subjects with severe organ failure.
No current medications can cure AD or stop the progres-
sion of AD. Some symptomatic treatments, such as memantine, Search Methods
donepezil, galantamine, and rivastigmine, may be beneficial in
Major English (PubMed, Embase, Cochrane Library data-
lessening memory loss and confusion. In the 1960s, scientists
bases, and the Cochrane Controlled Trials Register) and Chinese
from Germany and France extracted ginkgo flavonoids and
databases (WanFang Database, Chinese Biomedical Database,
ginkgolide from the leaves of Ginkgo biloba (GB), which have pro-
Chinese Scientific Journals Database, and China Network Knowl-
tective effects against cardiovascular and cerebrovascular diseases
edge Infrastructure) were searched from their inception until July
and antiaging effects and might be effective in the treatment of AD.
3, 2019. At the same time, the relevant literature is searched man-
ually to supplement them.
Department of Second Neurology, Handan First Hospital, Handan, Hebei, China. The English search terms included “ginkgo biloba*,” “Ginkgo
Address correspondence and reprint requests to Liping Cheng, MM, biloba extract*,” “GBE 761,” “Alzheimer disease*,” “senile demen-
Department of Second Neurology, Handan First Hospital, No. 25, Congtai
Rd, Congtai District, Handan 056002, Hebei, China; E‐mail: clp@126.com
tia,” “randomized controlled trial,*” and “randomized.” The Chinese
Conflicts of Interest and Source of Funding: The authors have no conflicts of search terms included “a_er_ci_hai_mo_bing,” “lao_nian_chi_dai,”
interest to declare. “a_er_ci_ hai_mo_shi_bing,” and “lao_nian_xing_chi_dai,” Ginkgo
Supplemental digital contents are available for this article. Direct URL citations biloba (“yin_xing_ye_zhi_ji,” “yin_xing_ye”), and randomized
appear in the printed text and are provided in the HTML and PDF versions
of this article on the journal’s Web site (www.clinicalneuropharm.com).
(“sui_ji_dui_zhao,” “sui_ji”). The search details are listed in the
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved. supplement (available online as supplemental digital content at
DOI: 10.1097/WNF.0000000000000394 http://links.lww.com/CNP/A13).

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Liao et al Clinical Neuropharmacology • Volume 43, Number 4, July/August 2020

FIGURE 1. Preferred reporting items for systematic reviews and meta-analyses flow diagram. Adapted from Moher et al.10 For more
information, visit http://www.prisma-statement.org.

Assessment of Study Quality Tool was used to assess the risk of bias of included RCTs.9 We
assessed 6 biases accordingly, namely, selection bias (random se-
Two evaluators used the modified Jadad scale to evaluate the quence generation and allocation concealment), performance bias
quality of the literature (1–3 points for low quality and 4–7 points and detection bias (blinding), attrition bias (incomplete outcome
for high quality).8 Low-quality articles were screened out, and data), reporting bias (selective outcome reporting), and other bias.
high-quality articles were included. The Cochrane Risk of Bias We categorized each item into low, unclear, or high risk of bias.

TABLE 1. Characteristics of the RCTs

n Male, % Intervention
Control
Authors Studies Exp Con Exp Con Diagnostic Criteria Experimental Group Group Outcomes
11
Le Bars et al, 1997 DB 120 116 45.83 37.93 DSM-III EGb 120 mg Placebo Efficiency
Schneider et al,12 DB 40 40 57.5 55 DSM-IV NINCDS/ EGb 240 mg, 120 mg Placebo Safety analysis
2017 ADRDA
Maurer et al,13 1998 DB 9 9 44.44 55.56 DSM-III NINCDS/ EGb 240 mg Placebo Efficiency
ADRDA
Ihl et al,14 2012 DB 163 170 33.13 34.71 NINCDS/ADRDA EGb 240 mg Placebo Efficiency safety
analysis
Mazza et al,15 2006 DB 25 26 48 38.46 DSM-IV EGb 160 mg Placebo Efficiency safety
analysis
Yancheva et al,16 DB 31 32 45.16 15.63 NINCDS/ADRDA EGb 240 mg + Donepezil Efficiency safety
2009 donepezil analysis
Kanowski et al,17 DB 79 79 30.38 26.58 DSM-III EGb 240 mg Placebo Efficiency
2003
DB, double blind; Exp, experimental group; Con, control group; DSM-III/IV, Diagnostic Statistical Manual of Mental Disorders, Third/Fourth Edition;
HAM-D, Hamilton Rating Scale for Depression; NINCDS-ADRDA, Clinical Diagnosis of the National Institute of Neurological and Communicative Dis-
orders and Stroke and the Alzheimer's Disease and Related Disorders Association.

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Clinical Neuropharmacology • Volume 43, Number 4, July/August 2020 GB Preparation for the Treatment of AD

Data Synthesis and Statistical Analyses

According to the recommendations of the Cochrane Collab-
oration Review, Review Manager Version 5.3 (http://www.
cochrane.org) and STATA Version 14.0 (http://www.stata.com/)
were used to perform meta-analyses. For dichotomous data, risk
ratio (RR) ±95% confidence interval (CI) was calculated. For or-
dered data, odds ratio (OR) value of ±95% CI was calculated.
Study heterogeneity was measured using I2, with I2 values greater
than 50% indicating heterogeneity. Funnel diagrams and Egger
tests could not be used to test for publication bias because of the
small number of studies that were included.

RESULTS

Study Selection
As shown in Figure 1, a total of 756 related literatures were
searched, 19 articles were obtained after screening, and 12
low-quality documents (≤3 points, the main reasons for low
score include: random sequence generation not clear, allocation
concealment not described, or blind method not used. For details,
see the Supplementary Table, http://links.lww.com/CNP/A13)
were removed by using the modified Jadad score. Seven RCTs
articles were included in the meta-analysis.11–17

Study Characteristics
Seven studies were included, all in English. The selected
studies met the inclusion criteria and were double-blind RCTs.
A total of 939 patients were included in 7 articles, including 352
male patients and 687 female patients. In the 7 studies, the duration
of drug treatment ranged from 3 months to 26 weeks. All the drugs
used were standard Ginkgo biloba extract EGb 761. The dosage of
drugs included 120, 160, and 240 mg/d. One of the studies com-
pared the efficacy of Ginkgo biloba preparations alone, donepezil
alone, and the combination of the 2 drugs. We included data from
the combination group and donepezil alone for analysis. Other stud-
ies compared the efficacy of Ginkgo biloba preparation and pla- FIGURE 3. Risk of bias summary of RCTs on AD.
cebo. Details of the included literature are shown in Table 1.
Outcomes
Risk of Bias Assessment
Seven studies described in detail the method of random allo-
Efficacy
cation with the use of the computer generated random sample set, We evaluated the efficacy of the drug based on the cognitive
and all of them were double-blind experiments. Four experiments function, activities of daily living (ADLs), and global clinical as-
described the allocation hiding method. All studies reported the sessment mentioned in the article.
number of withdrawal patients and the reasons for withdrawal, in-
cluding adverse drug reactions, loss of follow-up, and the use of Cognitive Function and ADLs
drugs prohibited under the agreement. Overall, all the included Three studies used the Alzheimer Disease Assessment Scale-
studies were of high quality (Figs. 2, 3). cognitive section18 and one study used Syndrom Kurz Test (SKT)19

FIGURE 2. Risk of bias graph of RCTs on AD.

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Liao et al Clinical Neuropharmacology • Volume 43, Number 4, July/August 2020

FIGURE 4. Forest plot of outcome cognitive function and ADLs.

to assess cognitive function. The effectiveness was judged by the preparations. Common adverse reactions include dizziness, head-
change of scores before and after treatment (Alzheimer Disease As- ache, upper respiratory tract infections, and agitation, and most
sessment Scale-cognitive section or SKT score decreased by at least adverse events were considered of mild intensity. No serious ad-
4 points). Two studies were based on the Geriatric Evaluation by verse reactions related to Ginkgo biloba preparations were re-
Relative's Rating Instrument,20 the Gottfries–Bråne–Steen (GBS)21 ported in all trials.
Scale subscore of ADLs, and GBS Scale to determine the im- A meta-analysis of the number of patients with adverse reac-
provement of ADLs. tions showed that I2 = 0 < 50%, P = 0.776 > 0.1, RR = 0.916, 95%
Four studies (7 data sets) were included. The heterogeneity CI = 0.840–0.998, Z = 2.00, P = 0.046, which indicated that
test showed that I2 = 52.4 > 50%, and P = 0.050 < 0.1 of Q test, Ginkgo biloba preparation had better safety (Fig. 9).
suggesting that existed heterogeneity between the selected litera-
ture (Fig. 4). The L‘Abbé is inspected, as shown in Figure 5. Sen-
sitivity analysis was performed on data from 4 studies (Fig. 6). In DISCUSSION
view of the different types of scales, the scales were divided into 2
groups and meta-analysis was conducted on each one (group 1 Summary of Evidence
used cognitive function averaging and group 2 used daily living In this article, the efficacy of Ginkgo biloba preparation in
ability assessment). The results were as follows (Fig. 7): the treatment of AD was systematically and comprehensively re-
For group 1, I2 = 12.4 < 50%, P = 0.331 > 0.1, indicates no viewed and meta-analyzed. The results of 5 studies directly showed
heterogeneity (RR = 1.983, 95% CI = 1.521–2.585, Z = 5.05, that Ginkgo biloba preparations had a certain effect (during a period
P < 0.001). For group 2, I2 = 0 < 50%, P = 0.624 > 0.1, indicates
no heterogeneity (RR = 1.089, 95% CI = 0.828–1.432, Z = 0.61,
P = 0.542).
This finding indicates that Ginkgo biloba preparation had a
certain effect (during a period of 3 months to 26 weeks in the trials),
unlike placebo in cognitive function. However, the effect on daily
functioning is uncertain.
Global Clinical Assessment
Three studies used the Clinical Global Impression Change
(CGIC)22 score to determine global clinical assessment. The degree
of change was divided into improvement, no change, and deterio-
ration. The CGIC is not included in this analysis because a study
classifies CGIC as improved or unchanged and deteriorated, and no
specific improvement or unchanged population can be achieved.
The included data were meta-analyzed (Fig. 8). After heterogeneity
test, I2 = 31.1% < 50%, P = 0.234 > 0.1, in Q test (OR = 3.119, 95%
CI = 2.206–4.410, Z = 6.44, P < 0.001), indicates that the efficacy
of Ginkgo biloba preparation is better than that of placebo.

Adverse Events
One study reported that no adverse reactions were observed
during treatment. Four studies reported the types of adverse reac-
tions; 3 studies reported in detail the number of adverse reactions
and the number of events, and one study reported the types and
quantities of adverse reactions of different doses of Ginkgo biloba FIGURE 5. L'Abbé of outcome cognitive function and ADLs.

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Clinical Neuropharmacology • Volume 43, Number 4, July/August 2020 GB Preparation for the Treatment of AD

FIGURE 6. Sensitivity analysis of outcome cognitive function and ADLs.

of 3 months to 26 weeks in the trials) on AD and whether it had Previously, a systematic review evaluated the efficacy of
effects was independent of drug dosage. However, a study did Ginkgo biloba preparations in the treatment of AD considering 6
not find a clear difference between the Ginkgo biloba preparation studies. The results showed that 240 mg of Ginkgo biloba prepa-
group and the placebo group. This result may be related to the rations could improve patients' daily living ability and may be ben-
slow deterioration of the disease in the control group. After sub- eficial in slowing down the deterioration of cognitive function and
group analysis of AD patients with psychiatric symptoms, the ef- mental symptoms.5
ficacy of Ginkgo biloba preparation was concluded to be better In this review, the effects of Ginkgo biloba preparation on
than that of placebo, and the difference was statistically signifi- cognitive function and clinical changes of AD patients were ana-
cant. Another study compared the treatment differences between lyzed. Through an analysis of the included data, Ginkgo biloba
Ginkgo biloba preparation combined with the donepezil group preparation is concluded to have a certain efficacy in improving
and the donepezil-alone group and found no significant differ- the above symptoms, as well as good security. However, when
ence. However, the study compared the Ginkgo biloba preparation we analyzed the ability of daily life, no difference was found be-
group with the donepezil-alone group and found no significant tween Ginkgo biloba preparation and placebo, which may be re-
difference. Therefore, the authors believe that Ginkgo biloba prep- lated to the limited data we included.
aration has the same effect as donepezil in the treatment of AD, Some studies have shown that ginkgolides contained in Ginkgo
and it has a certain effect in the treatment of AD. biloba preparations have antioxidant and anti-apoptotic biological

FIGURE 7. Forest plot of outcome cognitive function and ADLs.

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Liao et al Clinical Neuropharmacology • Volume 43, Number 4, July/August 2020

FIGURE 8. Forest plot of outcome Global Clinical Assessment. ES, effect size.

activities as well as significant promoting and protecting effects bias test was conducted because of the small number of studies,
on the development of brain neurons.23–25 Ginkgo flavonoids which may have an impact on the reliability of data. Moreover, only
can improve the level of acetylcholine and monoamine transmit- 7 studies that meeting the standards are included. No long-term
ters in brain tissue, increase the activity of superoxide dismutase study is involved. Therefore, this meta-analysis only proves that
in brain tissue, scavenge free radicals, resist lipid peroxidation, re- the ginkgo leaf preparation can alleviate the AD symptoms in
duce apoptosis in brain tissue, and protect brain function.26 the short term. The results do not suggest that the preparation
can modify the disease. The modifying effect of the preparation
needs to be further discusses in the studies at larger scale and with
Limitations a longer duration.
Our systematic review has some limitations. (1) Some differ- Therefore, the overall conclusions tend to be weak. In the future,
ences exist in AD diagnostic criteria, dosage, course of treatment additional large samples and multicenter RCTs with high-quality
of Ginkgo biloba preparations, and selection of dementia scale, meta-analysis should be included.
which may lead to bias, thus affecting outcome indicators. (2)
Subgroup analysis of all studies was not conducted according to
dosage because of limited data. (3) No further analysis was per-
formed for all studies. The efficacy on other symptoms (such as CONCLUSIONS
psychiatric symptoms) of patients was analyzed. (4) There was a The evaluation of this system shows that Ginkgo biloba prep-
lack of discussion about the size effect of Ginkgo biloba formula- aration can improve the cognitive function and overall improve-
tions, because only studies with placebo were included, such as cho- ment of AD patients and that it has good safety, indicating that
linesterase inhibitors and memantine and other nonpharmacological Ginkgo biloba preparation is a safe and effective drug for AD.
interventions such as cognitive rehab and enhanced physical activity. However, because of the limited number of samples, the evidence
This deserves further discussion in future analysis. (5) No publication supporting this conclusion may not be strong.

FIGURE 9. Forest plot of outcome of “Adverse events.”

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