Cork: Current Technological Developments and Future Perspectives

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Cork: Current Technological Developments and Future Perspectives for this Natural, Renewable, and Sustainable Material Ivo M. Aroso,*,†,‡ Ana R. Araújo,†,‡ Ricardo A. Pires,†,‡ and Rui L. Reis†,‡ †

3B’s Research Group - Biomaterials, Biodegradables and Biomimetics, University of Minho, Headquarters of the European Institute of Excellence on Tissue Engineering and Regenerative Medicine, AvePark-Parque de Ciência e Tecnologia, Zona Industrial da Gandra, 4805-017 Barco GMR, Portugal ‡ ICVS/3B’s - PT Government Associate Laboratory, Braga/Guimarães, Portugal ABSTRACT: Cork is the bark of Quercus suber L., the cork oak tree. It is currently explored for different industrial applications, of which stoppers for the wine industry is the most representative and economically important. During the processing stages, up to 30% of cork is transformed into powder, which is mainly used for energy production by the industry. This underexploited natural resource stream constitutes an opportunity for the development of new products. In this review, we discuss cork as a potential source of chemicals for alternative applications. Special emphasis is dedicated to (a) suberin, (b) the extractives fraction, and (c) the use of cork in nontraditional applications. Suberin constitutes a source of long chain hydroxyacids which can serve as building blocks for new macromolecules and materials. The structure and composition are briefly addressed, while the advances in suberin depolymerization, extraction methodologies, and the proposed applications for this material are thoroughly discussed. The extractives fraction is constituted by lipophilic and phenolic compounds that present strong antioxidant and biological activities. The extractives composition and its properties are addressed. Finally, the use of cork for recently proposed applications, such as the preparation of activated carbons and as templates for the adsorption of pollutants, are also presented. This review is intended to summarize the current knowledge and technological development state and to push for the progress toward an integrated cork economy. KEYWORDS: Cork, Suberin, Secondary metabolites, Antioxidants, Natural resources, Sustainable resources

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around 20−25 years. The first material extracted is thin, corrugated, with low suberin content, high density, and with many morphological defects. It is designated “virgin cork” and does not have sufficient quality for most of the common applications; consequently, it is only used on the production of agglomerated particle boards for nontechnical applications. The subsequent extractions are usually performed with a minimum interval of 9 years, allowing for the cork to develop the necessary thickness for the production of natural stoppers. The second extraction cork, designated “first reproduction cork”, is composed of material of higher quality than virgin cork; however, it still does not present the necessary properties for the production of wine stoppers. It is mainly used on less technically demanding applications such as agglomerated particle boards for thermal insulation, panels for sound and vibration dampening, and in some cases for agglomerated stoppers (Figure 1). Only on the third extraction does the harvested material have the necessary quality for the production of natural wine stoppers.

CORK, PRODUCTION, AND ECONOMIC IMPORTANCE The cork oak tree is a slow developing tree that grows predominantly along the Mediterranean basin. It requires a combination of hot and arid conditions and has good tolerance to extended periods of drought, making it well adapted to poor soils and desertification prone regions.1,2 The existing cork forests under commercial exploitation are managed by direct human intervention; however, they constitute a unique and diversified ecosystem of fauna and flora where a large number of animals and plants coexist.3,4 This ecosystem receives praises from a number of international environment organizations, such as the World Wildlife Fund (WWF).5,6 Cork oak forests occupy an estimated 2.1 million hectares worldwide, which translates to an annual production of 201 ktons of cork.7 Portugal accounts for 55% of the world production, with 90% for export. Cork stoppers are the most important product and constitute 70% of the revenue generated for the industry.7,8 The harvesting of cork is performed periodically through a manual and labor intensive process, without severe damage to the tree, after which it naturally regrows. The first extraction occurs when the tree reaches 25 cm in diameter, which happens at © 2017 American Chemical Society

Received: March 10, 2017 Revised: August 15, 2017 Published: September 27, 2017 11130

DOI: 10.1021/acssuschemeng.7b00751 ACS Sustainable Chem. Eng. 2017, 5, 11130−11146

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ACS Sustainable Chemistry & Engineering

composition accounts for 30−50% suberin, 15−30% lignin, 6−25% polysaccharides, and 8−20% extractives.24,25 The industrial exploitation of natural origin materials or chemicals is often hampered by the absence of a logistic chain that guarantees raw material sourcing in sufficient volumes, its year-round availability, cost of transportation, storage, decomposition, and preservation. Cork is already industrially produced and transformed; thus, these requirements are satisfied. Moreover, if the newly developed products, chemicals, or materials are obtained from existing, currently unused, or subused material streams, it will positively impact the business economy of raw material production and processing industries.

Figure 1. Quercus suber tree after debarking, cork products, and alternative routes for the valorization of residues.

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SUBERIN The presence of suberin is ubiquitous across the vegetable kingdom, and it can be found with different extents on barks, roots, and peels of some tubers. It constitutes a protective barrier and participates in the wound healing process of external tissues. Suberin presents an aliphatic-aromatic macrostructure with a highly variable composition between plant species and even from different structures from the same plant. Therefore, the term suberin is loosely used to define such structures.26 Moreover, despite the monomeric qualitative composition of the extracted material being usually well characterized, because the limits of the true suberin macrostructure are not well defined, its quantification is difficult and depends on the extraction methods employed. Also, the macrostructure arrangement and its interconnection with the remaining cell wall structural elements are still poorly understood. The suberin in cork constitutes one of the few natural, sustainable, and direct sources of α-hydroxyfatty acids, α,ω-dicarboxilyc acids, and homologous midchain dihydroxy or epoxy derivatives in sufficient amounts to justify commercial exploitation.25,27 Due to the high content of suberin in cork, it is expected that less raw material processing would be required when compared to other potential sources which will impact favorably the economics of the extraction process. In this section, we summarily review the physical structure and chemical composition of suberin and focus on the most recent progresses in suberin depolymerization and its applications.

These are constituted of one single piece of cork and are obtained from the best quality cork, also constituting the highest revenue item. Therefore, there is a span from 40 to 45 years between the seeding and the cork stopper.1,2,9 The macroscopic cellular structure of cork is well known and recognizable; however, its microscopic structure is still poorly understood. After growth, the cork cells lose their cytoplasm content and become void. It is accepted that the cell wall is a complex structure, constituted by the primary wall, mainly composed of cellulose, the secondary wall, assembled from lamellar depositions of suberin and also lignin to some extent, and the tertiary wall, which is constituted of polysaccharides.2,10−13 The resulting structure is constituted by an arrangement of hollow cells. The cross section of the radial direction (surface perpendicular to the bark growth direction) resembles that of a honeycomb with cells with 4 to 8 sides.

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PHYSICAL STRUCTURE AND CHEMICAL COMPOSITION The chemical composition of cork suberin has been proposed to be constituted of a polyester structure of long chain fatty acids, hydroxy fatty and phenolic acids, linked by ester groups, and cross linked by glycerol units.26,28,29 The aliphatic domain is bridged to the aromatic one by hydroxycinnamates, mainly ferulic acid derivatives, feruloylamides, and caffeates.26,30 However, the true limit of the suberin aromatic domain, and whether it is part of the suberin structure, is still a matter of debate between researchers.26,28,31 Nevertheless, the consensus among most researchers is to consider suberin as the fraction obtained after cleavage of the ester cross links present in cork. Based on this view, Graça26 has proposed that the term suberin should be reserved for the aliphatic polyester fraction structure, thus classifying suberin as a poly(acylglycerol) macromolecule.26 Through the years, several methodologies have been employed to study the chemical composition of suberin. Due to its tridimensional and insoluble nature, most methods are based on the depolymerization of the macrostructure through chemical treatment, i.e., hydrolysis of the ester linkages. The process

Figure 2. Piece of cork after extraction and cork cellular structure: cross section on radial (A) and axial (B) directions (scale bar: 50 μm).

The cross sections of the tangential and axial directions are morphological equivalents, and the structure is similar to brick wall (Figure 2).8,14 Cork comprises a remarkable set of properties that are unique within naturally occurring materials. These stem from its peculiar morphological arrangement and chemical composition and are the reason for the numerous applications where cork has been successfully used.15 It presents near-zero Poisson coefficient, complete recovery of shape after compression, low density, high thermal and acoustic insulation, damping properties, imperviousness to liquids, and resistance to most solvents including mild acidic and basic solutions.16−22 Its chemical composition is highly variable and is affected by different factors, such as geographical origin, climate, or age of the trees.23 The typical 11131


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presence of such a fraction in cork suberin or have completely excluded it. These suberan-like compounds are not considered in the currently proposed models of suberin.50,51 Therefore, these are most certainly incomplete and do not represent the cork suberin molecule on its entirety. The depolymerized suberin is usually comprised of linear long chain hydrocarbons, possessing from 16 to 26 carbons (with particular relevance to species with 18 and 22) and include α-acids, α,ω-diacids, and ω-hydroxyacids with or without extra functionalization at midchain by unsaturation, vicinal dihydroxy, and epoxy groups.25,26,52 Glycerol can amount up to 40% of the molar content, reflecting the importance of this component on the overall structure.28,29,53 By mass, the most abundant monomers are the 9-epoxyoctadecanodioic, 22-hydroxydocosanoic, 9,10-dihydroxyoctadecanodioic, and 9-epoxy-18-hydroxyoctadecanoic acids.25,26 The structures of the most relevant suberin monomers are summarized in Table 1.

results in the release and dissolution of the constitutive monomers, which are then identified and quantified by gas chromatography coupled with mass spectrometry (GC-MS) detection, usually after derivatization.32−38 The in situ characterization of suberin, using attenuated total reflectance infrared spectroscopy (ATR-FTIR) and solid state carbon-13 nuclear magnetic resonance (13C NMR), has also been performed.39−42 However, due to the complexity of the molecule and limitations of these techniques, the insight into its structural organization is limited. The depolymerization followed by GC-MS analysis is by far the most used technique for qualitative analysis of suberin, as demonstrated by the large number of reports comprising the use of this technique.25,26 The depolymerization with sodium methoxide in methanol under reflux conditions has been the most used methodology. It produces an extensive cleavage of the suberin molecule, with the release and dissolution of the monomers, mainly as methyl esters.33,36,38,43 The monomers and small mass fragments (mainly dimers and trimers) have been used to determine the suberin’s chemical composition, as wells as the local organization of the different components and the overall macromolecular structure of suberin. Other depolymerization methods have been also employed. These include alkaline hydrolysis (NaOH and KOH) with other alcohols44 containing variable water percentages,25,45 hydrogenolysis with LiBH4,46 permanganate oxidation,32 ionic liquids,47 and even enzymatic degradation.48 The depolymerization process results in the release of fatty acids, methyl esters of fatty acids and fatty alcohols, glycerol, and ferulic acid derivatives. However, irrespective of the method, the depolymerization is always incomplete, resulting in mixtures of monomers, dimers, and other small mass fragments in combination with oligomeric fragments (Figure 3). Consequently, the

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DEPOLYMERIZATION METHODS Cork suberin presents a complex molecular architecture and is intricately connected to other structural components. It is insoluble in most common solvents, requiring prior chemical cleavage whether for analysis, extraction, or conversion. Therefore, any attempt to valorize suberin will require the development of suitable depolymerization processes for its conversion to a usable format. However, until recently, the exploitation of suberin for practical applications was scarcely reported, and the depolymerization processes relied mostly on suberin obtained through the same procedures as for characterization studies. In the past few years, this paradigm appears to be changing with an increasing number of potential applications for suberin being reported in the literature. Moreover, it is also accompanied by a renewed interest in the depolymerization process, including optimization of the traditional ones or through the development of new methods. As stated before, the depolymerization of suberin is usually achieved by chemical cleavage of the ester cross links, and the newly proposed methods also follow this strategy. The approach seems to be to rely on technologies that have been proven for the conversion of other biomass feedstocks and to adapt them to the specificities of suberin and cork. The ideal depolymerization technology would be one that produces high yields of depolymerized suberin with the desired physical and chemical properties for the envisaged application. To facilitate the industrial implementation, it should also (i) comprise the minimum number of steps as possible, (ii) avoid the use of harsh chemicals and or conditions, and (iii) ideally use well established operations in the chemical industry for scalability simplicity. In this section, we discuss the technologies that have been used to obtain suberin monomers and that, in our opinion, have the potential to answer the challenge of yielding suberin and suberin subproducts for further use (summarized in Table 2). Namely, the working conditions of the proposed methods and its limitations and advantages are reviewed, while the yield and physical and chemical properties of the depolymerized products are also discussed. Traditionally, the depolymerization methods of election have been alkaline hydrolysis and alcoholysis, with particular emphasis on the later one. Several authors have reported the use of different homogeneous catalyzed-based reactive systems, such as NaOH or sodium methoxide in methanol or water, under different conditions.34,54−58 Coquet et al.59 have performed a

Figure 3. Typical gel permeation chromatogram (GPC) for suberin obtained after alkaline depolymerization; average MW = 6306 g/mol (unpublished results).

quantification of suberin and the relative abundance of its monomers can fluctuate significantly across different studies. Despite this, the qualitative composition is not significantly altered, implying that only the extension of the depolymerization is affected but not the selectivity. The percentage of detectable oligomeric structures is higher when mild depolymerization processes are used and decreasing with harsher conditions. However, even after such procedures are employed, a significant fraction of the suberin mass is still not detected by GC-MS due to its high molecular mass and low volatility.25,38 Gandini et al.25 have speculated that this fraction is actually composed by structure analogues to suberan, a nonhydrolyzable highly aliphatic macromolecule, found in the periderm of some Angiosperm species.25,49 But to date, no other authors have reported on the 11132


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ACS Sustainable Chemistry & Engineering Table 1. Structures of Most Common Suberin Monomers

Table 2. Summary of Suberin Depolymerization Methods, Conditions, and Major Product Properties To Obtain High Yieldsa Method

Depolymerization conditions

Chemical dep. with acid/base catalyst

Methanolysis or hydrolysis; From room T to reflux with NaOH and H2SO4 200 °C and 40 bar of H2; Pd/C and Rh/C catalysts

Chemical dep. with metal catalysts Oxypropylation Liquefaction Pyrolysis Ionic Liquids

Product properties

Variable yield and chemical composition; Limited selectivity 11.5% Ph/C and 7.2% for Pd/C of cork dry weight Cork powder + PO + KOH at 145 °C for 1 h Complete cork liquefaction; (240 °C during reaction) Mixture of all components Cork powder + Gly and NaOH; Gly + PEG400 at 200 °C Selective for suberin with the use of NaOH for 3h 800−900 °C Aliphatic bio-oil from cork liquefaction Cholinium alkanoates 100 °C and variable time Selective for suberin; Mainly oligomers

Refs 34, 54−59 60 68 64−66 87 47, 80−82, 84

a

NaOH: sodium hydroxide; H2SO4: sulfuric acid; KOH: potassium oxide; Pd/C: palladium in carbon support catalyst; Rh/C: ruthenium in carbon support catalyst; PO: propylene oxide; Gly: glycerol; PEG400: polyethylene glycol.

However, these homogeneous catalyzed methods require the neutralization of reactants and the separation of solids; the recovery of suberin is performed through solvent extraction with organic solvents. All of these steps add complexity, decrease the economic value, and put in question the environmental credentials of suberin. In this sense, Garrett et al.60 have proposed the heterogeneous catalytic hydrogenolysis of several tree barks (including cork) with palladium (Pd/C) and ruthenium (Rh/C) in carbon support catalysts. The process was carried out at 200 °C and 40 bar of hydrogen pressure for 4 h resulting in the formation of a suberin-like liquid that can be filtered out. Despite the total depolymerization of cork only reaching 11.5% (Rh/C) and

comparative evaluation of these different methods and reaction conditions, namely, by comparing acidic and basic methanolysis, acidic hydrolysis, and basic hydrolysis with water and ethanol. They found that, in general, as described in previous studies, the alkaline conditions produce higher yields. However, they also found that the processes conducted at room temperature produced only marginally lower yields than when carried at reflux temperature, 22% of total cork weight in opposition to 25%. The chemical composition was also different with higher yields of dihydroxy and trihydroxy acids and lower on ω-hydroxy fatty acids. Therefore, the use of optimized methodologies for suberin depolymerization can provide a basis to obtain specific monomers or enriched mixtures for future valorization. 11133


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makes them excellent choices to process natural origin polymers, such as cellulose, lignin, and suberin (all insoluble in common solvents without prior extensive chemical cleavage).71,72 The number of all possible ILs has been estimated to be a staggering 1018, and its properties are easily tuned based on the components combination, justifying its classification of “designer solvents”.73−75 However, the development of processes for the processing of natural polymers has been hampered by its high cost and high toxicity.76,77 With the introduction of biocompatible and biodegradable ILs based on cheap, readily available, and in some cases naturally occurring molecules derived from biomass, the present situation can change.78,79 Following this view, the extraction of cork suberin with ILs based on the cations cholinium and 1-ethyl-3-methylimidazolium combined with different alkanoate anions (hexanoate, octanoate, and decanoate) has been explored.80−83 The best results were obtained with cholinium-based ILs, which were able to solubilize the suberinic fraction of cork, while the polysaccharide and lignin domains remained insoluble.80,81 The extracted material was mainly composed by oligomers and polymeric fragments of suberin composed by the ester cross-linked monomers.81,84 However, the challenge of recovering the suberin fraction from the mixture and the effective and economically feasible regeneration of the IL was not addressed and will constitute a major hurdle for the process. Nevertheless, this methodology comprises a simple and direct procedure to solubilize and to separate suberin from the solid cork material. Attending to the tunability of the ILs’ properties, it is expected that further refinement of this strategy will result in higher extension of the ester cleavage and even to the selective extraction of suberin monomers. Pyrolysis constitutes yet another alternative route for conversion of biomass to chemicals. This technology is based on the thermal degradation, in absence of oxygen, of complex molecules into a pyrolytic liquid, the bio-oil. It has been extensively researched for the conversion of different biomass feed stocks, such as agricultural wastes (e.g., straw, olive pits, nut shells) and forestry wastes, such as bark and wood leftovers.85 The bio-oils properties are derived from the feedstock materials and processing conditions and are typically constituted by complex mixtures with hundreds of different compounds.85,86 Exploring this route, Marques et al.87 tested the pyrolysis of cork material producing different bio-oil products. They found that the composition is severely influenced by process temperature. At 500−650 °C, the cork bio-oil presents a composition similar to that of wood bio-oil, with high composition on aromatic lignin-like compounds. On the other hand, at higher temperature (800 to 900 °C), a cork-specific aliphatic-rich hydrophobic biooil is produced, which is associated with higher depolymerization of suberin. The cork bio-oil is mainly composed of simple molecules (alkenes, alkadienes, and alkanes) with lower molecular weight than is observed for other depolymerization methods. Therefore, the cork bio-oil shows prospect to be explored as basis for biofuel production or raw material for the synthesis of olefins. In this section, we discussed several methods that have been developed to depolymerize the cork’s suberin, under the prospect of valorization of the cork subproducts. The final product is usually a complex mixture of the numerous constitutive monomers and often includes variable percentages of oligomers and higher molecular weight structures of cross-linked material. Due to the structure of the suberin molecule, it is expected that the depolymerization products will always be complex mixtures requiring additional processing steps for refinement and or purification. However, due to the chemical similarity between the

7.2% (Pd/C) per dry weight of cork, the study is presented by the authors as a proof of concept for the catalytic depolymerization of suberin using heterogeneous catalysts. This process presents the advantage of producing a suberin-based extract while avoiding the neutralization and separation steps that are necessary when homogeneous catalysis with acids or bases is used. The liquefaction of cork is an alternative process to the traditional chemical depolymerization through methanolysis or hydrolysis that seems to have gained recent interest. The liquefaction of biomass offers the prospect of its rapid and efficient conversion to hydroxylated products and liquid polyols. When the reactive medium is integrated on the final product, the conversion process can be performed in one step, reducing the production of residues and increasing the economic and environmental interest of the process.61−63 In particular, the liquefaction of cork on polyhydric alcohols has been recently suggested.64−66 Yona et al.65 have proposed the liquefaction of cork in glycerol and glycerol/polyethylene glycol (PEG400) mixtures. The process is catalyzed by H2SO4 or NaOH and proceeds at fairly moderate temperatures (150 to 200 °C) for this methodology. The acid-catalyzed liquefaction in glycerol resulted in the liquefaction of the lignocellulosic fraction (lignin and cellulose fractions). However, when PEG400 is added, an increasing amount of suberin is also liquefied, with up to 95% of the cork mass being liquefied for the glycerol/PEG400 50:50, 200 °C, and 3 h process. On the other hand, when NaOH is used, irrespective of the process conditions or solvent mixture, only the suberin fraction is obtained. Soares et al.64 only evaluated the acid-catalyzed process and reached the same level of conversion (95%) after 60 min of liquefaction time, at 150 °C, and in the presence of 4% of H2SO4. Margarida et al.66 have used ultrasound irradiation to increase the rate of the liquefaction process. The reaction was carried out on a mixture containing 10% w/w of cork powder in 1:2 (% w/w) of 2-ethylhexanol and diethylene glycol containing 3% of p-toluene sulfonic acid. High frequency sound waves (24 kHz) with amplitudes from 60% to 100% at 400 W were applied for 3 min at the start of the reaction. The accelerated process could achieve 90% conversion in less than 3 min, while the nonaccelerated only achieved the same level of conversion after 60 min. The oxypropylation refers to a particular liquefaction methodology where a solid material is converted into a liquid polyol by means of grafting of OH groups with propylene oxide (PO). This process has been successfully applied to different natural materials, including cork.67 The oxypropylation of cork was proposed by Evtiouguina et al.,68 who submitted a mixture of cork powder and PO to high temperatures (up to 250 °C) and pressure (15 atm) in the presence of KOH. The product is a liquid polyol of significant viscosity at room temperature, composed by a mixture of all cork components and some polymerized PO. The works here described demonstrate that the liquefaction process can be applied to convert the cork solid material to a more workable liquid polyol in one step. With particular conditions, it is possible to adapt the methodology to present selectivity and yield a suberin fraction of tunable properties through the simple selection of solvent/reactant and/or reaction conditions. On trade-off, the polyols produced are complex mixtures containing a large percentage of oligomeric structures, which can be a hurdle for the development of industrial applications. The use of ionic liquids (ILs) for the processing of biomass is a somewhat recent proposition but has shown great promise.69,70 ILs present exceptional solvent properties and versatility, which 11134


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The typical physical aspect of depolymerized suberin (from alkaline depolymerization) and a rigid polyurethane membrane after cross linking with hexamethylene diisocyanete are shown in Figure 4.

different monomeric structures, the development of an effective separation process will be technically challenging and economically questionable. Therefore, the suberin valorization route should be concentrated on the development of technical solutions where the depolymerized suberin can be used whole, avoiding further processing steps.

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APPLICATIONS FOR DEPOLYMERIZED SUBERIN Despite the extensive literature on the physical structure and chemical composition of suberin, the reports on the development of applications for this material or based on its components are far scarcer. Nevertheless, the use of depolymerized suberin and its monomers for different applications has been the focus of some studies that were reported in the past few years (Table 3).

Figure 4. Depolymerized suberin as polyol raw material to prepare rigid polyurethane materials: physical aspect of (A) depolymerized suberin and (B) rigid polyurethane membrane after polymerization with hexamethylene diisocyanate (unpublished results).

Table 3. Summary of Potential Applications Proposed for Molecules and/or Materials Derived from Cork Molecules sourced from cork From suberin Ink additives Polyurethane materials: prepolymers and rigid materials Polyester materials: prepolymers and rigid films Polymer grafting additivies Additives for cosmetic products From extractives fraction Bioactive molecules UV protection agents Polymer antioxidant additives Cork or cork modified materials

A similar approach was followed by Evtigouguina et al.89 who have explored the used of the oxypropylated cork polyol to obtain polyurethane materials (in reaction with aliphatic and aromatic mono- and di-isocyanates). The reaction was performed in dichloromethane and the products recovered after separation with solvents. The reaction kinetics and products were similar to what was observed for depolymerized suberin obtained using alkaline methanolysis. However, in both cases, the authors have focused on understanding the type of reaction and product formation, failing to further develop practical applications for these polymers. Recently, the preparation of rigid polyurethane foams (PUFs) has been proposed by Gama et al.96 The authors have relied on the liquefied cork extract obtained by acid-catalyzed liquefaction process performed on a Glycerol/PEG400 1:9 mixture as starting materials.64 The produced foams were rigid and presented suitable properties to be applied as thermal insulators (low thermal conductivity). The properties of these foams are strongly influenced by the properties of the starting materials (which can be optimized through modification of the liquefaction process conditions), the reaction, and foaming process conditions. Therefore, it is a versatile process that allows the fine-tuning of the PUF formulations and properties for specific applications. Following or perhaps inspired by the polyester nature of the suberin molecule, several studies have focused on the exploitation of suberin monomers to prepare polyester polymeric materials. However, despite previous reports with suberin from different sources, the use of cork suberin with this purpose has only recently received interest.25,93,94 Sousa et al.93,94 reported the preparation of several novel biopolyesters from suberin. By using suberin monomer mixtures of tailored composition, they were able to obtain linear and cross-linked polymers. However, to achieve the desired reactive group balance, synthetic comonomers bearing hydroxyl and carboxyl groups were added. On a subsequent work, the authors have also reported the polycondensation of long-chain suberin model comonomers under different catalyzing systems. Namely, using bismuth(III) trifluoromethanesulfonate, p-dodecylbenzenesulfonic acid, and enzymatic catalysis with lipase B from Candida antartica, linear polyesters of up to 7300 Da were obtained. These results consist of the first systematic report on the use of cork suberin monomers as starting materials for the preparation of polyester materials. Garcia et al.84 developed a method to obtain a suberin-based film, from the reconstitution of ILs depolymerized suberin

Biosorbents for oil spillages Biosorbents for heavy metals Activated carbons

It includes the use of suberin monomers as offset ink additives,88 as starting macromonomers for the preparation of polyurethane prepolymers,57,89−91 rigid polyurethane materials,92 polyester prepolymers,93,94 rigid polyester films,84 grafting agent for composite materials,44 and as an ingredient for cosmetic products.95 In this section, we discuss the most relevant studies that report promising applications for suberin. The performance of depolymerized suberin as an additive to waterless and vegetable-oil printing ink was proposed and evaluated by Cordeiro et al.88 The suberin material was obtained by alkaline depolymerization in methanol and included in the ink formulation up to 10% w/w. The authors measured the impact in the ink properties and determined that, with the exception of reduction in viscosity, no other significant alteration was observable. Despite the conclusion that the suberin material could be used as additive in the ink, no further developments have been reported and, to the best of our knowledge, there is no commercial use regarding this application. The first truly consolidated effort to use depolymerized suberin as starting macromonomers in polymeric materials synthesis was reported by Cordeiro et al.57,91 in the mid-1990s. Namely, suberin monomers, obtained through the alkaline (NaOH) methanolysis and after chloroform extraction, were used on the preparation of polyurethane materials via polycondensation reactions. The reactions were carried out with different isocyanates producing a solid material comprised of linear, branched, and cross-linked structures. However, the presence of low molecular weight and noncross-linked fractions that are easily extracted with organic solvents was still observed. 11135


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ACS Sustainable Chemistry & Engineering monomers and oligomers. The distinctive characteristic of this process is that it proceeds through self-association without chemical additives or previous purification. This has only been observed for IL extracts and is attributed to the macrostructure being preserved and the catalytic effect exerted by the solvent. Following this procedure, the authors were able to prepare solid suberin films which mimic the original hydrophobicity with antimicrobial properties. From its simplicity and absence of harsh reaction conditions or use of toxic chemicals, this method opens interesting possibilities to develop films, membranes, and coatings based on natural polyesters, which can find a broad range of applications. The production of cork composite materials is currently one of the hot topics in cork research with several reports and applications being presented recently. The common strategy is to combine the polymeric material (containing additives and compatibilizing agents) directly with cork granules. However, Fernandes et al.44 followed a somewhat different approach: they proposed the use of depolymerized cork suberin (obtained from alkaline alcoholysis in ethanol) as a compatibilizing agent for composites. The depolymerized suberin was grafted to high density polyethylene (HDPE) during the reactive extrusion and combined with the cork particles to prepare the composites in one step. The suberin acted as a plasticizing agent, improving the cork particle dispersion, reducing the composite stiffness, and increasing its flexibility. The composites present higher mechanical properties, dimensional stability, and thermal resistance than the nonfunctionalized material. These effects are attributed to the compatibilizing effect of suberin between the functionalized polymer and the surface of the cork particles.

Some of the chemicals extracted and purified from plant materials, such as alkaloids, anthocyanins, flavonoids, quinones, lignans, steroids, and terpenoids have found commercial application as drugs, dyes, flavors, fragrances, and insecticides, among others.106,107 The cork extractives are no exception. The extractives fraction has been the focus of several studies, which helped to clarify its composition; however, the presence of new molecules has been recently reported.108,109 It comprises very distinct molecules, such as phenols and polyphenols, triterpenes, sterols, fatty acids, and linear chain alcohols. These are mainly classified as secondary metabolites but some are also regarded as precursors or intermediaries of other components.110 Most of the earlier studies focused on the extractives obtained with aqueous or polar solvents, probably due to the interest in the molecules that can migrate from stoppers to the wine.111 The molecules that compose the cork’s extractives fraction are usually obtained through simple solvent extraction, with the properties of the extracting solvent largely influencing the nature of the extract obtained. In this context, dichloromethane, chloroform and hexane have been the solvents of choice to obtain the lipophilic components, while the more polar components are usually obtained with methanol, ethanol, water, and its mixtures.98,112−114 The use of supercritical carbon dioxide has also been reported;115−117 these extracts are usually obtained as complex mixtures, still comprising many compounds. Therefore, the qualitative and quantitative analytical methods of choice are based on chromatographic techniques, such as GC-MS59,108,113,116,118 and HPLC-MS.119−121 The cork extractable fraction is typically divided in two main subgroups: (i) waxes (aliphatic and triterpenic compounds), obtained using nonpolar or low polarity solvents, such as dichloromethane, chloroform, and supercritical fluids and (ii) phenolic compounds typically obtained with polar solvents, such as water, methanol and ethanol.

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CORK EXTRACTIVES FRACTION The cork extractives fraction is composed by low molecular weight molecules that are not covalently bonded to (or have weak interaction with) the cell wall structural elements (i.e., suberin, lignin, and cellulose). This fraction can account for up to 24% w/w of the cork total mass; however, values of around 15% w/w are more commonly found.97 The quantity and quality of the extractives fraction is dependent on the geographical origin, climate, soil, genetic origin, the age of the tree, or even the different tree part from which the cork was obtained.97,98 The presence of these unbounded low molecular weight molecules is ubiquitous to all plants. They do not participate in the primary plant functions (growth, photosynthesis, and reproduction) and are commonly classified as secondary metabolites.99 These secondary metabolites are evolutionary markers and an adaptive characteristic of plants; they have functions related to defense against pathogens, signaling pathways, protection against ultraviolet radiation, and oxidative stress, among others. These secondary metabolites have diverse structures and present different properties, such as antioxidant, antimutagenic, anticarcinogenic, anti-inflammatory, and antimicrobial effects.100 These properties are beneficial for plants since they help to prevent diseases and to protect plants from toxic compounds, bacteria, and fungi, and to maintain the stability of the genome.101−103 Therefore, these molecules constitute prime candidates to transfer these functions to new systems and are inspirations for new molecular structures for further modification toward increased activity. The potential impacts of these molecules on human health have long been recognized, and plant metabolites have received renewed interest in the past few years, namely, for therapeutic and biotechnological applications and for food and pharmaceutical uses.104,105

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WAXES The term waxes describes the primary cuticle of vascular plants. They comprise a diverse mixture of aliphatic, triterpenoids, flavonoids, and/or phenolic lipids. Moreover, waxes contribute to the barrier function by reducing the loss of water and also reducing the absorption of chemicals (including pollutants and agrochemicals) through the aerial surface of plants.122 In cork, the waxes are found in the secondary cell wall in close association with suberin, constituting the wax lamella.123 This fraction is mainly composed by triterpenes and n-alkanes (from 16 to 34 carbons), n-alkanols (from 20 to 26 carbons), and fatty acids similar to those constituting suberin.59,108,124−127 A comparison between the triterpene composition and sterols obtained with different extracting techniques is presented in Table 4. The differences reflect not only the natural variability but also the use of different analytical techniques, making direct comparisons very difficult. The triterpenic fraction is mainly constituted by friedelin, cerin, betulin, betulinic acid, smaller amounts of sterols, and a minor fraction of other friedelane and lupane type components (Figure 5).45,97,98,127 Cork is the main natural source of friedelin and friedelanol, from which several derivatives (e.g., 2αhydroxyfriedelan-3-one, 2,3-secofriedelan-2-al-3-oic acid, 2α,3β-dihydroxy-friedelane, 3,4-secofriedelan-4-oxo-3-oic acid, among others) have been synthesized.128−130 Important bioactive properties have been attributed to different triterpenic molecules, including the capacity to inhibit the growth of several types of cancer, such as breast, renal, lung, 11136


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Table 4. Comparative Composition of Main Triterpenes and Sterols Extracted under Different Procedure Conditionsa,b Extracting solvent

Chloroform

DCM

Supercritical CO2

Reference

Coquet et al.58

Castola et al.116

Dichloromethane (DCM) Touati et al.*,107

Sousa et al.112

Touati et al.**,107

Castola et al.116

19.5 − 7.81 6.52 − − − 6.5

12.6 − − 1.62 4.38 − 1.74 6.0

2.50 1.26 − 0.26 1.30 0.30 − 5.6

2.31 4.63 − 0.32 2.19 0.59 − 3.6

4.70 7.28 − 1.65 2.80 0.51 − 5.6

12.2 − − 0.84 1.26 1.74 9.0 7.0

Compound Friedelin Cerin Friedelanol Betulin Betulinic acid β-Sitosterol Sitost-4-en-3-one Total extract yield (%) ***

a The yields are presented in mg of mass of compound per kg of cork dry weight. bThe extract composition was determined before (∗) and after (∗∗) alkaline hydrolysis; (∗∗∗): total extract yield in mass of fraction per mass of dry cork.

Figure 5. Structure of several triterpenes and one sterol (β-sitosterol) identified in cork lipophilic extracts.

central nervous system, and melanoma.120,131−134 For example, pentacyclic lupane-type triterpenes plant extracts demonstrate cytostatic activity on various in vitro cancer model systems.135 Fujiokta et al. have reported on the inhibitory effect betulinic acid in HIV-1 replication.136 Betulinic acid and betulin were also found to have antimalarial, antimicrobial, and spasmogenic activities.137 However, despite the presence of several triterpene molecules in cork, to the best of our knowledge, these are not being currently commercially explored, and other cork triterpenes have not yet been sufficiently studied. Saturated and unsaturated fatty acids are the second major group of lipophilic compounds. The most abundant are the docosanoic and hexadecanoic acids and the C18-acids, 9-octadecenoic, 9,12-octadecadienoic, and octadecanoic acids. A number of aliphatic alcohols in free and esterified form (e.g., docosan-1-ol and tetracosan-1-ol) and some aromatic compounds (vanillic and ferulic acids) have also been identified within the extracts of nonpolar solvents. Docosanol is currently used in cosmetic industry as a emulsifier,138 and in 2000, it was approved by the U.S. Food and Drug Administration as a

pharmaceutical antiviral agent for herpes under the commercial name Abreva.139 Ferulic acid is used as a precursor in the manufacturing of vanillin, a synthetic flavoring agent often used in place of natural vanilla extract140 or a stabilizer of vitamins C and E in skin photoprotection cosmetic products.141 However, due to their limited availability, it is doubtful that cork will constitute a viable economic source.

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PHENOLIC COMPOUNDS The cork extractive fractions are also rich in phenolic and polyphenolic compounds with very diverse structures (the structures of the most common are shown in Figure 6). These are usually obtained through extractions with polar solvents. Tannins or plant polyphenols can be monomeric or polymeric and can be classified into condensed tannins (or proanthocyanidins) and hydrolyzable tannins. While the central structure units of condensed tannins are flavan-3-ol units, linked together through carbon−carbon bond,142 hydrolyzable tannins comprise the ellagitannins and gallotannins (glucose and gallic acid).143−145 Proanthocyanidins are the most widely studied polyphenols 11137


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Figure 6. Structure of some of phenolic and polyphenolic compounds identified in cork’s extractive fraction.

since they are the most common flavonoids present in the human diet.146 Other phenolic compounds or extracts that have received particular interest are green tea extracts (epigallocatechin gallate, EGCG), curcumin, resveratrol, isoflavones, black raspberry powder (anthocyanins and ellagitannins), bilberry extract (anthocyanins), ginger extracts (gingerol derivatives), and pomegranate extracts (ellagitannins and ellagic acid).147−149 Despite the huge progress in conventional chemistry and pharmacology in producing effective drugs, the practical result about the use of phenolic compounds in human health is still under debate.150 Some of these compounds or similar structures can be found in the phenolic fraction of cork. Several studies have shown that ellagic acid is the predominant phenolic compound, followed by gallic and protocatechuic acids and the ellagitannins vescalagin and castalagin.119−121,151,152 The phenolic extracts, its fractions, or compounds have been directly associated with antitumoral,153,154 antibacterial,84 insecticide,130,155 UV radiation protection,120 and antioxidant120,156,157 effects. In particular, several recent studies have focused on specific potential applications for this fraction. Santos et al.152 performed an in-depth characterization of the cork phenolic fraction using multistage HPLC-MS and have identified five previously unknown molecules: methyl gallate, brevifolin carboxylic acid, caffeic acid isoprenyl ester, isorhamnetin-rhamnoside, and isorhamnetin. They also characterized its antioxidant potential and determined to be higher than that of commonly used antioxidants, such as butylated hydroxytoluene (BHT). Fernandes et al.121 also reported significant antioxidant activity of cork phenolic extracts, while detecting inhibition of the proliferation of human breast cancer cell line (ER+) MACF-7 and of the colon cancer cell lines Caco-2 and HT-29. Araújo et al.120 showed in an in vitro study that the presence of the cork phenolic extracts significantly decreases the DNA fragmentation and cell death after exposure to UV radiation, therefore exerting protective action. The authors concluded that

this effect is correlated with the extracts’ antioxidant capacity, while the antioxidant capacity was stronger for the extracts or its fractions with higher vescalagin and castalagin content. The use of cork extracts as processing additives, namely, as thermal oxidative protection in polymer processing, has been also explored by Fernandes et al.44 and Aroso et al.156 Cork−polypropylene (PP) composites were shown to present “natural” thermal oxidative protection, and after direct processing of PP with different fractions of cork fractions, it was shown that this effect derives from the extractives’ ethanol soluble fraction. The effect is attributed to the antioxidant capacity and good mixing of this fraction in this polymer. Therefore, for other polymers, it is possible that different fractions will also exert this effect. These results give hints for future developments that can lead to commercial products based on cork phenolic extracts. However, at present, further studies are necessary to completely understand the full potential of these fractions.

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OTHER APPLICATIONS OF CORK Apart from the traditional uses of cork and the attempts to valorize its distinctive chemical constituents (suberin and extractives), cork has also been explored as a biosorbent for traditional and emerging pollutants. Emerging pollutants are synthetic or naturally occurring chemicals that are not yet monitored but that have the potential to negatively impact the environment and human health.158 The removal of these contaminants often requires costly operations, and new techniques will be necessary for an economic decontamination process. In this sense, the use of biomass to remove pollutants constitutes an alternative and less expensive process. Different sources have been tested including bacteria, fungi, sea weeds, and agricultural and forestry residues. The use of living organisms is based on their capacity to grow on the polluted environment, incorporating the pollutant molecules through accumulation within their bodies 11138


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ionic strength solutions. However, the presence of surfactants decreases the sorption rate due to emulsion stabilization effects.167 The possibility of desorption and regeneration of the biosorbent material can further decrease the material requirements and the operational costs, constituting an interesting prospect. In this sense, Pintor et al.168 evaluated several strategies for the desorption of sunflower oil from cork granules, including the use of acidic and alkaline solutions, anionic and cationic surfactants, and mechanical compression. The best results were obtained following a step mechanical compression protocol achieving a maximum oil recovery of 67% after 10 cycles.168 The use of mechanical compression desorption is preferable due to its simplicity and also because it does not uses chemicals or extraction solutions, which would require subsequent treatments. Moreover, cork is highly elastic with near complete shape recovery after compression and presents a near zero Poisson coefficient.18,22 Therefore, cork can withstand repetitive compression cycles without reduction of its properties due to its intrinsic mechanical properties. To our knowledge, the only cork-biobased sorbent currently commercially available are the ones sold under the trade name Corksorb, produced by Amorim Isolamentos SA. These are sold under different formats (bulk, pillows, booms, etc.) and are designed to be applied for the absorption of oils, solvents, and chemical compounds across a number of industries.169 Biosorption of Heavy Metal Ions. Heavy metals are common pollutants originating from industrial activity. Due to their toxicity, they must be removed from the water waste streams. The most common method employed is the precipitation as sulfides or hydroxides. However, this method produces sludges that have to be deposited on landfills. Therefore, alternative methods, such as those based on the adsorption on activated carbon, activated alumina, or polymer resins are preferred. In this view, the use of inexpensive biobased sorbents is desirable, and cork wastes offer the prospect of cheap adsorbent materials. Cork wastes have been studied for the adsorption of copper,170,171 nickel,170,171 zinc,171 trivalent chromium,172 hexavalent chromium,173−176 cadmium,177 mercury,178 and lead.177 However, despite the technological feasibility, the somewhat lower adsorption capacity has hindered the development of commercial applications. Activated Carbons from Cork. Activated carbons are extensively exploited in a wide variety of adsorption processes due to their chemical resistance and form adaptability. They are most commonly prepared from charcoal and are therefore sometimes also designated by activated charcoal. However, the use of natural carbon sources, such as biomass, represents a prospective alternative for obtaining low cost carbons.179 Therefore, the use cork industrial wastes as a source for the production of activated carbon has been proposed and investigated in several studies.180−186 Cork may also present advantages over other carbonaceous materials due to its cellular structure, leading to high surface carbon materials and low water content (energy savings). The preparation of activated carbons from cork has been performed without preactivation and with physical and chemical preactivation.182 The chemical preactivation is preferred as it usually leads to final materials with higher surface area and has been performed with phosphoric acid, potassium hydroxide, or potassium carbonate.180,183,184,186 The use of cork-activated carbons has been demonstrated for the adsorption of volatile organic compounds (VOCs) (hexane, cyclo-hexane, methyl ethyl ketone, and 1,1,1-trichloroethane),186 emerging pollutants (ibuprofen,180,187,188 clofibric,188 acetaminophen,180,189 amitriptyline,190 paracetamol180), p-nitrophenol, and phenol191. However, regardless of the good performance of

or their ability for its metabolization. However, these are very specific and time-consuming processes, while the biomass residues are prospective options for biobased sorbent materials for the rapid and unspecific removal of contaminants. The sorption of the pollutants molecules occurs on the surface of the biosorbent material due to chemical or physical compatibility. Within this approach, cork’s industrial residues have been proposed for the extraction of pollutants. Unmodified or surfacemodified cork particles have been used as biosorbent with some commercial success and also as raw materials for the preparation of activated carbons. In the next sections, we discuss cork as a biosorbent material and as a precursor for activated carbons.

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BIORSORBENTS FROM CORK Biosorbents for Organic Pollutants. One of the applications where cork has been proposed as a biosorbent is for the adsorption of organic pollutants from aqueous streams, namely, for polycyclic aromatic hydrocarbons (PAHs). PAHs are molecules composed of multiple aromatic rings without further substituents. Despite some natural sources, such as volcanic activity and wildfires, most of what is found in the environment has origins from human activities. They are primarily produced from the incomplete combustion of organic matter, namely, fossil fuels, and also from industrial processes, such as the plastics industry. These molecules are chemically and biologically very stable and are, therefore, persistent in the environment. Because they are lipophilic, they can bioaccumulate along the food chain. The limits for surface water have been enforced by the European Directive 2006/0129 EC.159 Its removal is usually performed using activated carbon; however, this is an expensive procedure, namely, for large volumes of water containing low levels of pollutants. Therefore, there is a strong motivation for using low cost adsorbents that can significantly decrease the cost of the process. Olivella et al.160 proposed the use of granulated cork from processing leftovers for the removal of PAHs from water streams. The adsorption−desorption behavior of a mixture containing 13 PAHs was evaluated. The PAHs were found to adsorb rapidly on the surface of cork particles, with 80% of the adsorption occurring on the first 2 min of contact time. The best results were achieved for pyrene, anthracene, and phenanthracene.160 The adsorption capacity of cork for PAHs is directly related with the content on aliphatic extractives (waxes), rather than with the presence of suberin. Also, the adsorption is higher for lower molecular weight PAHs.161,162 On the contrary, the adsorption of aromatic pesticides on cork occurs primarily at the lignin and phenolic extractives level. These interact with cork components by establishing π-interactions and hydrogen bonding.163,164 Biosorbents for Oil Spillages. Another field of application of biosorbents is the sorption of oil and grease from water. The oil is more difficult to achieve as it implies the competitive adsorption between oil and water molecules and requires the ability of the biosorbent to hold the adsorbed material. The presence of oil in water can originate from effluents of industrial processes or accidental spillages. In either situation, the rapid and efficient removal of the oil is required to limit contamination. The sorption process of oil on cork’s surface depends on the properties of the oil and oil-in-water emulsion properties. The sorption occurs on the surface with almost no oil reaching the interior cellular layers, and the sorption capacity is proportional to the granules’ specific surface area165 and is usually well described by the Freundlich or linear partition models.166 The sorption is favored for lower pH due to the protonation of carboxylic groups, which decreases the surface charge, and for higher 11139


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substantially. Several authors have demonstrated different routes from depolymerized suberin to new functional materials. Notable examples are the preparation of polymeric materials such as polyester and polyurethanes in different physical formats. Others have explored the use of cork suberin in composites production to obtain better properties, with apparent success. Others still have demonstrated cork extractives as additives in polymer processing. The latest research results provide strong hints that with continuous effort from the industrial and scientific community, the development of commercial products based on cork suberin may be a reality in the foreseeable future.

the cork’s activated carbons, these studies remain at the laboratory scale, and no commercial application has been reported.

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CONCLUSIONS AND PERSPECTIVES Cork is a natural material with a long history of human use. Correct forestry practices have also made it one of the most environmentally sustainable natural materials. Cork stoppers for wine bottles are the most recognizable cork product, continuing to be the most important in terms of industry revenue. The revenues generated from cork stoppers support the entire production chain, from forestry activities to industrial processing of the material. But not all cork can be used in the production of cork stoppers. As with most natural materials, cork is a heterogeneous material, with parts that do not meet the standards for the production of stoppers, whether due to insufficient thickness or the presence of structural defects. Additionally, during stoppers production, part of the cork is also rejected as leftovers. Moreover, during tree growth, the initial two harvests are also not usable. Therefore, there is a significant percentage of cork material that cannot be used for the production of stoppers. This stream of unused material has prompted the industry to develop alternative applications. The leftovers of good quality cork are granulated to smaller pieces and used to produce agglomerated cork stoppers. The remaining granulated material, usually of lower quality, is used to obtain different products, such as composite materials, insulation panels, cork pavement, or fashion products, among others. However, despite the development of these alternative applications, one grade of cork byproduct remains for which no significant use has been developedcork powder. Cork powder is defined by the Portuguese standards NP-114 and NP-273 as being composed of particles below 0.25 mm. Currently, lacking better application and due to its high calorific value (18.9−29.3 MJ/kg) and low moisture content (10−15%), it is typically burned for energy production.192 However, when burned, the commercial value of this cork material is limited by (and equal to) the cost of the fuel it is replacing, usually natural gas. Cork powder has recently been proposed and commercially explored as a biosorbent, though this constitutes a low added-value solution that does not address the true potential of cork. Therefore, within the industry, cork powder continues to be treated as a residue of low economic value. Due to cork powder’s small particle composition, it is not expected that this material can find applications within the traditional cork uses, requiring innovative approaches. Until recently, the innovations in cork applications have focused on the macroscopic material, overlooking the potential as a source of natural and renewable chemicals. In our opinion, cork is a great example of a natural material that possesses all the requirements to assume an ever-growing role in the green chemistry of the future. The full potential of cork and its components is still underexplored. In this report, we have reviewed the current knowledge of cork chemical composition and discussed its potential applications, with particular focus on industrial byproducts and its chemical components. From the different valorization opportunities identified, we consider cork suberin to constitute the most promising cork material toward future commercial exploration. It is abundant, and its depolymerization has already been well described by several methodologies. However, its exploration in the preparation of new biobased materials has not received the same level of effort. Nevertheless, this situation seems to be changing in recent years with the number of publications growing

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Ivo M. Aroso: 0000-0002-0543-548X Ricardo A. Pires: 0000-0002-9197-0138 Notes

The authors declare no competing financial interest. Biographies

Ivo M. Aroso graduated in chemistry from the Faculty of Sciences of the University of Porto in 2003 and concluded postgraduate studies in Processing and Characterization of Materials at the University of Minho in 2007. In 2005, he joined 3B’s Research Group (University of Minho, Portugal), where he has participated in several industry-funded and academic research projects. His main research interests are focused on the valorization of natural materials for different applications, including biomaterials for medical applications, active pharmaceutical ingredients (APIs) development, natural antioxidants for polymer processing, and deep eutectic solvents (DES).

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international prizes and is the PI of projects with a budget totaling more than 40 million Euros.

Ana R. Araújo graduated in Chemical Engineering from the Instituto Superior de Engenharia do Porto in 2011. Starting in October of 2011, she has developed research work in the 3B’s Research Group, participating in several projects funded by the cork industry, with a focus on the development of new applications for cork subproducts and their potential application in the biomedical field. In 2015, she initiated her studies towards obtaining a Ph.D., under the scope development of biomedical applications from natural polyphenols extracted from cork. She aims to prove the capacity of these molecules as inhibitors of protein aggregation, a common cause of neurodegenerative disorders.

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ACKNOWLEDGMENTS Ivo Aroso acknowledges the financial support from FCT through Grant SFRH/BD/42273/2007. The authors acknowledge the financial support from Projeto “NORTE-08-5369-FSE-000037”, financed by Programa Operacional Norte 2020. This work was also supported by the European Research Council, Grant Agreement ERC-2012-ADG-20120216-321266 for the project ComplexiTE and the European Union H2020, Grant H2020TWINN-2015-692333 − CHEM2NATURE.

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REFERENCES

(1) Fortes, M. A.; Rosa, M. E.; Pereira, H. A Cortiça; 1st ed.; IST Press: Lisbon, 2004. (2) Silva, S. P.; Sabino, M. A.; Fernandes, E. M.; Correlo, V. M.; Boesel, L. F.; Reis, R. L. Cork: properties, capabilities and applications. Int. Mater. Rev. 2005, 50 (6), 345−365. (3) Simoes, M. P.; Belo, A. F.; Fernandes, M.; Madeira, M. Regeneration patterns of Quercus suber according to montado management systems. Agroforest Syst 2016, 90 (1), 107−115. (4) Bugalho, M. N.; Caldeira, M. C.; Pereira, J. S.; Aronson, J.; Pausas, J. G. Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services. Front Ecol Environ 2011, 9 (5), 278−286. (5) Pinto-Correia, T.; Ribeiro, N.; Sa-Sousa, P. Introducing the montado, the cork and holm oak agroforestry system of Southern Portugal. Agroforest Syst 2011, 82 (2), 99−104. (6) Ribeiro, P. F.; Santos, J. L.; Bugalho, M. N.; Santana, J.; Reino, L.; Beja, P.; Moreira, F. Modelling farming system dynamics in High Nature Value Farmland under policy change. Agric., Ecosyst. Environ. 2014, 183, 138−144. (7) APCOR Yearbook; 2015. (8) Pereira, H.; Rosa, M. E.; Fortes, M. A. The Cellular Structure of Cork from Quercus-Suber L. Iawa Bull. 1987, 8 (3), 213−218. (9) Palma, J. H. N.; Paulo, J. A.; Faias, S. P.; Garcia-Gonzalo, J.; Borges, J. G.; Tome, M. Adaptive management and debarking schedule optimization of Quercus suber L. stands under climate change: case study in Chamusca, Portugal. Reg Environ. Change 2015, 15 (8), 1569− 1580. (10) Pereira, H., The Formation and Growth of Cork. In Cork; Elsevier Science B.V.: Amsterdam, 2007; Chapter 1, pp 7−31. (11) Costa, A.; Nunes, L. C.; Spiecker, H.; Graca, J. Insights into the Responsiveness of Cork Oak (Quercus suber L.) to Bark Harvesting. Econ. Bot. 2015, 69 (2), 171−184. (12) Oliveira, G.; Costa, A. How resilient is Quercus suber L. to cork harvesting? A review and identification of knowledge gaps. For. Ecol. Manage. 2012, 270, 257−272. (13) Teixeira, R. T.; Pereira, H. Suberized Cell Walls of Cork from Cork Oak Differ from Other Species. Microsc. Microanal. 2010, 16 (5), 569−575. (14) Gibson, L. J.; Easterling, K. E.; Ashby, M. F. The Structure and Mechanics of Cork. Proc. R. Soc. London, Ser. A 1981, 377 (1769), 99− 117. (15) Pereira, H. The Rationale behind Cork Properties: A Review of Structure and Chemistry. BioResources 2015, 10 (3), 6207−6229. (16) Faria, D. P.; Fonseca, A. L.; Pereira, H.; Teodoro, O. M. N. D. Permeability of Cork to Gases. J. Agric. Food Chem. 2011, 59 (8), 3590− 3597. (17) Sen, A.; Van den Bulcke, J.; Defoirdt, N.; Van Acker, J.; Pereira, H. Thermal behaviour of cork and cork components. Thermochim. Acta 2014, 582, 94−100. (18) Oliveira, V.; Rosa, M. E.; Pereira, H. Variability of the compression properties of cork. Wood Sci. Technol. 2014, 48 (5), 937−948.

Dr. Ricardo A. Pires graduated in Technological Chemistry from the Faculty of Sciences of the University of Lisbon (12/1998) and was awarded a Ph.D. in Materials Science and Engineering from the Technical Superior Institute from the Technical University of Lisbon (12/2004). He is currently an Assistant Researcher at the 3B’s Research Group, University of Minho, Braga, Portugal, where he been developing research activities for more than 10 years. His research is focused on the development of natural-based composites and self-assembling hydrogel systems for biomedical applications, as well as the exploitation of antioxidant activity of natural-based compounds, e.g. polyphenols, in the development of therapeutical strategies to tackle neurodegenerative disorders.

Professor Rui L. Reis, Ph.D., DSc, Hon. Causa MD, FBSE, FTERM, member of NAE, is the Vice-President for R&D of the University of Minho, Portugal, Director of the 3B’s Research Group and of the ICVS/ 3B́ s Associate Laboratory of UMinho. He is also the CEO of the European Institute of Excellence on Tissue Engineering and Regenerative Medicine, the Global President of the Tissue Engineering and Regenerative Medicine International Society (TERMIS) ,and the Editor-in-chief of the Journal of Tissue Engineering and Regenerative Medicine. He is a recognized world expert, with almost 1000 published works and more than 36 000 (h = 94 according to Google Scholar) citations to his work, on biomaterials, natural origin polymers, tissue engineering, and regenerative medicine. He has been awarded many 11141


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