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Year : 2016  |  Volume : 4  |  Issue : 1  |  Page : 1-6

Proanthocyanidin: A natural dentin biomodifier in adhesive dentistry

Department of Conservative Dentistry and Endodontics, Kothiwal Dental College and Research Centre, Moradabad, Uttar Pradesh, India

Date of Web Publication9-Feb-2016

Correspondence Address:
Dr. Payal Singh
Department of Conservative Dentistry and Endodontics, Kothiwal Dental College and Research Centre, Moradabad, Uttar Pradesh
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2321-4619.176013

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Proanthocyanidin (PA), a plant flavonoid, has recently been used in adhesive and restorative dentistry as a natural collagen cross-linking agent. As the long-term stability of the resin-bonded dentin is still questionable due to hydrolysis of collagen by collagenolytic enzymes, the use of collagen cross-linking agents has been proposed to enhance mechanical properties of dentin matrix and reduce biodegradation rates of collagen. Therefore, this paper discusses the chemistry and properties of PA, its role in stabilizing the bonded interface and enhancing the clinical longevity of adhesive restorations, and also considers various factors related to its incorporation in the bonding protocol.

Keywords: Cocoa seed, cross-linking, dentin biomodification, grape seed, proanthocyanidin (PA)

How to cite this article:
Nagpal R, Singh P, Singh S, Tyagi SP. Proanthocyanidin: A natural dentin biomodifier in adhesive dentistry. J Res Dent 2016;4:1-6

How to cite this URL:
Nagpal R, Singh P, Singh S, Tyagi SP. Proanthocyanidin: A natural dentin biomodifier in adhesive dentistry. J Res Dent [serial online] 2016 [cited 2021 Jan 28];4:1-6. Available from: http://www.jresdent.org/text.asp?2016/4/1/1/176013

  Introduction Top

Despite various developments in the adhesive dentistry, which have focused on the improvement of bonding agents and techniques, a very limited investigation has explored the contribution of collagen structure/stability to bond strength. The stabilization of dentin collagen with biocompatible cross-linking agents to increase mechanical properties and decrease enzymatic degradation with matrix metalloproteinase inhibitor (MMPI) may be of clinical importance to improve dentin bond strength.

Type I collagen provides tensile strength, form, and cohesiveness to various tissues such as dentin. It is present in in the form of fibrils and remains stabilized by lysyl oxidase-mediated covalent intermolecular cross-linking. Application of exogenous cross-linking agents to several connective tissues is helpful to modify the structures of collagen fibrils, and improve their degradation resistance as well as stabilization. Various synthetic cross-linkers (e.g., formaldehyde, glutaraldehyde (GD), epoxy compounds, and carbodiimide) have been used. However, every one of them has some disadvantage, such as high cytotoxicity, mismatched mechanical properties, and unsatisfied long-term stability. Genipin and proanthocyanidins (PAs), as natural cross-linking agents, overcome some of the drawbacks that are typically encountered with the synthetic cross-linking agents, and have been successfully used in the pretreatment of biological tissues to improve their mechanical properties. [1]

  Proanthocyanidins: Natural Sources Top

PAs are a class of bioflavonoids that are naturally occurring plant metabolites available in fruits, vegetables, nuts, seeds, flowers, and barks. In 1947, Jack Masquelier discovered oligomeric proanthocyanidins (OPCs) in the skin of a peanut by accident.

Plants, most notably apples, maritime pine bark, cinnamon, Aronia fruit, cocoa beans, grape seed, grape skin (procyanidins and prodelphinidins), and red wine of Vitis vinifera (the European wine grape) contain PA. However, bilberry, cranberry, black currant, green tea, black tea, and other plants also contain these flavonoids. Cocoa beans contain the highest concentrations. This bioflavanoid can also be isolated from Quercus petraea and Quercus robur heartwood (wine barrel oaks). Açaí oil, obtained from the fruit of the açaí palm (Euterpe oleracea), is rich in numerous procyanidin oligomers.

Apples contain on an average per serving about eight times the amount of PA found in wine, with some of the highest amounts found in the Red Delicious and Granny Smith varieties. Maritime pine bark extract called Pycnogenol contains 65-75% PAs (procyanidins). PA glycosides can be isolated from cocoa liquor. Cistus salviifolius also contains OPCs.

  Significance in medical field Top

PAs have gained popularity in the fields of nutrition, health, and medicine due to their physiological activities such as antioxidant, antimicrobial, and antiinflammatory properties, effects on cardiovascular diseases, antiallergic and enzyme inhibitory activities against phospholipase A2, cyclooxygenase, and lipooxygenase. PAs lack toxicity and are known to stabilize and increase the cross-linkage of type 1 collagen fibrils.

  Chemistry and General Properties Top

PA or condensed tannin is composed of condensed flavon-3-ol subunits, catechin, epicatechin, and epicatechin-3-O-gallate and linked mainly through C4-C8. A high structural diversity based on these four monomers molecules (catechin, ent-catechin, epicatechin, and ent-epicatechin), different types of interflavonoids bonds, and the various lengths of chains are unique characteristics of the agent. [1]

PA has been given particular attention because of its ability to bind to proline-rich proteins, [2] such as collagen, and facilitate the enzyme proline hydroxylase activity that is essential for collagen biosynthesis. [3] Apart from the advantages of a natural occurring cross-linking agent over a synthetic one, it shows vast biological activities with good biocompatibility and a faster reaction rate than genipin.

The combined cross-linking potential and anticollagenolytic effects of PA would be beneficial in preventing degradation of dentin collagen within the hybrid layer. Liu et al. depicted that the poorly infiltrated demineralized dentin at the bottom of the hybrid layer can be mechanically strengthened by PA biomodification and it contributed to the stabilization of the bonding interface. [4]

PA consists of highly hydroxylated structures that are capable of forming insoluble complexes with carbohydrates and proteins. [5] The mechanism of PA-induced cross-linking has been proposed including covalent, ionic, hydrogen bonding, and hydrophobic interactions. The cross-linking mechanism between PA and collagen may be primarily by the formation of hydrogen bonding between the protein amide carbonyl and the phenolic hydroxyl groups in addition to covalent and hydrophobic bonds, which are the major force for stabilizing PA-treated collagen and increasing its mechanical properties. [6]

  Significance in Dentistry Top

Durability of the bond between resin and tooth substrate is of significant importance for the clinical longevity of adhesive restorations. However, the long-term stability of the resin-bonded dentin is still questionable. [7] In vitro researches have shown that resin-dentin bonds obtained with contemporary hydrophilic dentin adhesives deteriorate over time due to hydrolysis of collagen by collagenolytic enzymes (matrix metalloproteinases and cysteine cathepsins) [8],[9],[10],[11],[12],[13],[14],[15] [Table 1]. PA has been used in the adhesive and restorative dentistry as a natural collagen cross-linking agent. PA can be readily extracted from grape seed and cocoa seed with regular and nontoxic solvents such as water, acetone, and ethanol. Grape seed extract has been reported to induce exogenous cross-links.
Table 1: Literature review of studies evaluating the role of PA in enhancing resin-dentin bond stability

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  Effect on Dentin Mechanical Properties: Role in Enhancing the Durability of Resin-Dentin Bond Top

Several studies have shown that PA functions as dentin collagen matrix stabilizer, thereby improving its mechanical properties and increasing its resistance to biodegradation. [32],[33],[34] Contact angle measurements have demonstrated that the hydrophobicity of PA-modified collagen films improved as a result of cross-linking between PA and collagen. The water vapor permeability of collagen/PA films decreased with increasing PA content due to formation of a denser structure, which in turn prevented moisture permeation. Castellan et al. also reported the ability of PA-rich (grape seed and cocoa seed) extracts to increase the short- and long-term mechanical properties of demineralized dentin and the short-term resin-dentin bond strength. [25],[35] Pretreatment of demineralized dentine with PA increased the bond strength of simplified etch-and-rinse adhesives to both sound and caries-affected dentine. Furthermore, the nanomechanical properties of bonded interfaces improved following the use of PA on etched dentin. Green et al. showed that PA released from the experimental adhesive decreased the collagenase activity by masking the cleavage site of collagen, thereby increasing the resistance of the collagen to degradation by collagenase. [23] Hence, it has been speculated that PA hydrogen bond formation in multiple sites on the collagen molecules reduces possible cleavage sites.

Castellan et al. reported that induction of an interfibrillar cross-link in the dentine collagen matrix also resulted in a decrease in its swelling ratio. This, in turn, could have resulted in decreasing collagenase sorption and reduced enzymatic degradation of the PA-treated dentine matrix. [25] Castellan et al. reported that PA pretreatment increased the immediate elastic modulus of dentin matrix and was effective even after bacterial collagenase challenge or 1-year of storage in artificial saliva. [18] Additionally, it provided enhanced immediate adhesion and long-term stabilization to demineralized dentin after 1-year of aging in water.

  Mechanism of Action Top

For PA, three mechanisms of action have been proposed for protecting collagen from degradation. First, the protease resistance may be achieved via irreversible conformational changes of proteases within the catalytic domain or allosteric inhibition of other modular domains that coparticipate in collagen biodegradation. In addition to its cross-linking effect, PA from the elm tree and cranberry extracts has also been shown to inhibit production of matrix metalloproteinases (MMPs) 1, 3, 7, 8, and 9 and it is found to be a potential inhibitor of MMP-2 and MMP-9. Epasinghe et al. demonstrated that PA could inactivate more than 90% of soluble recombinant MMP-2, -8, and -9 and approximately 70-80% of cysteine cathepsins B and K. [36] Second, PA may indirectly interfere with protease production and activation by modulating host immune responses. Third, PA increases the density of the collagen network by inducing exogenous cross-links and decreases collagenase absorption indicated by reduced swelling ratio of demineralized dentin, thereby enhancing the matrix resistance against enzymatic degradation. The advantage of inactivating proteolytic enzymes in the dentin matrix by cross-linking is a nonspecific mechanism, i.e., it cross-links all types of MMPs and cysteine cathepsins. These cross-links involve covalent bonds that are stable over time unlike the reversible electrostatic binding of chlorhexidine (CHX).

  Variations in PA Application Protocol Reported in the Literature Top

As a primer or incorporation into adhesive

There are two possible options when incorporating PA in the current adhesive systems: As an additive to the adhesives or as a primer. Green et al. evaluated that PA incorporation directly into dental adhesives increased the substantivity of PA in the hybrid layer and enhanced its collagen cross-linking effect but resulted in a less than optimum quality of the hybrid layer, presumably due to the low degree of double bond conversion caused by the radical scavenging ability of PA. [23] In addition, Hechler et al. evaluated the long-term performance of PA application both as an additive to the adhesive and as a primer in an extra bonding step. They found that after 52 weeks' exposure to collagenase digestion, the bond strength of the PA-primer group was significantly higher than that of the control, whereas no significant difference was found between the PA-adhesive group and the control group. [37] This observation strongly supports the use of PA as a primer. Clinically, biomodification with PA using an extra step in the bonding protocol is less favorable than directly adding PA into adhesive system, which is in contrast to the clinician's preference for simplification. However, this may result in a lower risk of interfering with the well-balanced monomer-solvent cocktails. It has been confirmed that the degree of conversion is not significantly affected by this additional PA biomodification step.

Epasinghe et al. stated that the incorporation of 3% PA into an experimental dental adhesive adversely affected resin-dentin bond strength. However, no significant difference in bond strength was found among the PA-free and 1% and 2% PA-containing adhesives. Two percent PA incorporated into dental adhesive provided the greatest reduction in nanoleakage at the bonded interface without compromising the 24-h resin-dentin bond strength. [24] With the incorporation of 1-2% PA into adhesive resin, PA could be trapped within the linear polymer chains after curing. However, with higher concentrations of PA, the formation of linear polymer chains could be disturbed due to the higher density of the PA molecules resulting in inadequate polymerization of the resin and formation of microvoids, thus creating weaker resin-dentine interface and higher frequency of water channels. Furthermore, due to its free radical scavenging effect, higher PA concentration could inhibit the free radical polymerization of the resin.

Application time

It has been reported in various studies that pretreating the demineralized dentin by PA-based agents for 10 min was effective in increasing the mechanical properties of dentin matrix, enhancing the resin-dentin microtensile bond strength, and decreasing the enzymatic degradation compared to the nontreated group. [25],[28] However, the application time of PA varied from 10 min to 1 h, which was not clinically practical. Liu et al. examined the changes in dentin collagen's ultimate tensile strength after being treated by PA for clinically favorable time periods (30 s, 60 s, and 120 s). Even by doing so, dentin collagen's ultimate tensile strength was not significantly improved regardless of the treatment time unless the concentration of PA was increased from 5% to 10% and 15%. However, longer treatment time (>10 min) led to significant increases in elastic modulus and ultimate tensile strength. [38] Finally, they concluded that PA could effectively cross-link collagen and improve its biological stability in time periods as short as 10 s.

  Interaction of Solvent used for PA Solution with Solvents of Adhesive Systems Top

Factors such as solvents, the extraction process of the products, pH, and temperature may influence the structure, composition as well as overall cross-linking potency of PA. The complexity of natural products, their chemical structures, and extraction mode result in the use of different solvents for each extract. The effectiveness and stability of cross-linking treatment depend both on the source/type of PA-rich extract and the adhesive system employed. Castellan et al. found that grape seed extract (GSE) showed a more predictable behavior when an ethanol-water based adhesive was applied and cocoa seed extract demonstrated enhanced results with acetone-based adhesive. [18] This was probably due to a greater affinity among solvents from adhesives and solutions.

Protein-polyphenolics complexation can be measured by the Hansen solubility parameter (dH value). Both ethanol and acetone are polar solvents miscible in water. The dH values of ethanol and acetone are lower than that of distilled water; hence, less hydrogen bonding sites would be occupied by the weaker bond-forming solvent. These additional available hydrogen bonding sites, coupled with the collagen structure, may then allow more direct hydrogen bonding between PA-collagen or collagen-collagen molecules, which induce collagen cross-linking and result in stronger mechanical properties. Therefore, it was concluded by Han et al. that the use of ethanol as the adhesive solvent also promotes PA and collagen interactions by decreasing the dielectric constant of the adhesive and enhancing the stability of hydrogen bonds. [1] Hence, it is reasonable to predict that the solvent system used in PA solution interacts differently with diverse solvents from the adhesive system.

  Effect of PA Concentration on the Degree of Conversion of Monomer Top

Yi Liu et al. examined the effect of different concentrations of PA (0%, 2.5%, 5%, and 10%) incorporated in the resin formulation, on the degree of conversion (DC) and polymerization behavior of a Bis-GMA/HEMA model adhesive with three different photoinitiators, including the camphorquinone (CQ)/amine, CQ/amine/iodonium salt, and (2, 4, 6-trimethylbenzoyl) phosphine oxide (TPO) systems. It was found that PA hampers the monomer conversion and alters the polymerization kinetics in all adhesives regardless of the photoinitiators used. However, the CQ/A/I-2 or TPO systems could maintain a satisfactory degree of conversion (>65%) while a significant amount of PA was incorporated (5%). Although addition of PA decreased the degree of conversion to some extent, it is in the range of acceptable limits within the adhesive.

  Conclusion Top

Biomodification of demineralized dentin matrix with PA inhibits the proteolytic activity effectively and stabilizes the adhesive/dentin interface against enzymatic degradation. Thus, incorporation of PA into simplified hydrophilic adhesive systems may be a means to improve the durability of adhesive restorations. However, more in vivo research is required to validate its use in clinical setting.

  References Top

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[PUBMED]  Medknow Journal  
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