Review of the Chemical Composition, Pharmacological Effects, Pharmacokinetics, and Quality Control of Boswellia carterii
Objective. This review aimed to systematically summarize studies that investigated the bioactivities of compounds and extracts from Boswellia. Methods. A literature review on the pharmacological properties and phytochemicals of B. carterii was performed. The information was retrieved from secondary databases such as PubMed, Chemical Abstracts Services (SciFinder), Google Scholar, and ScienceDirect. Results. The various Boswellia extracts and compounds demonstrated pharmacological properties, such as anti-inflammatory, antitumour, and antioxidant activities. B. carterii exhibited a positive effect on the treatment and prevention of many ageing diseases, such as diabetes, cancer, cardiovascular disease, and neurodegenerative diseases. Conclusion. Here, we highlight the pharmacological properties and phytochemicals of B. carterii and propose further evidence-based research on plant-derived remedies and compounds.
Frankincense resin comes from the tree of the genus Boswellia (family Burseraceae). Boswellia resins are recorded in texts with their traditional medical practices in an ancient civilization such as ancient China, Persia, and India. It was subsequently included in Chinese Pharmacopoeia Volume I. B. carterii was firstly used as a traditional Chinese medicine for treating urticaria. Modern pharmacological studies confirmed that B. carterii could be not only anti-inflammation, antioxidation, antiviral, antimalarial, and antitumour, but also protect liver and nerve. 3-O-Acetyl-11-keto-β-boswellic acid, 3α-acetoxy-8,24-dienetirucallic acid, and 3α-acetoxy-7,24-dienetirucallic acid are related to its anti-inflammatory effect. Incensole acetate plays an important role in its neuroprotective effect.
According to previous comments and reports [1–4], volatile oils and terpenes are the main components of B. carterii. However, although many chemical components have been isolated and identified from B. carterii, the toxicology and pharmacokinetic studies of Boswellia long-term use are lacking. Some review articles on B. carterii have been published, mainly concerning its chemical composition and pharmacological activity [1, 5–9]. In this review, we strictly analyze the current state of knowledge of phytochemistry, quality control, pharmacological effects, and pharmacokinetics. It is hoped that this review will fill the knowledge gap, complement the published review on its chemical composition and pharmacological activity, and provide support and perspectives on future research and clinical application of B. carterii.
A literature search was performed to collect relevant information of the traditional uses, as well as pharmacological properties and phytochemicals of B. carterii. Electronic databases were searched, including Google Scholar, SciFinder, PubMed, and ScienceDirect, and several literature articles published before August 2019 were reviewed. Additional primary data such as books were examined, including “The Compendium of Materia Medica” and “Chinese Pharmacopoeia.” Searching for relevant information on B. carterii was performed using multiple keywords, such as “B. carterii”; “Traditional uses”; “Phytochemistry”; “Pharmacological activities”; “Anti-tumour”; “Anti-inflammatory”; “Wound-healing properties”; and “Hepatoprotective.” All chemical structures were drawn using ChemBioDraw Ultra 14.0 software.
The chemical structure of B. carterii is primarily composed of terpenoids. A total of 304 compounds were identified, including 148 triterpenes, 94 diterpenes, and 62 compounds classified as volatile oils. All identified compounds are listed and numbered in Table 1.
2.1.1. Volatile Oil
Volatile oil, also known as an essential oil, is a general term for a class of oily compounds with aromatic odors. It can volatilize at average temperature and can be distilled with water vapor. Volatile oil from B. carterii primarily contains monoterpenes, sesquiterpenes, and ester compounds. It is worth mentioning that the classification here does not contain volatile diterpenoids and triterpenes, and we have described them in the corresponding classification (Scheme 1).
Diterpenoid refers to a group of compounds whose molecular skeleton contains four isoprene units and 20 carbon atoms.
It contains monocyclic diterpenoids, dicyclic diterpenoids, tricyclic diterpenoids, and tetracyclic diterpenoids. Fifty-one kinds of monocyclic diterpenoids, eighteen kinds of dicyclic diterpenoids, twenty-two kinds of tricyclic diterpenoids, and three kinds of tetracyclic diterpenoids were extracted from B. carterii.
(1) Monocyclic Diterpenoid. Monocyclic diterpenoid is a group of diterpenoids with one closed-loop carbon atom (Scheme 2).
(2) Dicyclic Diterpenoid. Dicyclic diterpenoid is a group of diterpenoids with two closed-loop carbon atoms (Scheme 3).
(3) Tricyclic Diterpenoid. Tricyclic diterpenoid is a group of diterpenoids with three closed-loop carbon atoms (Scheme 4).
(4) Tetracyclic Diterpenoid. Tetracyclic diterpenoid is a group of diterpenoids with four closed-loop carbon atoms (Scheme 5).
The triterpenoid is a terpenoid composed of 30 carbon atoms. According to the “Isoprene Rule,” most triterpenes consist of the condensation of 6 isoprene units (30 carbons). It can be divided into tetracyclic triterpenoids and pentacyclic triterpenoids. Fifty-seven tetracyclic triterpenes and ninety-one pentacyclic triterpenes were identified from B. carterii.
(1) Tetracyclic Triterpenoid. Tetracyclic triterpenoid is a group of triterpenoids with four closed-loop carbon atoms (Scheme 6).
(2) Pentacyclic Triterpene. A pentacyclic triterpenoid is a group of triterpenoids with five closed-loop carbon atoms (Scheme 7).
3. Quality Control
It is vital that quality control is for the safety and effectiveness of traditional Chinese medicine (TCM). Many rapid, sensitive, and stable technologies have been applied for quality analysis of B. carterii. A thin-layer chromatography method is developed to differentiate and identify three crucial Boswellia species . A total of twenty compounds, which contained two tricyclic diterpenes, twelve triterpenes, and six volatile oil, were detected by GC, GC/MS, SPME, TRSDMC , TLC, and HPLC. We summarized the information in Table 2.
B. carterii has acted as an ethnodrug for a long history because of its pharmacological effects. Boswellia contains biologically active compounds that exhibit pharmacological activities (Table 3).
4.1. Anti-Inflammatory Effects
It was recorded that B. carterii resin has been applied to treat various inflammatory diseases such as rheumatoid arthritis. Boswellic acids, the most well-known active components of B. carterii resin, were identified to have anti-inflammatory properties. Boswellic acids, in particular 3-O-acetyl-11-keto-β-boswellic acid, interfered with COX-1 and could regulate the anti-inflammatory effect in the way of inhibiting the expression of 5-lipoxygenases (5-LO) and 12-lipoxygenases (12-LO) and the suppression of cyclooxygenases, especially COX-1 . 3-O-Acetyl-11-keto-β-boswellic acid reduced Th17 differentiation by interrupting IL-1ß-mediated IRAK1 signal, which may regulate IL-1ß signal by inhibiting the phosphorylation of IL-1 receptor-related kinase 1 and STAT3 .
Microsomal prostaglandin E2 synthase-1 (mPGES-1) was confirmed to be a boswellic acid-interacting protein, and boswellic acid inhibited mPGES-1-mediated prostaglandin (PG) H2 conversion to PGE2 . Besides boswellic acids, other known triterpene acids, particularly 3α-acetoxy-8,24-dienetirucallic acid, and 3α-acetoxy-7,24-dienetirucallic acid, isolated from B. carterii suppressed mPGES-1 . The pull-down experiments and selective inhibition of the expression of iNOS induced by LPS suggested that ß-boswellic acid could be anti-inflammation through inhibiting LPS activity . Incensole acetate inhibited cytokine secretion and LPS-induced NF-κB activation through suppressing IκB kinase (IKK) phosphorylation . Incensole acetate reduced the activation of glial cells, the expression of TGF-β, IL-1β, and TNF-α mRNA, and the activation of NF-κB. Incensole acetate induced macrophages dead in closed head injury mice . The above studies indicate that incensole acetate could inhibit inflammation and protect neurons and may show potential effects against ischemia and reperfusion. Furthermore, 3α-acetoxy-28-hydroxy-lup-20(29)-en-4β-oic acid inhibited the biosynthesis of COX-, 5-LO-, and 12-LO-derived eicosanoids, acting as an efficient inhibitor of cPLA2α, and consequently suppressed eicosanoid biosynthesis in intact cells .
4.2. Antioxidant Effects
Research on the antioxidative effects of B. carterii has focused on the compounds 3-O-acetyl-9, 11-dehydro-β-mastic acid  and alcohol extracts . The antioxidative effects were observed by inhibiting 5-lipoxygenase , scavenging oxygen free radicals , and inhibiting a significant increase in the lipid peroxidation marker malondialdehyde (MDA) . Besides, the extracts from B. carterii showed antioxidant effects using the DPPH- and ABTS-free radical scavenging methods . Interestingly, the methanol fraction of the mastic-containing complex showed anti-inflammatory and antioxidant effects and promoted angiogenesis and epithelial regeneration in mice that had epithelial damage . Oxidative damage is one of the causes of human ageing, and the antioxidant effect of frankincense helps to slow down this process.
4.3. Antitumour Effects
B. carterii compounds and extracts showed adverse effects on glioblastoma, prostate cancer, fibrosarcoma, neuroblastoma, bladder cancer, leukemia, colon cancer, breast cancer, and liver cancer, which are partly related to the ageing [31, 57, 59, 60]. The cellular pathways modulated by B. carterii to exert anticancer effects are involved in the following aspects. B. carterii regulated the p21/FOXM1/cyclin B1 pathway, downregulated Aurora B, and upregulated the p53 signalling pathway . Acetyl-lupeolic acid primarily inhibited Akt by directly binding the pleckstrin homology domain. Acetyl-lupeolic acid could lead to three results, namely, the loss of mitochondrial membrane potential, the hindrance of phosphorylation of following targets of the Akt pathway, and the inhibition of the mTOR target p70 ribosomal hexaprotein kinase and β-catenin, p65/NF-κB, and c-Myc . B. carterii was also shown to significantly inhibit c-Myc expression  and block Sp1 DNA-binding activity to inhibit Sp1-stimulated androgen receptor promoter activity . At both Ser473 and Thr308 positions, 3-acetyl-11-keto-β-boswellic acid induced Akt phosphorylation . Tirucallic acids functioned in combination with the pleckstrin homeodomain of Akt to inhibit Akt activation and downregulate the pathway that activates Akt . B. carterii diterpenoids selectively docked with HIV-1 reverse transcriptase . B. carterii triterpenoids target cancer-related proteins, including poly (ADP-ribose) polymerase-1, tankyrase, and the folate receptor . ß-Boswellic acid could target cancer-associated proteins, such as proteasomes, 14-3-3 proteins, heat shock proteins, and ribosomal proteins . B. carterii essential oil activated heat shock proteins and histone core proteins .
Clinically, the combination of B. carterii, betaine, and inositol could reduce breast density, relieve pain in benign breast masses, reduce anxiety, and reduce masses in menopausal women [83–85]. Besides, B. carterii prolonged the survival of patients with lung cancer , reduced fatigue, enhanced vitality, and reduced insulin use in patients with pancreatic cancer . B. carterii also exhibited a beneficial effect for patients with bilateral lung and metastatic bladder cancers .
4.4. Antiviral Effects
The n-hexane-soluble mixture, MeOH extract, EtOAc-soluble mixture, n-BuOH-soluble mixture, water extract, and H2O-soluble mixture of B. carterii showed an antiviral effect by inhibiting the hepatitis C virus protease  and the Epstein–Barr virus early antigen .
4.5. Antimicrobial Effects
4.6. Neuroprotective Effects
A neuroprotective effect has been associated with B. carterii extracts that demonstrated antidepressant properties, resistance to inflammation caused by cerebral ischemia, promotion of neurodevelopment, and resistance to Alzheimer’s disease . Research in this area has focused on incensole acetate and gum resin from Boswellia. The TPRV3 pathway was associated with the antidepressant effect of B. carterii [52, 70]. The ability of B. carterii to promote nerve development may be related to its ability to increase CaMKII mRNA expression . Incensole acetate reduced NF-κB activity, and GFAP expression in the brain  showed an antidepressant effect in acute and chronic treatment cases  and reduced the inflammatory response of nerve tissues via the NF-κB pathway . Also, triterpene acids showed cytotoxicity in neuroblastoma .
4.7. Hepatoprotective Effects
4.8. Kidney Protective Effects
Prophylactic treatments using B. carterii showed benefits in anti-acute and anti-chronic renal failure cases. Oral administration of B. carterii induced a reduction in serum creatinine, serum urea, blood urea nitrogen, and C-reactive protein activity .
4.9. Immunomodulatory Effects
The compounds and fractions of B. carterii promoted the transformation of peripheral blood lymphocytes, regulated the expression of lymphokines in mouse spleen cells, dose-dependently inhibited the expression of Th1 cytokines, and dose-dependently promoted the expression of Th2 cytokines . Furthermore, acetyl-11-keto-β-boswellic acid, by preventing IL-1R-related kinase 1 phosphorylation and subsequently inhibiting STAT3 phosphorylation, affected the IL-1β signalling, thereby inhibiting Th17 cell differentiation . Moreover, it is interesting that the purified compounds showed carrier-dependent immunomodulation in vitro and that the purified compounds are less active than the total compounds .
4.10. Other Effects
B. carterii compounds showed an effect on the lung cell structure of rats , affected the development of Callosobruchus species by increasing oxidative stress , and reduced the level of oxidation to promote cardiovascular protection .
4.11. Side Effects
The side effects refer to the pharmacological effects of a drug beyond its therapeutic purpose following the application of a therapeutic amount of the drug. Understanding drug side effects is required to formulate a clinical medication plan and to avoid health risks. The side effects of B. carterii are primarily related to smoke-induced reproductive toxicity. Histopathological sections and ultrastructure of the testis and epididymis showed adverse effects on sperm development. Sperm counts, viability, and speed decreased in varying degrees, and the proportion of abnormal sperm increased. Fructose levels in epididymal fluid and prostate fluid were reduced, and also, a luteinizing hormone, testosterone, and follicle-stimulating hormone levels in plasma and protein were reduced [75, 92]. Other studies have shown that sialic acid and carnitine in cauda epididymal plasma are reduced .
Pharmacokinetics offers scientific support for the clinical use of B. carterii. The experiments have shown that 3-acetyl-11-keto-β-boswellic acid and 11-keto-β-boswellic acid are absorbed more by laboratory animals when administered in processed frankincense forms. Using HPLC, the Cmax of 3-acetyl-11-keto-β-boswellic acid and 11-keto-β-boswellic acid was 3.197 μg/mL and 2.037 μg/mL for vinegar-processed frankincense (VPF), respectively, and 0.987 μg/mL and 1.937 μg/mL for frankincense oral administration (FRA), respectively . The processed and nonprocessed products exhibited a significant difference in absorption. Meanwhile, 3-acetyl-11-keto-β-boswellic acid was absorbed more easily than 11-keto-β-boswellic acid, and the values of Cmax were observed in the order of VPF > SFF (stir-fried frankincense) > FRA. The levels of plasma 11-keto-β-boswellic acid and 3-acetyl-11-keto-β-boswellic acid reduced slowly, especially for the VPF group compared with the FRA group. In the VPF group, pharmacokinetic parameters of 11-keto-β-boswellic acid and 3-acetyl-11-keto-β-boswellic acid, such as Cmax, AUC0-t, and AUC0–∞, were greatly increased, while V/F and CL/F values were decreased . These results show that the clinical use value of frankincense can be further enhanced .
The resins of B. carterii have been used for the treatment of inflammation-related diseases, such as traumatic injury and inflammatory pain in China for a long time. Recently, the traditional medicine had become a hot research topic, while more positive effects and other potential medical values have been found. In this study, we listed the isolated components of Boswellia resin by category according to previous research and summarized their pharmacological effect on a different model. The different components of Boswellia resin have found a series of beneficial effects on many diseases when applied in laboratory research, and some have been approved for clinical use. We hope more research about quality control, and the novel component can be conducted in the future.
This article reviewed the research performed on the components of B. carterii in terms of quality control, phytochemistry, pharmacological effects (including side effects), and pharmacokinetics. We highlighted studies showing that frankincense exhibits anti-inflammatory, antitumour, and antioxidant activities, including some important organ-protective effects on the heart, liver, and kidney. We also found that B. carterii exhibits a good effect on the treatment and prevention of geriatric diseases. The review also presented studies showing that pure compounds could exhibit lower immunomodulatory activities than the crude extract, with some progress being made in identifying the mechanisms involved. However, we found that some studies did not investigate relevant toxicology and pharmacokinetic aspects.
Furthermore, the studies did not provide an in-depth evaluation of the bioactivity of the extracts and the isolated compounds, or in vivo experiments that might indicate therapeutic relevance. Based on the above research and deficiencies, clinicians should remain cautious when using this plant as a therapeutic drug until further research demonstrates the safety, quality, and efficacy of B. carterii. As such, extensive pharmacological and chemical experiments, including human metabolism studies, require future investigations.
A literature review on the pharmacological properties and phytochemicals of B. carterii was performed. The information was retrieved from secondary databases such as PubMed, Chemical Abstracts Services (SciFinder), Google Scholar, and ScienceDirect.
Conflicts of Interest
The authors declare that they have no conflicts of interest.
KH conceptualized the idea. KH conducted the literature survey and edited the manuscript. YRC provided input during preparation and edited the manuscript. Xiaoyan Xu submitted the manuscript. KYL and Xiaoyan Xu provided input during preparation and edited the manuscript. FHZ and MHL provided guide and technical support. Kai Huang and Yanrong Chen contributed equally to this work.
The authors thank for the support of dataset and software from Southern Medical University and the guidance from the guide teachers Prof. Liu and Prof. Zhou. This project was supported by grants from the National Natural Sciences Foundation of China (no. 81774213) and the Innovation Project of Southern Medical University (nos. 201812121009 and 201812121140).
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