Review Caries Res 2015;49(suppl 1):38–45 DOI: 10.1159/000377734
Published online: April 13, 2015
Natural Products and Caries Prevention Lei Cheng a, b Jiyao Li a, b Libang He a, b Xuedong Zhou a, b State Key Laboratory of Oral Diseases and b Department of Operative Dentistry and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Key Words Dental caries · Natural products · Polyphenol compounds · Traditional herbs
Abstract Dental caries is considered as the most common polymicrobial oral disease in the world. With the aim of developing alternative approaches to reduce or prevent the decay, numerous papers showed the potential anticaries activity of a number of natural products. The natural products with anticaries effects are selected from e.g. food, beverages, flowers or traditional herbs. Most of the effective components are proven to be polyphenol compounds. Many of the natural products are studied as antibacterial agents, while some of them are found to be effective in shifting the de-/remineralization balance. However, the mechanisms of the anticaries effects are still unclear for most of the natural products. In the future, more efforts need to be made to seek novel effective natural products via in vitro experiment, animal study and in situ investigations, as well as to enhance their anticaries effects with the help of novel technology like nanotechnology. © 2015 S. Karger AG, Basel
Dental caries is still a challenge for human beings [Selwitz et al., 2007; Hu et al., 2011]. The knowledge of dental caries increases, but investigators and dentists are struggling for the prevention and treatment of the decay. Though antibiotics are very effective in preventing dental © 2015 S. Karger AG, Basel 0008–6568/15/0497–0038$39.50/0 E-Mail [email protected] www.karger.com/cre
caries in vivo and in vitro, their excessive use can lead to alterations of the oral and intestinal flora [Goldin and Gorbach, 1984]. Besides, undesirable side effects such as development of bacteria to tolerance, vomiting, diarrhea and teeth stains limited their use [Dickinson and Surawicz, 2014; Gopinath et al., 2014; Vennila et al., 2014]. Numerous clinical and laboratory papers in the past decades have indicated the anticaries effect of fluoride, which exerts its caries-preventive effect by shifting the de-/remineralization balance favorably. However, there is still a need to seek products complementary to fluoride. There has been a rising interest in biologically active compounds derived from natural products which may have potential therapeutic uses in dentistry [Groppo et al., 2008; Newman, 2008]. Researchers selected different foods and beverages for their investigations like e.g. tea, coffee, grape, propolis, shiitake mushrooms (Lentinula edodes) or traditional herbs [Spratt et al., 2012]. Some of the natural products have already been added into mouth rinses or chewing gums for in situ experiments [Campus et al., 2011; Gupta et al., 2014]. Most of the studies found that the effective compounds in natural products belong to polyphenol compounds. A polyphenol is any substance that contains at least 1 aromatic ring with 1 or more hydroxyl groups (other substituents can be present) [Yoo et al., 2011]. Polyphenol compounds are derived from different kinds of natural products, and in vitro experiments indicated that some of them could be effective in killing bacteria or inhibiting biofilms [Ferrazzano et al., 2011], while some of them were able to regulate the demineralization or remineralProf. Xuedong Zhou State Key Laboratory of Oral Diseases West China Hospital of Stomatology Sichuan University, Chengdu (China) E-Mail zhouxd @ scu.edu.cn
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a
Galla Chinensis
Galla chinensis, formed when the Chinese sumac aphid Baker (Melaphis chinensis Bell) parasitizes the leaves of Rhus chinensis Mill, is a potentially interesting agent in dental caries prevention. In several previous studies, galla chinensis extracts (GCE) have been found to be effective in inhibiting demineralization and enhancing remineralization [Chu et al., 2007; Cheng et al., 2008; Zou et al., 2008; Guo et al., 2012]. Cheng et al. [2008] found GCE had enhanced the efficacy of fluoride in shifting the de-/remineralization of dental enamel [Cheng et al., 2008]. In the studies of Huang et al. [2010], there was a significant synergistic effect of combined nanohydroxyapatite and galla chinensis treatments on the remineralization. The mechanism of galla chinensis is still unclear, but several hypotheses were proposed to explain it. Chu et al. [2007] demonstrated that chemical compounds of galla chinensis might act as a calcium ion carrier which supplied the lesion body of initial dental caries with calcium ions from the remineralization solution. Zhang et al. [2009a] proposed the ‘enamel organic matrix-galla chinensis-Ca’ hypothesis. An atomic force microscopy study offered some evidence for this hypothesis. It indicated that the morphological changes and the increased roughness of carious enamel surface treated with GCE, and numerous nanosize elliptical particles were distributed on the lesion surface [Zhang et al., 2009a]. Scanning electron microscopy, energy-dispersive spectrometry and X-ray microdiffraction were applied to analyze the morphological, chemical and crystal characters of the remineralized surface, respectively, on initial carious enamel treated with GCE [Zhang et al., 2009b]. The chemical compounds of galla chinensis are complex, GCE-B1 and GCE-B2 were extracted from GCE and characterized as gallic acid and methyl gallate by spectroscopic methods including mass spectrometry and nuclear magnetic resonance [Chu et al., 2007]. Cheng et al. [2008] compared the remineralization potential of both GCE and gallic acid via transverse microradiography investigation in an in vitro study. The results indicated that both of the compounds could reduce the lesion depth and the integrated mineral loss compared with a negative control group. More detailed analyses were then carried out to Natural Products to Prevent Dental Caries
evaluate the remineralization of the surface layer and the lesion body. Interestingly, more remineralization was observed on the surface layer after being treated with gallic acid, while GCE treatment enhanced more mineral deposition in the lesion body [Cheng et al., 2008]. Combined with other investigations, the mechanism seems to be different between GCE and gallic acid [Cheng et al., 2009, 2010; Cheng and ten Cate, 2010]. Gallic acid might act as a calcium ion carrier and helps to deposit more calcium ions on the surface layer of dental caries lesions. GCE is composed of different polyphenol compounds; some of them might form a barrier to prevent calcium ion deposition on the lesion surface. Then, the remineralization of the surface layer was prevented, but more calcium ions could be transmitted through the surface layer into the lesion body. So it explains why remineralization was more obvious in the lesion body. Another investigation indicated that gallic acid affects and participates in the formation of hydroxyapatite, and regulates the morphology and structure of the crystals, to enhance the remineralization process [Tang et al., 2015]. The original GCE solution has a low pH, which might dissolve dental enamel. An in vitro experiment was designed to investigate the effects of pH on GCE stability, as well as its anticaries properties. The results showed that GCE solutions were unstable under neutral and alkaline conditions. pH did not significantly influence the inhibiting effect of GCE on enamel demineralization [Huang et al., 2012]. Besides its potential effects in shifting the de-/remineralization balance, GCE have been proven to be able to inhibit dental biofilms. In an in vitro experiment, Cheng et al. [2010] investigated the effects of GCE at different stages of biofilms formed with saliva as inoculum. The results demonstrated that GCE treatments inhibited growth and acid metabolism of both nascent and mature microcosm biofilms. Xie et al. [2008] designed an experiment to investigate the antibiofilm effect of GCE using a 4-organism bacterial consortium (Streptococcus sanguis, Streptococcus mutans, Actinomyces naeslundii, Lactobacillus rhamnosus). A GCE was able to inhibit the growth of multiple-species biofilms on enamel blocks and then reduced the demineralization of dental enamel.
Propolis
Propolis has attracted increased interest due to its antimicrobial activity against a wide range of pathogenic microorganisms. The major constituents of propolis are Caries Res 2015;49(suppl 1):38–45 DOI: 10.1159/000377734
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ization of dental hard tissue [Chu et al., 2007; Cheng et al., 2008]. So this review is to summarize previous studies of natural products and their components on the prevention of dental caries.
Magnolia Bark
Magnolia bark is a plant part which has been widely used in medicine for 2,000 years [Watanabe et al., 1983]. The two effective components of magnolia bark extract are magnolol and honokiol which have been reported to inhibit the growth of S. mutans, Streptococcus sobrinus, Porphyromonas gingivalis, Fusobacterium nucleatum, Aggregatibacter actinomycetemcomitans, Capnocytophaga gingivalis and Veillonella dispar in vitro and to reduce the dental caries values in an animal experiment [Chang et al., 1998; Ho et al., 2001; Greenberg et al., 2007]. Magnolia bark extract has previously been added into a xylitol chewing gum. In a randomized controlled intervention trial, 30-day use of a chewing gum containing magnolia bark extract showed beneficial effects on oral health, including reduction of salivary mutans streptococci, plaque acidogenicity and bleeding on probing [Campus et al., 2011].
Tea
Tea is considered as one of the most widely consumed beverages in the world, especially in Asian countries, and tea is also reported as the major source of flavan-3-ols and flavonols in the US diet [Song and Chun, 2008]. Though tea is composed of polyphenols, the polyphenol type and 40
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levels are determined by how the tea has been processed [Astill et al., 2001]. The effective components of green tea are mainly attributed to its polyphenol contents commonly referred to as catechins, including epigallocatechin-3-gallate, epigallocatechin, epicatechin-3-gallate and epicatechin [Taylor et al., 2005]. Black tea comprises oligomers such as theaflavins and polymers known as thearubigins. Oolong tea contains considerable amounts of catechins and oligomerized catechins [Balentine et al., 1997]. Catechins and theaflavins, polyphenolic compounds derived from tea (Camellia sinensis, fam. Theaceae), have been reported to have a wide range of biological activities including prevention of tooth decay and oral cancer in several in vitro studies [Yang, 1997; Yang et al., 1999, 2000; Hamilton-Miller, 2001; Yang et al., 2002]. Green tea might be linked to a lower incidence of some pathological conditions including oral cancer, dental caries, stroke, cardiovascular diseases and obesity [Taylor et al., 2005; Chacko et al., 2010]. Various papers revealed the anticaries effects of tea extracts via in vitro and in vivo experiments. The polyphenol contents of green tea have been reported to inhibit varieties of pathogenic bacterial growth including S. mutans and S. sobrinus. Another in vitro study confirmed the inhibitory activities of green tea extracts on cariogenic and periodontopathic bacteria [Araghizadeh et al., 2013]. Application (oral rinsing) of green tea solution without sugar for a short time could strongly inhibit salivary and plaque numbers of S. mutans which are important causative bacteria of caries both initially and secondarily [Awadalla et al., 2011]. The study of Lee et al. [2004] indicated that green tea leaves and black tea can be used as a convenient, slow-release source of catechins and theaflavins to prevent dental caries. Volunteers gently chewed 2 g of green tea leaves for 5 min and thoroughly rinsed the mouth. Then high concentrations of catechins (Cmax = 131.0–2.2 μM) and theaflavins (Cmax = 1.8–0.6 μM) were observed in saliva according to a high performance liquid chromatography system analysis. Camellia extract MJ (Taiyo Kagaku), a food additive in Japan, is a green tea extract with over 1,500 ppm of fluoride. A cup of green tea was reported to contain 0.5–1 g of catechins/l [Hamilton-Miller, 2001], while Camellia extract MJ contains approximately 0.06 g of catechins/l. Suyama et al. [2011] used chewing gum containing Camellia extract MJ as the source of fluoride. An in situ experiment found it produced a superior level of remineralization and acid resistance of dental enamel [Suyama et al., 2011]. Oolong tea extract (OTE) was shown to possess a strong antiglucosyltransferase activity which originates Cheng/Li/He/Zhou
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flavonoids [Usia et al., 2002], organic acids, phenols, various kinds of enzymes, vitamins and minerals [Velikova et al., 2000]. Tunisian propolis ethanol extract was proven to have anticariogenic and antibiofilm effects in an in vitro experiment [Kouidhi et al., 2010]. The effective component of propolis could inhibit both glucosyltransferase activities and bacterial growth [Koo et al., 2002b]. Besides, the cytotoxicity of propolis was tested using gingival fibroblast cells. The results indicated that appropriate solutions can be prepared which are strongly antibacterial and noncytotoxic as well [Sonmez et al., 2005]. Furthermore, a previous study investigated the ethanolic extract of a novel type of propolis and its purified hexane fraction on mutans streptococcus biofilms and the development of dental caries in rats. The results suggested that the cariostatic properties of propolis were due to the reduction of acid production and acid tolerance of cariogenic streptococci; these biological activities may be attributed to its high content of fatty acids [Duarte et al., 2006b].
Grapes
Grapes (Vitis vinifera) [Daglia et al., 2007a; Thimothe et al., 2007] and grape seed extracts (GSE) [Sarni-Manchado et al., 1999] have been considered as effective anticaries agents. Phenolic fractions of a limited number of grape varieties, including V. vinifera and Vitis interspecific hybrid varieties, can significantly decrease the enzymatic activity of S. mutans GtfB and GtfC [Yano et al., 2012]. Proanthocyanidins in GSE are thought to be the effective components in inhibiting dental caries. Proanthocyanidins could inhibit the surface-adsorbed gluocsyltransferase and F-ATPase activities, and the acid production by S. mutans [Duarte et al., 2006a]. The capability of GSE in inhibiting the demineralization and/or promoting the remineralization of artificial root carious lesions was reported previously [Xie et al., 2008]. Hypotheses have been proposed for GSE promoting remineralization of dental caries. GSE may contribute to mineral deposition on the superficial layer of the lesion [Kosasi et al., 1989; Xie et al., 2008]. The combination of GSE with fluoride showed both significant antiplaque activities and antioxidant properties. The results indicated that the antibiofilm activity of the combination of 2,000 μg/ml of GSE with 10.2 mg/ml of Fluorinol® was greater than that of each compound tested alone [Furiga et al., 2014]. Grape phenolic extracts could be maintained in the wine and keep the ability to inhibit bacteria. Several papers investigated the antimicrobial effects of red wine. Thimothe et al. [2007] found that wine and grape phenolic extracts, as well as pomace phenolic extracts, could kill different Streptococcus spp. strains associated with dental caries. In another study, red wine and dealcoholized red Natural Products to Prevent Dental Caries
wine were tested using a biofilm model of the supragingival plaque. The results indicated that red wine and dealcoholized wine had an antimicrobial effect against F. nucleatum and Streptococcus oralis [Munoz-Gonzalez et al., 2014].
Coffee
Coffee, another popular worldwide drink, was reported to combat some diseases, including dental caries [Daglia et al., 2007b; Antonio et al., 2011, 2012]. The antibacterial ability was also due to polyphenols [Koo et al., 2002a; Yatsuda et al., 2005; Farah et al., 2006]. A recent paper has proven the antibacterial effect of Coffea canephora extract against S. mutans, and its inhibiting effects on the demineralization of tooth enamel under biofilm conditions were also observed [Antonio et al., 2011, 2012]. The action mode is considered that C. canephora caused bacterial lysis and consequently the release of calcium into the medium. One of the advantages of coffee is that it is normally consumed in a concentrated form (6– 10%), which is higher than the effective concentration reported previously (1–2%) [Meckelburg et al., 2014].
Cacao
Cacao beans, the main constituent of chocolate, contain some polyphenols which exhibit antiglucosyltransferase activity. The cariostatic activity of cacao mass extract was studied in vitro and in experimental animals [Ooshima et al., 2000a, b]. A previous study indicated that cacao mass extract possesses some anticariogenic potential, but its anticaries activity is not strong enough to significantly suppress the cariogenic activity of sucrose [Ooshima et al., 2000a]. An animal study demonstrated that the extract could become a novel anticaries substance as a mild chemoprophylactic agent [Ooshima et al., 2000b].
Hesperidin
Hesperidin, a citrus flavonoid, was able to preserve bovine dentine collagen against proteolytic degradation. It has also been reported that hesperidin reduced the susceptibility of dentine lesions to acid-dependent demineralization with the potential to promote the remineralization process [Hiraishi et al., 2011]. In another paper, hesCaries Res 2015;49(suppl 1):38–45 DOI: 10.1159/000377734
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from polymeric polyphenols in oolong tea leaves [Nakahara et al., 1993]. Furthermore, OTE has been shown to inhibit experimental dental caries in specific pathogenfree rats infected with either S. sobrinus 6715 (serotype g) or S. mutans MT8148R (serotype c) when given in both diet and drinking water [Ooshima et al., 1993]. In addition, OTE has been shown to reduce dental plaque deposition in humans [Ooshima et al., 1994]. Oolong tea polyphenols may inhibit bacterial adherence to the tooth surface by reducing the cell surface hydrophobicity of mutans streptococci, and OTE may inhibit the caries-inducing activity of mutans streptococci by reducing the rate of acid production [Matsumoto et al., 1999].
Traditional Medicine
Different countries have their folk medicine, and researchers tried to select effective agents from a great amount of traditional herbs in their countries. In Asia, Wong et al. [2010] investigated 20 traditional Chinese medicines for their antimicrobial activity against 4 common oral bacteria, including Streptococcus mitis, S. sanguis, S. mutans and P. gingivalis. The results indicated that 13 of them had an antibacterial effect on some bacteria species and fructus armeniaca mume was effective against all 4 bacteria. Rheum undulatum (Polygonaceae) is a perennial herb distributed and cultivated mainly in East Asia [Choi et al., 2005]. The dichloromethane fraction from R. undulatum, which is composed mainly of aloe emodin, emodin, chrysophanol and physcion, had inhibitory effects on the glycolytic acid production of S. mutans biofilms [Kim et al., 2011]. In another paper, ethanol extracts of 35 groups of Thai herbal formulas were tested for antibacterial activity against S. mutans. The tests found that Albizia myriophylla had the strongest activity with minimum inhibitory concentrations at 3.9 μg/ml against S. mutans [Joycharat et al., 2012]. In Laos and Vietnam, Kammu women used 3 plants (including Dracontomelon dao nuts) to stain their teeth black. The soot of D. dao nuts could effectively inhibit growth of salivary mutans streptococci in an in vitro experiment [Tayanin and Bratthall, 2006]. Phyllanthus emblica is one of the most celebrated herbs in the Indian system of traditional medicine. Emblica officinalis extract could reduce acid production, biofilm formation, cell surface hydrophobicity, glucan production, and sucrose-dependent and independent adherence of S. mutans [Hasan et al., 2012]. Different populations and cultures around the world have been using various tools, like porcupine bones or chewing sticks to clean their teeth and gums [Khoory, 1983; Eid et al., 1990]. In middle-eastern and eastern African cultures, a chewing stick called miswak is widely used to clean the teeth and gums. Darmani et al. [2006] found that aqueous extracts of miswak and derum en42
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hance the growth of fibroblasts and inhibit the growth of cariogenic bacteria, and the derum extract had greater activity than that of miswak. More et al. [2008] studied other chewing sticks made of traditional South African medicinal plants, including their antibacterial effects and cytotoxicity. The extracts of Annona senegalensis, Englerophytum magalismontanum, Dicerocarym senecioides, Euclea divinorum, Euclea natalensis and Parinari curatellifolia showed positive inhibitory activity against five microorganisms [More et al., 2008]. In all of temperate Europe and in the Himalayas, China and Japan, the stem bark of Juglandaceae (Juglans regia, walnut) is quite popular and is used as a tooth-cleaning tool. The bark of J. regia is also known to contain fluorides which have been well studied as an effective anticaries agent [Almas and al-Lafi, 1995]. One study has concluded that these chewing sticks were 20% poorer than the toothbrush in reducing plaque scores. The extracts were tested for their effect on the growth, in vitro adherence, glucan-induced aggregation and the acid-producing ability of S. mutans [Jagtap and Karkera, 2000]. In western, central and southern Mexico, Iostephane heterophylla was collected, and the compounds isolated from the roots had a significant antimicrobial activity against oral pathogens [Hernandez et al., 2012].
Conclusion
Though numerous papers focused on how to use natural products to combat dental caries, there are still some problems to be solved. Firstly, the natural products showed weaker effects in caries prevention compared with traditional chemical agents, like antimicrobials or fluoride. Secondly, the mechanisms of the effective components are still unclear for most of the natural products. So in future studies, more efforts should be made to find potential agents isolated from natural products, investigate their mechanisms and modify them to have stronger inhibiting effects on dental caries. (1) Novel natural products and effective components should be found in future investigations. In previous studies, most of the effective compounds isolated from natural products are polyphenols, which are found in plants, vegetables and flowers. It is interesting to find out some other natural products to prevent dental caries. In some traditional medicine systems, not only plants, but also animal extracts and minerals are used as medicine. Furthermore, the studies of natural products focus on two aspects: antibacterial effects and shifting the de-/reminCheng/Li/He/Zhou
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peridin was found to reduce lesion depth and mineral loss, indicating that hesperidin inhibited demineralization and probably enhanced remineralization even under fluoride-free conditions [Islam et al., 2012]. The mechanism of hesperidin may be related to its interaction with collagen and/or noncollagenous proteins, resulting in stabilizing the collagen matrix and induction of remineralization [Liu et al., 2004].
eralization balance. Besides, very few natural products like stevia were used to replace the dietary carbohydrates; so, in the future, some additional agents isolated from natural products might be able to eliminate dietary carbohydrates from the diet. (2) More cytotoxicity tests are needed. At the early stages, experiments were carried out to test the antibacterial effect of natural products on the planktonic cell. Then biofilm experiments were designed. Some researchers started to apply animal studies or in situ experiments in their investigations [Brighenti et al., 2012]. For most of the natural products, studies in vitro have indicated their antibacterial activity against cariogenic bacteria [Ho et al., 2001; Greenberg et al., 2007, 2008], but the clinical effects still remain unproven [Wallace, 2004]. Therefore, more in situ experiments are needed in the future. Though most of the natural products are claimed to have been used for a long time in traditional medicine, cytotoxicity tests are still needed if they are planned to be used in the clinic. (3) Chemical component or combined effect? In many previous papers, crude extracts of natural products were used, while some researchers tried to find out the effective component isolated from the natural products. For example, the methanolic extract from Artocarpus heterophyllus showed antibacterial activity against cariogenic bacteria. Then serial chromatographic purifications offered 2 active compounds, including 6-(3-methyl-Lbutenyl)-5,2′,4′-trihydroxy-3-isoprenyl-7-methoxyflavone and 5,7,2′,4′-tetrahydroxy-6-isoprenylflavone [Sato et al., 1996]. Another example is galla chinensis.
Several papers found that the crude extracts of galla chinensis had satisfactory effects on promoting remineralization of dental enamel. Gallic acid is one promising component isolated from galla chinensis, but the action modes were different between GCE and gallic acid. Tang et al. [2015] made a further investigation on the effect of gallic acid on the morphology and growth of hydroxyapatite crystals. Thus, it implied that the crude extract of galla chinensis might have several effective components which showed combined effects on the regulation of the de-/remineralization balance. (4) Novel technology should be helpful in enhancing the anticaries effect of natural products. He et al. [2014] synthesized nanosized calcium phosphate particles incorporating tea polyphenol and tested their potential as caries-preventive agent. Nanosized tea polyphenol-modified CaP at lower pH (5.5) significantly enhanced remineralization of dental hard tissue, to the same extent as the nanohydroxyapatite controls. Since tea polyphenol was proven to be able to inhibit bacterial growth and enzyme activities, the novel tea polyphenol-modified CaP nanoparticle, at low pH, is a potential dual-functional remineralization and antibacterial product. Nanotechnology will be a useful tool to develop the natural products in caries prevention.
Disclosure Statement The authors have no conflict of interest to declare.
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Published online: April 13, 2015
Natural Products and Caries Prevention Lei Cheng a, b Jiyao Li a, b Libang He a, b Xuedong Zhou a, b State Key Laboratory of Oral Diseases and b Department of Operative Dentistry and Endodontics, West China Hospital of Stomatology, Sichuan University, Chengdu, China
Key Words Dental caries · Natural products · Polyphenol compounds · Traditional herbs
Abstract Dental caries is considered as the most common polymicrobial oral disease in the world. With the aim of developing alternative approaches to reduce or prevent the decay, numerous papers showed the potential anticaries activity of a number of natural products. The natural products with anticaries effects are selected from e.g. food, beverages, flowers or traditional herbs. Most of the effective components are proven to be polyphenol compounds. Many of the natural products are studied as antibacterial agents, while some of them are found to be effective in shifting the de-/remineralization balance. However, the mechanisms of the anticaries effects are still unclear for most of the natural products. In the future, more efforts need to be made to seek novel effective natural products via in vitro experiment, animal study and in situ investigations, as well as to enhance their anticaries effects with the help of novel technology like nanotechnology. © 2015 S. Karger AG, Basel
Dental caries is still a challenge for human beings [Selwitz et al., 2007; Hu et al., 2011]. The knowledge of dental caries increases, but investigators and dentists are struggling for the prevention and treatment of the decay. Though antibiotics are very effective in preventing dental © 2015 S. Karger AG, Basel 0008–6568/15/0497–0038$39.50/0 E-Mail [email protected] www.karger.com/cre
caries in vivo and in vitro, their excessive use can lead to alterations of the oral and intestinal flora [Goldin and Gorbach, 1984]. Besides, undesirable side effects such as development of bacteria to tolerance, vomiting, diarrhea and teeth stains limited their use [Dickinson and Surawicz, 2014; Gopinath et al., 2014; Vennila et al., 2014]. Numerous clinical and laboratory papers in the past decades have indicated the anticaries effect of fluoride, which exerts its caries-preventive effect by shifting the de-/remineralization balance favorably. However, there is still a need to seek products complementary to fluoride. There has been a rising interest in biologically active compounds derived from natural products which may have potential therapeutic uses in dentistry [Groppo et al., 2008; Newman, 2008]. Researchers selected different foods and beverages for their investigations like e.g. tea, coffee, grape, propolis, shiitake mushrooms (Lentinula edodes) or traditional herbs [Spratt et al., 2012]. Some of the natural products have already been added into mouth rinses or chewing gums for in situ experiments [Campus et al., 2011; Gupta et al., 2014]. Most of the studies found that the effective compounds in natural products belong to polyphenol compounds. A polyphenol is any substance that contains at least 1 aromatic ring with 1 or more hydroxyl groups (other substituents can be present) [Yoo et al., 2011]. Polyphenol compounds are derived from different kinds of natural products, and in vitro experiments indicated that some of them could be effective in killing bacteria or inhibiting biofilms [Ferrazzano et al., 2011], while some of them were able to regulate the demineralization or remineralProf. Xuedong Zhou State Key Laboratory of Oral Diseases West China Hospital of Stomatology Sichuan University, Chengdu (China) E-Mail zhouxd @ scu.edu.cn
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a
Galla Chinensis
Galla chinensis, formed when the Chinese sumac aphid Baker (Melaphis chinensis Bell) parasitizes the leaves of Rhus chinensis Mill, is a potentially interesting agent in dental caries prevention. In several previous studies, galla chinensis extracts (GCE) have been found to be effective in inhibiting demineralization and enhancing remineralization [Chu et al., 2007; Cheng et al., 2008; Zou et al., 2008; Guo et al., 2012]. Cheng et al. [2008] found GCE had enhanced the efficacy of fluoride in shifting the de-/remineralization of dental enamel [Cheng et al., 2008]. In the studies of Huang et al. [2010], there was a significant synergistic effect of combined nanohydroxyapatite and galla chinensis treatments on the remineralization. The mechanism of galla chinensis is still unclear, but several hypotheses were proposed to explain it. Chu et al. [2007] demonstrated that chemical compounds of galla chinensis might act as a calcium ion carrier which supplied the lesion body of initial dental caries with calcium ions from the remineralization solution. Zhang et al. [2009a] proposed the ‘enamel organic matrix-galla chinensis-Ca’ hypothesis. An atomic force microscopy study offered some evidence for this hypothesis. It indicated that the morphological changes and the increased roughness of carious enamel surface treated with GCE, and numerous nanosize elliptical particles were distributed on the lesion surface [Zhang et al., 2009a]. Scanning electron microscopy, energy-dispersive spectrometry and X-ray microdiffraction were applied to analyze the morphological, chemical and crystal characters of the remineralized surface, respectively, on initial carious enamel treated with GCE [Zhang et al., 2009b]. The chemical compounds of galla chinensis are complex, GCE-B1 and GCE-B2 were extracted from GCE and characterized as gallic acid and methyl gallate by spectroscopic methods including mass spectrometry and nuclear magnetic resonance [Chu et al., 2007]. Cheng et al. [2008] compared the remineralization potential of both GCE and gallic acid via transverse microradiography investigation in an in vitro study. The results indicated that both of the compounds could reduce the lesion depth and the integrated mineral loss compared with a negative control group. More detailed analyses were then carried out to Natural Products to Prevent Dental Caries
evaluate the remineralization of the surface layer and the lesion body. Interestingly, more remineralization was observed on the surface layer after being treated with gallic acid, while GCE treatment enhanced more mineral deposition in the lesion body [Cheng et al., 2008]. Combined with other investigations, the mechanism seems to be different between GCE and gallic acid [Cheng et al., 2009, 2010; Cheng and ten Cate, 2010]. Gallic acid might act as a calcium ion carrier and helps to deposit more calcium ions on the surface layer of dental caries lesions. GCE is composed of different polyphenol compounds; some of them might form a barrier to prevent calcium ion deposition on the lesion surface. Then, the remineralization of the surface layer was prevented, but more calcium ions could be transmitted through the surface layer into the lesion body. So it explains why remineralization was more obvious in the lesion body. Another investigation indicated that gallic acid affects and participates in the formation of hydroxyapatite, and regulates the morphology and structure of the crystals, to enhance the remineralization process [Tang et al., 2015]. The original GCE solution has a low pH, which might dissolve dental enamel. An in vitro experiment was designed to investigate the effects of pH on GCE stability, as well as its anticaries properties. The results showed that GCE solutions were unstable under neutral and alkaline conditions. pH did not significantly influence the inhibiting effect of GCE on enamel demineralization [Huang et al., 2012]. Besides its potential effects in shifting the de-/remineralization balance, GCE have been proven to be able to inhibit dental biofilms. In an in vitro experiment, Cheng et al. [2010] investigated the effects of GCE at different stages of biofilms formed with saliva as inoculum. The results demonstrated that GCE treatments inhibited growth and acid metabolism of both nascent and mature microcosm biofilms. Xie et al. [2008] designed an experiment to investigate the antibiofilm effect of GCE using a 4-organism bacterial consortium (Streptococcus sanguis, Streptococcus mutans, Actinomyces naeslundii, Lactobacillus rhamnosus). A GCE was able to inhibit the growth of multiple-species biofilms on enamel blocks and then reduced the demineralization of dental enamel.
Propolis
Propolis has attracted increased interest due to its antimicrobial activity against a wide range of pathogenic microorganisms. The major constituents of propolis are Caries Res 2015;49(suppl 1):38–45 DOI: 10.1159/000377734
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ization of dental hard tissue [Chu et al., 2007; Cheng et al., 2008]. So this review is to summarize previous studies of natural products and their components on the prevention of dental caries.
Magnolia Bark
Magnolia bark is a plant part which has been widely used in medicine for 2,000 years [Watanabe et al., 1983]. The two effective components of magnolia bark extract are magnolol and honokiol which have been reported to inhibit the growth of S. mutans, Streptococcus sobrinus, Porphyromonas gingivalis, Fusobacterium nucleatum, Aggregatibacter actinomycetemcomitans, Capnocytophaga gingivalis and Veillonella dispar in vitro and to reduce the dental caries values in an animal experiment [Chang et al., 1998; Ho et al., 2001; Greenberg et al., 2007]. Magnolia bark extract has previously been added into a xylitol chewing gum. In a randomized controlled intervention trial, 30-day use of a chewing gum containing magnolia bark extract showed beneficial effects on oral health, including reduction of salivary mutans streptococci, plaque acidogenicity and bleeding on probing [Campus et al., 2011].
Tea
Tea is considered as one of the most widely consumed beverages in the world, especially in Asian countries, and tea is also reported as the major source of flavan-3-ols and flavonols in the US diet [Song and Chun, 2008]. Though tea is composed of polyphenols, the polyphenol type and 40
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levels are determined by how the tea has been processed [Astill et al., 2001]. The effective components of green tea are mainly attributed to its polyphenol contents commonly referred to as catechins, including epigallocatechin-3-gallate, epigallocatechin, epicatechin-3-gallate and epicatechin [Taylor et al., 2005]. Black tea comprises oligomers such as theaflavins and polymers known as thearubigins. Oolong tea contains considerable amounts of catechins and oligomerized catechins [Balentine et al., 1997]. Catechins and theaflavins, polyphenolic compounds derived from tea (Camellia sinensis, fam. Theaceae), have been reported to have a wide range of biological activities including prevention of tooth decay and oral cancer in several in vitro studies [Yang, 1997; Yang et al., 1999, 2000; Hamilton-Miller, 2001; Yang et al., 2002]. Green tea might be linked to a lower incidence of some pathological conditions including oral cancer, dental caries, stroke, cardiovascular diseases and obesity [Taylor et al., 2005; Chacko et al., 2010]. Various papers revealed the anticaries effects of tea extracts via in vitro and in vivo experiments. The polyphenol contents of green tea have been reported to inhibit varieties of pathogenic bacterial growth including S. mutans and S. sobrinus. Another in vitro study confirmed the inhibitory activities of green tea extracts on cariogenic and periodontopathic bacteria [Araghizadeh et al., 2013]. Application (oral rinsing) of green tea solution without sugar for a short time could strongly inhibit salivary and plaque numbers of S. mutans which are important causative bacteria of caries both initially and secondarily [Awadalla et al., 2011]. The study of Lee et al. [2004] indicated that green tea leaves and black tea can be used as a convenient, slow-release source of catechins and theaflavins to prevent dental caries. Volunteers gently chewed 2 g of green tea leaves for 5 min and thoroughly rinsed the mouth. Then high concentrations of catechins (Cmax = 131.0–2.2 μM) and theaflavins (Cmax = 1.8–0.6 μM) were observed in saliva according to a high performance liquid chromatography system analysis. Camellia extract MJ (Taiyo Kagaku), a food additive in Japan, is a green tea extract with over 1,500 ppm of fluoride. A cup of green tea was reported to contain 0.5–1 g of catechins/l [Hamilton-Miller, 2001], while Camellia extract MJ contains approximately 0.06 g of catechins/l. Suyama et al. [2011] used chewing gum containing Camellia extract MJ as the source of fluoride. An in situ experiment found it produced a superior level of remineralization and acid resistance of dental enamel [Suyama et al., 2011]. Oolong tea extract (OTE) was shown to possess a strong antiglucosyltransferase activity which originates Cheng/Li/He/Zhou
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flavonoids [Usia et al., 2002], organic acids, phenols, various kinds of enzymes, vitamins and minerals [Velikova et al., 2000]. Tunisian propolis ethanol extract was proven to have anticariogenic and antibiofilm effects in an in vitro experiment [Kouidhi et al., 2010]. The effective component of propolis could inhibit both glucosyltransferase activities and bacterial growth [Koo et al., 2002b]. Besides, the cytotoxicity of propolis was tested using gingival fibroblast cells. The results indicated that appropriate solutions can be prepared which are strongly antibacterial and noncytotoxic as well [Sonmez et al., 2005]. Furthermore, a previous study investigated the ethanolic extract of a novel type of propolis and its purified hexane fraction on mutans streptococcus biofilms and the development of dental caries in rats. The results suggested that the cariostatic properties of propolis were due to the reduction of acid production and acid tolerance of cariogenic streptococci; these biological activities may be attributed to its high content of fatty acids [Duarte et al., 2006b].
Grapes
Grapes (Vitis vinifera) [Daglia et al., 2007a; Thimothe et al., 2007] and grape seed extracts (GSE) [Sarni-Manchado et al., 1999] have been considered as effective anticaries agents. Phenolic fractions of a limited number of grape varieties, including V. vinifera and Vitis interspecific hybrid varieties, can significantly decrease the enzymatic activity of S. mutans GtfB and GtfC [Yano et al., 2012]. Proanthocyanidins in GSE are thought to be the effective components in inhibiting dental caries. Proanthocyanidins could inhibit the surface-adsorbed gluocsyltransferase and F-ATPase activities, and the acid production by S. mutans [Duarte et al., 2006a]. The capability of GSE in inhibiting the demineralization and/or promoting the remineralization of artificial root carious lesions was reported previously [Xie et al., 2008]. Hypotheses have been proposed for GSE promoting remineralization of dental caries. GSE may contribute to mineral deposition on the superficial layer of the lesion [Kosasi et al., 1989; Xie et al., 2008]. The combination of GSE with fluoride showed both significant antiplaque activities and antioxidant properties. The results indicated that the antibiofilm activity of the combination of 2,000 μg/ml of GSE with 10.2 mg/ml of Fluorinol® was greater than that of each compound tested alone [Furiga et al., 2014]. Grape phenolic extracts could be maintained in the wine and keep the ability to inhibit bacteria. Several papers investigated the antimicrobial effects of red wine. Thimothe et al. [2007] found that wine and grape phenolic extracts, as well as pomace phenolic extracts, could kill different Streptococcus spp. strains associated with dental caries. In another study, red wine and dealcoholized red Natural Products to Prevent Dental Caries
wine were tested using a biofilm model of the supragingival plaque. The results indicated that red wine and dealcoholized wine had an antimicrobial effect against F. nucleatum and Streptococcus oralis [Munoz-Gonzalez et al., 2014].
Coffee
Coffee, another popular worldwide drink, was reported to combat some diseases, including dental caries [Daglia et al., 2007b; Antonio et al., 2011, 2012]. The antibacterial ability was also due to polyphenols [Koo et al., 2002a; Yatsuda et al., 2005; Farah et al., 2006]. A recent paper has proven the antibacterial effect of Coffea canephora extract against S. mutans, and its inhibiting effects on the demineralization of tooth enamel under biofilm conditions were also observed [Antonio et al., 2011, 2012]. The action mode is considered that C. canephora caused bacterial lysis and consequently the release of calcium into the medium. One of the advantages of coffee is that it is normally consumed in a concentrated form (6– 10%), which is higher than the effective concentration reported previously (1–2%) [Meckelburg et al., 2014].
Cacao
Cacao beans, the main constituent of chocolate, contain some polyphenols which exhibit antiglucosyltransferase activity. The cariostatic activity of cacao mass extract was studied in vitro and in experimental animals [Ooshima et al., 2000a, b]. A previous study indicated that cacao mass extract possesses some anticariogenic potential, but its anticaries activity is not strong enough to significantly suppress the cariogenic activity of sucrose [Ooshima et al., 2000a]. An animal study demonstrated that the extract could become a novel anticaries substance as a mild chemoprophylactic agent [Ooshima et al., 2000b].
Hesperidin
Hesperidin, a citrus flavonoid, was able to preserve bovine dentine collagen against proteolytic degradation. It has also been reported that hesperidin reduced the susceptibility of dentine lesions to acid-dependent demineralization with the potential to promote the remineralization process [Hiraishi et al., 2011]. In another paper, hesCaries Res 2015;49(suppl 1):38–45 DOI: 10.1159/000377734
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from polymeric polyphenols in oolong tea leaves [Nakahara et al., 1993]. Furthermore, OTE has been shown to inhibit experimental dental caries in specific pathogenfree rats infected with either S. sobrinus 6715 (serotype g) or S. mutans MT8148R (serotype c) when given in both diet and drinking water [Ooshima et al., 1993]. In addition, OTE has been shown to reduce dental plaque deposition in humans [Ooshima et al., 1994]. Oolong tea polyphenols may inhibit bacterial adherence to the tooth surface by reducing the cell surface hydrophobicity of mutans streptococci, and OTE may inhibit the caries-inducing activity of mutans streptococci by reducing the rate of acid production [Matsumoto et al., 1999].
Traditional Medicine
Different countries have their folk medicine, and researchers tried to select effective agents from a great amount of traditional herbs in their countries. In Asia, Wong et al. [2010] investigated 20 traditional Chinese medicines for their antimicrobial activity against 4 common oral bacteria, including Streptococcus mitis, S. sanguis, S. mutans and P. gingivalis. The results indicated that 13 of them had an antibacterial effect on some bacteria species and fructus armeniaca mume was effective against all 4 bacteria. Rheum undulatum (Polygonaceae) is a perennial herb distributed and cultivated mainly in East Asia [Choi et al., 2005]. The dichloromethane fraction from R. undulatum, which is composed mainly of aloe emodin, emodin, chrysophanol and physcion, had inhibitory effects on the glycolytic acid production of S. mutans biofilms [Kim et al., 2011]. In another paper, ethanol extracts of 35 groups of Thai herbal formulas were tested for antibacterial activity against S. mutans. The tests found that Albizia myriophylla had the strongest activity with minimum inhibitory concentrations at 3.9 μg/ml against S. mutans [Joycharat et al., 2012]. In Laos and Vietnam, Kammu women used 3 plants (including Dracontomelon dao nuts) to stain their teeth black. The soot of D. dao nuts could effectively inhibit growth of salivary mutans streptococci in an in vitro experiment [Tayanin and Bratthall, 2006]. Phyllanthus emblica is one of the most celebrated herbs in the Indian system of traditional medicine. Emblica officinalis extract could reduce acid production, biofilm formation, cell surface hydrophobicity, glucan production, and sucrose-dependent and independent adherence of S. mutans [Hasan et al., 2012]. Different populations and cultures around the world have been using various tools, like porcupine bones or chewing sticks to clean their teeth and gums [Khoory, 1983; Eid et al., 1990]. In middle-eastern and eastern African cultures, a chewing stick called miswak is widely used to clean the teeth and gums. Darmani et al. [2006] found that aqueous extracts of miswak and derum en42
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hance the growth of fibroblasts and inhibit the growth of cariogenic bacteria, and the derum extract had greater activity than that of miswak. More et al. [2008] studied other chewing sticks made of traditional South African medicinal plants, including their antibacterial effects and cytotoxicity. The extracts of Annona senegalensis, Englerophytum magalismontanum, Dicerocarym senecioides, Euclea divinorum, Euclea natalensis and Parinari curatellifolia showed positive inhibitory activity against five microorganisms [More et al., 2008]. In all of temperate Europe and in the Himalayas, China and Japan, the stem bark of Juglandaceae (Juglans regia, walnut) is quite popular and is used as a tooth-cleaning tool. The bark of J. regia is also known to contain fluorides which have been well studied as an effective anticaries agent [Almas and al-Lafi, 1995]. One study has concluded that these chewing sticks were 20% poorer than the toothbrush in reducing plaque scores. The extracts were tested for their effect on the growth, in vitro adherence, glucan-induced aggregation and the acid-producing ability of S. mutans [Jagtap and Karkera, 2000]. In western, central and southern Mexico, Iostephane heterophylla was collected, and the compounds isolated from the roots had a significant antimicrobial activity against oral pathogens [Hernandez et al., 2012].
Conclusion
Though numerous papers focused on how to use natural products to combat dental caries, there are still some problems to be solved. Firstly, the natural products showed weaker effects in caries prevention compared with traditional chemical agents, like antimicrobials or fluoride. Secondly, the mechanisms of the effective components are still unclear for most of the natural products. So in future studies, more efforts should be made to find potential agents isolated from natural products, investigate their mechanisms and modify them to have stronger inhibiting effects on dental caries. (1) Novel natural products and effective components should be found in future investigations. In previous studies, most of the effective compounds isolated from natural products are polyphenols, which are found in plants, vegetables and flowers. It is interesting to find out some other natural products to prevent dental caries. In some traditional medicine systems, not only plants, but also animal extracts and minerals are used as medicine. Furthermore, the studies of natural products focus on two aspects: antibacterial effects and shifting the de-/reminCheng/Li/He/Zhou
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peridin was found to reduce lesion depth and mineral loss, indicating that hesperidin inhibited demineralization and probably enhanced remineralization even under fluoride-free conditions [Islam et al., 2012]. The mechanism of hesperidin may be related to its interaction with collagen and/or noncollagenous proteins, resulting in stabilizing the collagen matrix and induction of remineralization [Liu et al., 2004].
eralization balance. Besides, very few natural products like stevia were used to replace the dietary carbohydrates; so, in the future, some additional agents isolated from natural products might be able to eliminate dietary carbohydrates from the diet. (2) More cytotoxicity tests are needed. At the early stages, experiments were carried out to test the antibacterial effect of natural products on the planktonic cell. Then biofilm experiments were designed. Some researchers started to apply animal studies or in situ experiments in their investigations [Brighenti et al., 2012]. For most of the natural products, studies in vitro have indicated their antibacterial activity against cariogenic bacteria [Ho et al., 2001; Greenberg et al., 2007, 2008], but the clinical effects still remain unproven [Wallace, 2004]. Therefore, more in situ experiments are needed in the future. Though most of the natural products are claimed to have been used for a long time in traditional medicine, cytotoxicity tests are still needed if they are planned to be used in the clinic. (3) Chemical component or combined effect? In many previous papers, crude extracts of natural products were used, while some researchers tried to find out the effective component isolated from the natural products. For example, the methanolic extract from Artocarpus heterophyllus showed antibacterial activity against cariogenic bacteria. Then serial chromatographic purifications offered 2 active compounds, including 6-(3-methyl-Lbutenyl)-5,2′,4′-trihydroxy-3-isoprenyl-7-methoxyflavone and 5,7,2′,4′-tetrahydroxy-6-isoprenylflavone [Sato et al., 1996]. Another example is galla chinensis.
Several papers found that the crude extracts of galla chinensis had satisfactory effects on promoting remineralization of dental enamel. Gallic acid is one promising component isolated from galla chinensis, but the action modes were different between GCE and gallic acid. Tang et al. [2015] made a further investigation on the effect of gallic acid on the morphology and growth of hydroxyapatite crystals. Thus, it implied that the crude extract of galla chinensis might have several effective components which showed combined effects on the regulation of the de-/remineralization balance. (4) Novel technology should be helpful in enhancing the anticaries effect of natural products. He et al. [2014] synthesized nanosized calcium phosphate particles incorporating tea polyphenol and tested their potential as caries-preventive agent. Nanosized tea polyphenol-modified CaP at lower pH (5.5) significantly enhanced remineralization of dental hard tissue, to the same extent as the nanohydroxyapatite controls. Since tea polyphenol was proven to be able to inhibit bacterial growth and enzyme activities, the novel tea polyphenol-modified CaP nanoparticle, at low pH, is a potential dual-functional remineralization and antibacterial product. Nanotechnology will be a useful tool to develop the natural products in caries prevention.
Disclosure Statement The authors have no conflict of interest to declare.
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