Abstract
Pinus trees are widely distributed worldwide, and pine needles, pine bark, pinecones, etc., have potential medicinal value. This paper reviews the medicinal potential of extracts from different organs of three trees of the genus Pinus in East Asia. Studies have shown that pine trees are rich in bioactive compounds, and these compounds have a variety of pharmacological activities, including antioxidation, anti-inflammatory, antibacterial, antitumor, and hypolipidemic effects. The wide range of pharmacological activities of these bioactive components is helpful for the treatment of cardiovascular diseases, inflammatory diseases, tumors, and other diseases. These findings can help promote research on the medicinal potential of Pinus and its organs to realize the efficient utilization of byproducts of pine resources.
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Medicinal Potential of Pine Trees: A Brief Review Focusing on Three Species
Qinsong Li, Qiyu Li, Anping Wang, and Wenxuan Quan *
Pinus trees are widely distributed worldwide, and pine needles, pine bark, pinecones, etc., have potential medicinal value. This paper reviews the medicinal potential of extracts from different organs of three trees of the genus Pinus in East Asia. Studies have shown that pine trees are rich in bioactive compounds, and these compounds have a variety of pharmacological activities, including antioxidation, anti-inflammatory, antibacterial, antitumor, and hypolipidemic effects. The wide range of pharmacological activities of these bioactive components is helpful for the treatment of cardiovascular diseases, inflammatory diseases, tumors, and other diseases. These findings can help promote research on the medicinal potential of Pinus and its organs to realize the efficient utilization of byproducts of pine resources.
DOI: 10.15376/biores.20.1.Li
Keywords: Masson pine; Pollen; Extracts; Biological activity
Contact information: Guizhou Key Laboratory for Information Systems of Mountainous Areas and Protection of Ecological Environment /Guizhou Key Laboratory of Forest Cultivation in Plateau Mountain, Guizhou Normal University, Guiyang, China, 550001; *Corresponding author: wenxuanq@gznu.edu.cn
INTRODUCTION
Pinus trees are widely distributed in the Northern Hemisphere and include various species and large biomasses. There are a variety of Pinus plants distributed in East Asia, among which Masson pine (Pinus massoniana Lamb.), red pine (Pinus densiflora Sieb. et Zucc.), and Korean pine (Pinus koraiensis Sieb. et Zucc.) are typical. These three pine species are important timber trees with slight differences in their physical properties. Overall, their woods exhibit good physical performance, and many studies have explored their primary applications as timber (Wang et al. 2018b; Peng et al. 2022; Zhang et al. 2022; Suri et al. 2022; Park et al. 2024). Many byproducts are produced in the process of forest management and protection, especially after harvesting wood, including branches, needles, bark, pinecones, etc. These materials all contain large amounts of active substances (Fig. 1). Masson pine is a 2-needle pine. It is native to central and southern China and northern Vietnam. It is the main tree species used for afforestation in southern China and one of the main industrial timber tree species in southern China (Feng et al. 2014; Zhang et al. 2015). Red pine, a type of 2-needle pine, is distributed mainly in northeastern China, southeastern Russia, Korea, and Japan (Jiang et al. 2012). Korean pine is a 5-needle pine that is widely distributed in Northeast China, the Korean Peninsula, and the Russian Far East. Korean pine has become a valuable economic tree species because of its excellent wood quality and delicious seeds (Li et al. 2020; Weng et al. 2020; Shitara et al. 2021).
Fig. 1. Metabolites, functions, and applications of Pinus species
In East Asia, various parts of the pine tree, including pine needles, cones, bark, and pollen, have historically been used for their medicinal and dietary properties (Kim and Chung 2000). Masson pine natural products have sedative, analgesic, antipyretic, anti-inflammatory, and antibacterial effects. The active substances are derived mainly from plant bark, pine needles, pollen, etc. Polysaccharides constitute a significant class of bioactive compounds that is recognized for their diverse pharmacological properties, particularly their strong immunomodulatory functions (Wang et al. 2021). Biologically active polysaccharides represent a substantial resource for potential applications, particularly in the medical field. They have attracted considerable interest in vaccine development, emerging as a significant trend in the advancement of vaccine adjuvants (Li et al. 2015). In recent years, with increasing research, the polyphenols (Dziedziński et al. 2021) and flavonoids (Delgado-Alvarado et al. 2022) of Pinus trees have gradually become known and have attracted increasing attention (Fig. 2). Research on the activity of different organs of three kinds of Pinus trees is based mainly on the antioxidative, antiobesity, anticancer, antibacterial, and other aspects of the extract (Table S1).
RESEARCH AND APPLICATION OF MASSON PINE
Polysaccharides are the most common structurally diverse macromolecules produced by organisms during their metabolism, and they are composed of repetitive structural features linked by glycosidic linkages. The normal operation of plants is beneficial for their growth and development. They have attracted much attention because of their significant biological activity, and they have developed rapidly in drug research (Huang et al. 2019; Sivanesan et al. 2022). The polysaccharide structure forms an important part of the cell membranes of higher plants, animals, and microorganisms and is involved in major physiological functions. In recent years, due to the outstanding curative effects of natural products and extracts in the prevention and treatment of diseases, polysaccharides have been applied in the treatment of diseases (Yu et al. 2018; Santos et al. 2021). The biological activity of the Masson pine pollen polysaccharide is reflected mainly in its pharmacological application. Any dose of pollen polysaccharide can increase the general antibody level, blood lymphocyte ratio, lymphocyte proliferation rate, average daily intake, and average daily gain of rabbits (Wei et al. 2011). These findings indicate that pollen polysaccharides have potential as immune enhancers. More importantly, sulfated derivatives of pollen polysaccharides and pollen polysaccharides have been found to inhibit the proliferation of cancer cells (Chu et al. 2013; Shang et al. 2022). These findings indicate the potential of pollen polysaccharides as anticancer drugs.
Fig. 2. Medicinal parts and extraction fractions of Pinus species
There are more in-depth studies on the application of polysaccharides from pollen in poultry. Researchers have reported that pollen polysaccharides have immune-enhancing, immune response-modulating, virus infection-inhibiting, and virus proliferation-inhibiting effects on Proteus mirabilis, subgroup B avian leukosis virus, Bordetella avium, H9N2 subtype avian influenza virus, Newcastle disease virus, and avian leukosis virus subgroup J (Cui et al. 2013; Guo et al. 2014; Zhu et al. 2016; Wang et al. 2019; Shang et al. 2020; Cui et al. 2021; Sha et al. 2021). There is further demonstration of the potential of pollen polysaccharides as immune enhancers. The differential expression of several proteins in pollen polysaccharide-treated chickens is associated with the host innate immune response, stress-induced immune response, or lipid synthesis-related pathways (Yang et al. 2018). Moreover, studies in mice have shown that they are a new type of immune enhancer for livestock and regulate the intestinal microenvironment (Zhao et al. 2013; Niu et al. 2021). In addition, polysaccharides extracted from pollen have antioxidant and antiviral activities (Yang et al. 2015). Among them, pollen polysaccharides were found to have a significant protective effect against CCl4-induced acute hepatotoxicity (Zhou et al. 2018). In addition, pollen polysaccharides were found to have an immune-enhancing effect on a porcine reproductive and respiratory syndrome virus subunit vaccine (Peng et al. 2016). In summary, the polysaccharides extracted from the pollen of Masson pine have antioxidant, antiviral, and immunomodulatory properties. Given the widespread distribution and significant resource availability of Masson pine, these findings indicate considerable potential for future applications and advancements in research and development.
An extract of Masson pine needles can improve the diversity and structure of the gut microbial composition, production performance, egg quality, and serum indicators in laying hens (Guo et al. 2022). The results indicated that the needles are efficient inhibitors with a corrosion inhibition efficiency of 95% (Wang et al. 2018a). Needle polysaccharides significantly improved serum lipid levels and reduced malondialdehyde levels in mice and had significant antioxidant capacity and the ability to reduce inflammation (Chu et al. 2019).
Some active substances are extracted from the needles of Masson pine via the supercritical CO2 fluid extraction method, and studies have shown that the extracts have antioxidant activity (Yang et al. 2021). Several new compounds have been isolated and identified from the extracts of fresh needles of Masson pine, such as massonside A, massonside B, massonside C, massonianoside F, and 3,8-dimethyl-heracetin-7-O-β-D-glucopyranoside, and their biochemical activities need to be further investigated (Xiao et al. 2017, 2020).
Masson pine bark extract was shown to improve the viability and fertility potential of spermatozoa after cryo-resuscitation (Li et al. 2021). Both pinmassin D and abieta-8,11,13,15-tetraen-18-oic acid, obtained from the root bark of Masson pine, moderately inhibited phosphodiesterase type 4D (Fu et al. 2020). Studies have shown that dietary supplements with bark extract as the main ingredient can reduce oxidative stress in healthy elderly people (Ferguson et al. 2022). Additionally, the bark extract significantly inhibited the growth of lung cancer cells. Furthermore, bark extract inhibited the wound healing and migration of lung cancer cells and significantly inhibited the invasive ability of HeLa cells (Li et al. 2016; Mao et al. 2017). Proanthocyanidin from the pine bark of Masson pine significantly inhibited the growth of ovarian cancer cells and induced dose-dependent apoptosis (Liu et al. 2015). These results indicate that extracts related to Masson pine have great medicinal potential.
RESEARCH AND APPLICATION OF RED PINE
Supercritical fluid extracts of red pine needles significantly inhibited the lipopolysaccharide-induced expression of monocyte macrophage (RAW264.7) macrophage proinflammatory mediators, inducible nitric oxide synthase, interleukin-6, and interleukin-1β in mouse leukemia cells (Venkatesan et al. 2017). Moreover, the 40% ethanolic extract of needles had stronger radical scavenging activity (Venkatesan et al. 2019a), and needles had a greater antioxidant capacity than did the bark (Venkatesan et al. 2019b, 2020). Protocatechuic and shikimic acids were isolated and identified from fermented pine needle extract, which has fibrinolytic activity and aspirin-like inhibitory effects on fibrin formation (Park et al. 2016). Ethanolic pine needle extract modulates the stress response in mice, and the stress response in mice is significantly reduced after the administration of ethanolic pine needle extract (Lee et al. 2017a). Studies have shown that the water extract of red pine can be used as an herbal prescription or health functional food to prevent or treat osteoporotic bone diseases (Shim and Ma 2018).
Red pine needle extract promotes the expression of some mitogenic proteins during liver regeneration in rats (Lee et al. 2019). Mice treated with needle extract exhibited complete protection against high-risk human papillomavirus (Lee et al. 2021a). The addition of fermented needle extract to the diet increased the egg production percentage, egg mass, and feed intake throughout the experimental period. In addition, the addition of fermented needle extract to the diet improved egg shell color, yolk color, and shell breakage intensity and increased the antioxidant activity of egg yolk in laying hens (Kothari et al. 2021). Needle hexane extract inhibited the proliferation of gastric cancer cells (Kim et al. 2020d). A variety of peptides extracted from needles have good antibacterial activity, and the peptides show no detectable hemolytic activity or cytotoxicity at antimicrobial concentrations (Lee et al. 2021b). Researchers have also reported potential antiphotoaging properties of needle extracts on the skin (Huh et al. 2015), suggesting that needle extracts also have potential as skin care products.
PineXol is extracted from red pine bark and has beneficial effects, such as antioxidant, anti-inflammatory, and antiadipogenic activities, in vitro. The antiobesity effect of red pine bark extract (PBE) was also achieved by blocking hepatic lipogenesis via the inhibition of adipogenesis in adipocytes (Ahn et al. 2017a,b). Researchers have studied PBE and reported that it is rich in polyphenols, flavonoids, and proanthocyanidins, which exert neuroprotective effects against cerebral ischemic injury in gerbils and have antiamnesic effects (Kim et al. 2018a; Park et al. 2021c; Go et al. 2022). An increase in the phenolic content of bark extracts increases their antioxidant efficiency (Venkatesan et al. 2019).
The addition of bark extract to weaned piglet diets significantly increased the total antioxidant status, and the addition of PBE had no adverse effect on growth (Kim et al. 2022a), whereas the addition of the PBE-chitosan composite improved growth performance and reduced the diarrhea rate and diarrhea index in weaned piglets (Ro et al. 2023). These findings suggest the potential of PBE as a livestock food additive. PBE increased antioxidant indices (superoxide dismutase and catalase activities and malondialdehyde content) and decreased acetylcholinesterase activity in hippocampal lysates of scopolamine-induced amnesic Sprague‒Dawley rats (Kim et al. 2022b). PBE also reduces inflammation (Lee et al. 2018a), lowers blood pressure (Kim et al. 2020a), and enhances the thermal stability of biobased antioxidant films (Han et al. 2018).
Researchers have synthesized silver nanoparticles from aqueous silver nitrate solutions via pine cone extract, a new material with moderate antibacterial activity that inhibits a variety of dermatological pathogens (Velmurugan et al. 2015). Red pine cone extracts also inhibited food poisoning microorganisms (Lee et al. 2018b). Bio-oil prepared by fast pyrolysis of pinewood chips was also found to have antibacterial activity against Bacillus cereus and Listeria monocytogenes (Patra et al. 2015b). Bio-oil was also found to have significant antioxidant capacity (Patra et al. 2015a). The results of cellular studies of extracellular vesicles isolated from the sap of Pinus cereus plants revealed that extracellular vesicles were cytotoxic to tumor cells but not to normal cells (Kim et al. 2020b). Methane emissions from cattle are significantly reduced when red pine extracts are added to their diet (Lee et al. 2020). Among the various compounds from red pine needles, dehydroabietic and 4-epi-trans-communic acids have been isolated. Researchers confirmed that both compounds inhibited angiotensin-converting enzyme activity in human umbilical vein endothelial cells (Park et al. 2021d). In experiments in which a human keratinocyte cell line was used as the study material, it was confirmed that malonic acid isolated from red pine extracts retarded cellular aging (Park et al. 2021a). A substance was extracted from pine branches with ethanol, and the results of in vitro tests revealed that the extract inhibited cellular inflammation and reduced cellular damage (Kim et al. 2021).
RESEARCH AND APPLICATION OF KOREAN PINE
Korean pine needle extract has antiobesity, cholesterol-lowering, hepatoprotective, and antidiabetic properties. Researchers have reported that an ethanolic extract of needles containing lambertianic acid has antiobesity and cholesterol-lowering effects (Lee et al. 2016b). The extract from needles is linked to a decrease in waist circumference and cholesterol levels while also increasing superoxide dismutase activity (Lee et al. 2016a). These findings suggest that needle extract ameliorates alcohol-induced fatty liver via the activation of phosphorylated liver kinase B1 (LKB1)–AMP-activated protein kinase and the modulation of proteins related to lipogenesis synthesis, cholesterol synthesis, and fatty acid oxidation (Hong et al. 2017; Park et al. 2021b). Through experiments in rats, the needle extract was also found to have anticancer, antiobesity, antidiabetic, and antihyperlipidemic biological activities (Lee et al. 2022a). Korean pine needles have fatigue resistance, as assessed by weight-loaded forced swimming and rotarod tests in mice (Lee et al. 2022b).
The polyphenols of Korean pine pinecones have been more intensively studied, and the phenolic compound of the ethanol eluent of polyphenols from the pinecone of Korean pine showed the strongest inhibitory effect on human colon cancer line cells (Yi et al. 2016; 2017a). Subsequently, it was found to significantly inhibit tumor growth (Yi et al. 2017b). Phytochemicals prepared from extracts of waste red pine cones also increased the contents of major functional fatty acids, conjugated linoleic acid, and eicosapentaenoic acid, but the ω6:ω3 fatty acid ratio was also reduced in the milk of Holstein cows (Kim et al. 2016). The addition of pinecone extract to the diet of hens increased egg production and the immune response during inflammation and improved the intestinal flora (Kim et al. 2018b). This study provides a basis for the utilization of pine cone extracts in animal husbandry and introduces the use of pinecones. Researchers have prepared novel chitosan microspheres encapsulated with pinecone polyphenols and pine polyphenol-loaded microspheres with protective effects against 60Co-γ radiation-induced damage in mice via the emulsion crosslinking technique (Shao et al. 2018). The biological activity of pinecone extracts has also been investigated, and the results revealed that pinecone extracts have anticancer activity (Lee et al. 2017b). These findings indicate the potential of pinecone extract as an anticancer drug.
Among the studies on pinecones, pine cone polysaccharides have been studied more frequently. The extraction of pinecone polysaccharides from pinecones via the hot water extraction method results in polysaccharide extraction rates of up to 10.25% (Zhao et al. 2019). Researchers have extracted various polysaccharide fractions. These polysaccharide fractions have significant scavenging effects on hydroxyl radicals, as well as a high reducing ability (Zhang et al. 2016, 2021a). Pine cone extracts have in vitro and in vivo antibacterial effects (Kim et al. 2020c), and they inhibit cell proliferation through cell cycle arrest (Xin et al. 2021). The essential oil of a pinecone nanoemulsion was prepared from the essential oil of pinecones, and the prepared nanoemulsion has good stability and can effectively inhibit tumor growth, promote apoptosis, and inhibit the proliferation of cancer cells (Zhang et al. 2020).
Few studies have examined extracts of Korean pine bark, which have inhibitory effects on α-glucosidase activity and, at the same time, have the strongest inhibitory effect on nitric oxide production in activated macrophages (Shpatov et al. 2017). The extract of bark had a good radioprotective effect on rat splenocytes (Yun et al. 2017). Bark polyphenols have antioxidant capacity, inhibit cancer cell growth, induce cell cycle arrest and induce apoptosis (Huang et al. 2021). Polysaccharides obtained from purified pine nuts effectively protect cells from damage caused by CCl4 (Qu et al. 2019). Pinecone scale polyphenols promote the proliferation of osteoblasts (Diao et al. 2018). Researchers have improved the extraction process of Korean pine nut-coated films and reported that Korean pine nut-coated films have a natural antioxidant capacity (Zhang et al. 2021b). A study of various substances extracted from Korean pine shoots revealed that the extracted compounds had an effect on C6 glioma cells via the induction of nerve growth factor secretion (Park et al. 2020). Researchers added Korean pine extract to the feed of pigs, which increased the average daily weight gain (Seok et al. 2021). The hot water extract of Korean pine bark has a low yield but a high content of phenolic compounds. However, its antioxidant activity is low (Ku et al. 2007). Korean pine waste extracts have great application value in both human health and the livestock industry, which helps promote the use of resources and the development of related industries.
CONCLUSIONS AND FUTURE PERSPECTIVES
This paper has examined the medicinal potential of three pine species, with a particular emphasis on the polysaccharides found in Masson pine pollen, which have been extensively studied, particularly for their immunomodulatory effects, demonstrating significant application prospects. In contrast, research on needle and bark extracts is relatively limited; however, several bioactive compounds that exhibit anti-inflammatory and anticancer properties have nonetheless been identified. Research on red pine has focused primarily on needle and bark extracts, which have yielded notably positive results as livestock feed additives, although the efficacy of various extraction methods shows considerable variability. Similarly, investigations into Korean pine have focused predominantly on needle and bark extracts, with needle extracts primarily exhibiting antiobesity properties and bark extracts demonstrating anticancer effects, suggesting their potential utility as animal feed additives. Overall, Masson pine is distinct from the other two species because of its extensive distribution, substantial biostorage capacity, and greater application potential. In terms of medicinal capacity, all three pine species possess a significant array of active compounds, including polysaccharides, flavonoids, phenols, and bio-oils, with polysaccharides, flavonoids, and phenols constituting the principal components.
These pine species contain a diverse array of active compounds, including polysaccharides, flavonoids, phenols, and bio-oil. Polysaccharides, which are predominantly found in pine pollen, are known to enhance immune function and inhibit the proliferation of cancer cells, whereas flavonoids, which are concentrated in pine needles and bark, exhibit antioxidant, antibacterial, antihypertensive, and antiobesity properties. Phenolic compounds display antioxidant, antiobesity, and anticancer activities, and bio-oils are recognized for their antibacterial and antioxidant effects. Although further research is necessary to comprehensively validate their therapeutic effects, existing studies underscore their significant medicinal potential. This paper also addresses the critical importance of employing appropriate extraction techniques to efficiently isolate these bioactive components while maintaining their biological activity. Research on Pinus not only provides a foundation for medical applications but also suggests that ongoing investigations will unveil new opportunities for drug development and advances in the nutraceutical industry.
ACKNOWLEDGMENTS
The authors are grateful to the National Natural Science Foundation of (31960301), Projects of Guizhou Provincial Department of Education (QJJ[2024]324), and the Postdoctoral Research Foundation of China Project (2020M673583XB).
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Article submitted: October 11, 2024; Peer review completed: December 8, 2024; Revised version received and accepted: December 27, 2024; Published: January 10, 2025.
DOI: 10.15376/biores.20.1.Li
APPENDIX
Table S1. Three Pinus Species Extract Sources, Compounds, Extraction Methods, Experimental Materials, Effect, Products or Possible Uses
