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Forsythia suspensa (Thunb.) Vahl. (Family Oleaceae) is an ornamental shrub, the fruits of which are used as the well-known TCM “Forsythiae Fructus” (FF) (连翘in Chinese). The TCM characteristics of FF are summarized as bitter in flavor, with a mild cold nature and lung, heart or intestinum meridian distributions (Pharmacopoeia Commission of PRC, 2015), those characteristics are parallel to the characterisation of anti-inflammatory TCM, according to Chen and Zhang (2014). In Shennong’s herbal, FF was used for the treatment of pyrexia, inflammation, gonorrhea, carbuncle and erysipelas (Cho et al., 2011). Two forms of FF are available, the greenish fresh ripe fruit called “Qingqiao” and the yellow fully ripe one called “Laoqiao”. Both of them serve as official sources of FF, nevertheless, Qingqiao is used more frequently in TCM prescriptions (Jia et al., 2015). The major producing areas of FF are Hebei, Shaanxi, Shanxi, Shandong, Anhui, Henan, Hubei, Jiangsu (cultivated) and Sichuan Provinces (Editorial Board of Flora of China, 1978).

In the 2015 edition Chinese Pharmacopoeia, 114 Chinese medicinal preparations containing FF are listed, such as Shuanghuanglian oral solution, Yinqiao Jiedu tablet, Niuhuang Shangqing tablets, etc (Pharmacopoeia Commission of PRC, 2015). Modern researches reveal its anti-inflammatory (Kim et al., 2003), antioxidant (C.C. Chen et al., 1999), antibacterial (Han et al., 2012), anti-cancer (Hu et al., 2007), anti-virus (Ko et al., 2005), anti-allergy (Hao et al., 2010), neuroprotective (S. Zhang et al., 2015) effects, etc. Although only the fruit is used as TCM, some studies reported the phytochemistry and pharmacological effects of leaves (Ge et al., 2015, Zhang et al., 2015), flowers (Takizawa et al., 1981) and seeds (Zhang et al., 2002) of F. suspensa. Therefore, we now provide a systematic overview of the available information of F. suspensa, including traditional uses, botany, phytochemistry, pharmacology, toxicity, pharmacokinetics and quality control. Also, the possible future directions of research are discussed.

Section snippets

Traditional uses

In classical Chinese herbal texts, FF is recorded as useful in the treatment of rat fistula, scrofula, carbuncle, malignant ulcer, gall tumor, heat and poison (Shennong’s herbal, Bencao Chongyuan, Bencao Zhengyi, Zhenglei Bencao). According to many ancient classics, this medical herb is considerably effective on clearing the heat of heart channel and releasing the dampness-heat of spleen and stomach. It is also therapeutic for the treatment of stranguria, oedema, qi stagnancy and blood stasis

Botany

F. suspensa (Weeping Forsythia) is an ornamental deciduous shrub native to China, growing to a height of about 3 m (Fig. 1). It has hollow internodes with spreading or pendulous branchlets that are yellow-brown or gray-brown in colour. Leaves are usually simple, but sometimes 3-foliolate. Leaf blades are ovate, broadly ovate, or elliptic-ovate and 2–10 × 1.5–5 cm2 in size with a rounded to cuneate base and an acute apex. Both sides of the leaves are green, glabrous with sharply or coarsely

Phytochemistry

Nowadays, 237 compounds have been found in F. suspensa, including 46 lignans (1–46), 31 phenylethanoid glycosides (47–77), 11 flavonoids (78–88), 80 terpenoids (89–168), 20 cyclohexylethanol derivatives (169–188), six alkaloids (189–194), four steroidals (195–198) and 39 other compounds (199–237). Among them, two components (21–22) were isolated from the flowers of F. suspensa, 19 components (94–100, 107–111, 115–117, 198, 233–235) were isolated from the leaves of F. suspensa, four constituents

Anti-inflammatory effects

Anti-inflammatory activities of FF support its heat-clearing effects (Guo et al., 2015). Inflammation is a physical respond to infectious, allergic, or chemical stimulation (Lee et al., 2011). It engages in the development of chronic diseases, such as skin diseases, allergies, and cancer, etc. FF is one of TCM with potent anti-inflammatory capacities, it is widely applied to chronic and acute inflammation. The anti-inflammatory activities of FF ranked top five among 81 tested TCM (70% ethanol

Toxicity

Up to now, there is no report on the toxicity of FF. Daily administration dose of FF is suggested to be 6–15 g (Pharmacopoeia Commission of PRC, 2015). Relevant reports indicated no acute toxicity of water or ethanol extract of the leaves of F. suspensa in mice, even at daily dose of 61.60 g/kg (Ai et al., 2011, Hou et al., 2016, Li et al., 2013). Han et al. (2017) reported no acute toxicity of phillyrin (from the leaves of F. suspensa) in NIH mice (18.1 g/kg/day, p.o., for14 days) or no

Pharmacokinetics

Li et al. identified nine phase I metabolites of phillyrin in urinary samples of rats and presented its possible metabolic pathways in rats. Phillyrin was initially hydrolyzed into phillygenin and then converted to other metabolites dominantly through methylation, demethylation, dehydroxylation and ring-opening procedures (Li et al., 2014c). H. Wang et al. (2016) identified 34 phase I and phase II metabolites of phillyrin and indicated that hydrolysis, oxidation and sulfation were major

Quality control

To control the quality of FF, the Chinese Pharmacopoeia suggests morphological, microscopic and TLC identification in addition to HPLC determination. Qualified FF samples should contain more than 0.150% phillyrin (Pharmacopoeia Commission of PRC, 2015).

However, a single quantitative marker, phillyrin, seems insufficient to assess the quality of FF. Recently, various bioactive components in FF were examined by distinctive chromatography, electrophoresis, MS and NMR methods, such as

Conclusion and future perspectives

The present review summarizes comprehensive information about the traditional uses, botany, phytochemistry, pharmaceutical effects, toxicity, pharmacokinetics and quality control of F. suspensa. In classical Chinese herbal texts and the Chinese Pharmacopoeia, FF is dominantly used for heat-clearing and detoxifying. Till now, more than 230 compounds have been separated and identified from this herb. Among them, lignans and phenylethanoid glycosides are considered as characteristic and bioactive

TCM definitions

Yin: “Yin” is one of the two complementary opposite forces of nature, per the ancient Chinese construct of the universe. “Yin” is characterised as slow, soft, yielding, diffuse, cold, wet or tranquil, and it is associated with water, earth, the moon, femininity and nighttime.

Qi: In acupuncture terms, “qi” is the “life force”. It is the source of all movement within the body, the protection against invasion of the body, the source of all metabolic activity, provides for the holding of tissues

Acknowledgments

This work was supported by the Beijing Joint Project of Science Research with postgraduate education–Key technology research and application of safety evaluation of toxic Chinese medicinal materials based on the chemical composition and the characteristics of zebrafish.

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Ethnopharmacological relevance

Forsythiae Fructus (called Lianqiao in Chinese), the fruit of Forsythia suspensa (Thunb.) Vahl, is utilized as a common traditional medicine in China, Japan and Korea. It is traditionally used to treat pyrexia, inflammation, gonorrhea, carbuncle and erysipelas. Depending on the different harvest time, Forsythiae Fructus can be classified into two forms, namely Qingqiao and Laoqiao. The greenish fruits that start to ripen are collected as Qingqiao, while the yellow fruits that are fully ripe are collected as Laoqiao. Both are applied to medical use. This review aims to provide a systematic summary of F. suspensa (Forsythia suspensa (Thunb.) Vahl) and to reveal the correlation between the traditional uses and pharmacological activities so as to offer inspiration for future research.

Materials and methods

All corresponding information about F. suspensa was searched by Scifinder and obtained from scientific databases including Springer, Science Direct, Wiley, Pubmed and China Knowledge Resource Integrated (CNKI). Local dissertations and books were searched as well.

Results

According to classical Chinese herbal texts and Chinese Pharmacopoeia, Forsythiae Fructus dominantly displays heat-clearing and detoxifying effects in TCM prescriptions. In modern research, more than 230 compounds were separated and identified from F. suspensa. 211 Of them were isolated from fruits. Lignans and phenylethanoid glycosides are considered as the characteristic and active constituents of this herb, such as forsythiaside, phillyrin, rutin and phillygenin. They exhibited anti-inflammatory, antioxidant, antibacterial, anti-virus, anti-cancer and anti-allergy effects, etc. Currently, there is no report on the toxicity of Forsythiae Fructus, despite slight toxicity of forsythiaside reported in local publications. Compared to Laoqiao, Qingqiao contains higher levels of forsythiaside, forsythoside C, cornoside, rutin, phillyrin, gallic acid and chlorogenic acid and lower levels of rengyol, β-glucose and S-suspensaside methyl ether.

Conclusion

Heat-clearing actions of Forsythiae Fructus are based on the anti-inflammatory and antioxidant properties of lignans and phenylethanoid glycosides. Detoxifying effects attribute to the antibacterial, antiviral and anti-cancer activities of Forsythiae Fructus. And traditional Chinese medicine (TCM) characteristics of Forsythiae Fructus (bitter flavor, slightly cold nature and lung meridian) supported its strong anti-inflammatory effects. In addition, the remarkable anti-inflammatory and antioxidant capacities of Forsythiae Fructus contribute to its anti-cancer and neuroprotective activities. The higher proportion of lignans and phenylethanoid glycosides in Qingqiao than Laoqiao might explain the better antioxidant ability of Qingqiao and more frequent uses of Qingqiao in TCM prescriptions. For future research, more in vivo experiments and clinical studies are encouraged to further clarify the relation between traditional uses and modern applications. Regarding to Qingqiao and Laoqiao, they remain to be differentiated by all-round quality control methods, and the chemical compositions and clinical effects between them should be compared.