Dão Pedro de Carvalho Neto
Xavier P. Gonot-Schoupinsky2†
Freda N. Gonot-Schoupinsky- 1Federal Institute of Education, Science and Technology of Paraná, Londrina, Brazil
- 2Independent Researcher, Monte-Carlo, Monaco
This systematic scoping review presents evidence from 52 primary research articles for the beneficial, and sustainable, use of coffee in personal care products. The identification and evaluation of natural ingredients that harbor bioactive compounds capable of supporting healthy personal care and protecting and improving the appearance and condition of skin and hair is topical. Demand for natural and sustainable ingredients in beauty and personal care products is driving growth in a market valued at over $500 billion. Coffee, as one of the world's favorite beverages, is widely studied for its internal benefits. External benefits, however, are less known. Here the potential of coffee and its by-products as ingredients in cosmetic and personal care formulations is explored. Diverse applications of a range of bioactive compounds from the coffee bean, leaves, and by-products, are revealed. Research is evaluated in light of economic and environmental issues facing the coffee industry. Many of the 25 million smallholder coffee farmers live in poverty and new markets may assist their economic health. Coffee by-products are another industry-wide problem, accounting for 8 million tons of residual waste per year. Yet these by-products can be a rich source of compounds. Our discussion highlights phenolic compounds, triacylglycerols, and caffeine for cosmetic product use. The use of coffee in personal care products can benefit consumers and industry players by providing natural, non-toxic ingredients and economic alternatives and environmental solutions to support sustainability within the coffee production chain. Database searches identified 772 articles. Of those included (k = 52), a minority (k = 10; N = 309) related to clinical trials and participant studies. Applications were classified, using the PERSOnal Care products and ingredients classification (PERSOC). Sustainability potential was evaluated with the Coffea Products Sustainability (COPS) model. Overall objectives of the systematic scoping review were to: (1) scope the literature to highlight evidence for the use of coffee constituents in externally applied personal care products, and (2) critically evaluate findings in view of sustainability concerns.
Introduction
The preparation and use of personal care products and cosmetics can be traced back to 10,000 B.C. in ancient Egypt and Persia, where scented herbal oils were used for moisturizing and hygienic purposes (Kumar, 2005; Chaudhri and Jain, 2009). The market for cosmetics and body care is one of the fastest growing consumer markets; its value exceeded $500 billion in 2021 (Statista, 2021). The global market for “green cosmetics,” personal care products containing natural ingredients (e.g., extracts, natural oils, or by-products of fruits and grains processing plants) as substitutes for volatile organic compounds (VOCs) and synthetic chemicals, is particularly buoyant and is predicted to increase to US$54 billion by 2027 (Statista, 2019). In Europe alone, green cosmetics have achieved a compound annual growth rates of 20% and represented over 30% of total cosmetic sales in 2015 (Liobikiene and Bernatoniene, 2017). Growing concerns and awareness of consumers about environmental risks and potential chemical toxicity are the main reasons for the on-going development of the “green cosmetics” market (Zillich et al., 2015; Lin et al., 2018). Coffee, well-known for its unique and pleasant sensorial and organoleptic characteristics, possesses wide-ranging and beneficial properties. These are relevant to the personal care product industry as green credentials, and functional active ingredients, increase in importance.
The study of coffee, coffeaology as we term it (Gonot-Schoupinsky, 2021), has unveiled over 1,000 different volatile and non-volatile compounds (Pereira et al., 2019), presenting a range of functional properties, including antioxidant, anti-inflammatory, anti-hypertensive, and antimicrobial activities (Esquivel and Jiménez, 2012; Pereira et al., 2020). The mature fruit consists of: (i) an external husk (exocarp), which is rich in caffeine, chlorogenic acids, and tannins (Pereira et al., 2019); (ii) an intermediary pulp and mucilaginous layer (mesocarp), source of carbohydrates, such as glucose, fructose, and pectin (Janissen and Huynh, 2018); (iii) parchment, composed of cellulose, caffeine, and minerals (Esquivel and Jiménez, 2012); (iv) silverskin (integument), composed of polysaccharides, such as cellulose and hemicelluloses, as well as proteins and phenolic compounds (Pereira et al., 2020); and (v) finally the seeds (endocarp), containing significant concentrations of caffeine, polyphenols, flavonoids, and triacylglycerols (TAG), bioactive compounds with high antioxidant and antimicrobial activities (Yashin et al., 2013; Haile and Kang, 2019). Coffee leaves also carry important bioactive compounds, including alkaloids, polyphenols, tannins, xanthonoids, and TAG, that can be explored by the cosmetic industry (Chen, 2019; Ngamsuk et al., 2019). Least explored are coffee flowers, which also harbor several secondary metabolites with antioxidant activity, including trigonelline, gallic acid, chlorogenic acid, and caffeine (Pinheiro et al., 2021).
The two most cultivated coffee species are Arabica (Coffea arabica), which comprises 60% of traded coffee, and Robusta (Coffea canephora), which comprises the majority of remaining industrial production; nevertheless, there are 124 wild Coffea species which merit more attention, with some under threat of extinction (Davis et al., 2019). Coffeaology has to date focused on the cultivation, harvesting, drying, pulping, and roasting of Arabica and Robusta beans for drinking coffee and issues relating to by-products from these processes (Rezende et al., 2007; Silva et al., 2011; Huch and Franz, 2015; Pereira et al., 2017). Interest relating to sustainability issues surrounding the waste generated by the roasting, grinding, and percolation processes is increasing; silverskin and spent coffee grounds are the main residual wastes (Murthy and Naidu, 2012; del Pozo et al., 2020). Over 8 million tons of residual coffee is disposed in landfills resulting in serious environmental challenges including toxicity in humans, animals and aquatic organisms (Fernandes et al., 2017). The use of these residues with varying concentrations of high-added value compounds (e.g., polyphenols, terpenes, flavonoids, caffeine, chlorogenic acids) is proposed as a renewable source of active ingredients for the cosmetic industry (Barbulova et al., 2015; Bessada et al., 2018). This is opportune, as players in the coffee industry must find a solution to the wastage from by-products (Esquivel and Jiménez, 2012; Murthy and Naidu, 2012; Jiménez-Zamora et al., 2015; Blinová et al., 2017).
The economic health of 25 million smallholder farmers, many of whom struggle and must rely on a seasonal crop, is also problematic (Mohan et al., 2016; Vanderhaegen et al., 2018; Davis et al., 2019). Therefore, the exploration of new income streams for coffee farmers supporting multiple harvest opportunities, such as coffee wastes, leaves and flowers, is pertinent. Based on these developments, this paper performs a systematic scoping review of the literature to uncover, classify, and discuss the use of coffee constituents in personal care products. Our exploration of active green and sustainable coffee ingredients was framed using the PERSOnal Care products and ingredients classification (PERSOC), and Coffea Products Sustainability (COPS) model. The research questions were (1) what is the evidence for the use of coffee constituents in externally applied personal care products? and (2) what is the potential to harness coffee as a sustainable ingredient?
Methods
Design
A scoping review design, as opposed to a systematic design, best supported our objective to comprehensively investigate this broad and diverse field (Munn et al., 2018). In addition, the Preferred Reporting Items for Systematic Reviews Scoping Review (PRISMA-ScR) was followed (Peters et al., 2015; Tricco et al., 2018), as shown in Table 1.
Table 1. PRISMA-ScR checklist.
Search Strategy
Searching commenced in November 2020 to identify relevant articles, published in English, since 1970, initially in PubMed/Medline, and then in Web of Science. The PICO framework was used to refine the search strategy: Population (all), Interventions (testing cosmetics and personal care formulations), Comparison (none), Outcome (use of coffee in cosmetic and personal care formulations) (Schardt et al., 2007). Because the search term “coffee” and “personal care” resulted in thousands of articles, we searched for “Coffea,” i.e., the botanical term, alongside “skin,” “hair,” and “cosmetics.” Complementary searches in Google Scholar and Scopus up until February 2021 were also undertaken as shown in the PRISMA diagram (Figure 1).
Figure 1. PRISMA flow diagram.
Screening and Data Extraction
Articles were imported into the Rayyan systematic review platform (Ouzzani et al., 2016) for initial assessment. Following the removal of duplicates, title and abstract screening was undertaken on 772 articles, and 180 records were assessed for eligibility as shown in the PRISMA flow diagram (Figure 1). Critical appraisal of sources of evidence, optional for scoping reviews (Peters et al., 2015; Munn et al., 2018), was not undertaken (as shown in Table 1). Data extraction followed JBI methodology (Peters et al., 2015) and was undertaken for 52 primary research articles.
Oral products were not investigated in this study. Data extraction included: (i) application discussed; (ii) part of the coffee plant, or extract used, and coffee type; (iii) active ingredients and how they were tested; (iv) main findings of the research; (v) potential impact of findings on sustainability issues.
Classification of Articles
Articles were classified to facilitate the analysis according to the personal care application of the formulation or final product investigated. These applications were defined as: (1) Protect (e.g., sunscreens); (2) Embellish (i.e., products that can color, decorate, or alter e.g., make-up, hair color, hair sprays); (3) Remedy (i.e., any products claiming healing or medicinal qualities, such as the stimulation of hair follicles, or the reduction of cellulite); (4) Sanitize (e.g., soaps, scrubs, foams); (5) Odorize (e.g., perfume); or (6) Condition (e.g., moisturizers, creams, shaving creams, among others). The PERSOnal Care products and ingredients classification (PERSOC) is shown in Figure 2.
Figure 2. The PERSOnal Care products and ingredients classification (PERSOC). The PERSOnal Care products and ingredients classification (PERSOC) enables classification according to whether the product or ingredient can Protect, Embellish, Remedy, Sanitize, Odorize, or Condition (PERSOC). Thus, PERSOC is a dual acronym. It should be noted that products and ingredients may have multiple uses, thus could be classified in one or more PERSOC category.
Critical Assessment Relating to Sustainability
Articles were evaluated according to the potential of coffee to be harnessed in a sustainable way. The Coffea Products Sustainability model (COPS) (Figure 3) was conceived to consider: (1) development of non-toxic products; (2) utilization of coffee industry waste; (3) new income streams for coffee farmers. Scoring is detailed in Table 2.
Figure 3. COffea Products Sustainability model (COPS). 1. Development and promotion of bio-degradable non-toxic personal care products and ingredients for consumer and environmental health benefits; 2. Utilization of coffee industry waste (e.g., spent coffee grounds, husks, silverskin) in personal care products to address environmental challenges relating to waste disposal; 3. Environmentally friendly diversification and new income streams for farmers including supporting multiple harvest opportunities (e.g., leaves, flowers) which leave farmers less dependent on coffee bean seasonality.
Table 2. Sustainability assessment criteria and scoring.
Results
The articles assessed (k = 52) were all empirical primary research studies; in fact only one relevant review (Bessada et al., 2018) was identified. Data extraction highlights categorized according to the formulation functionality to Protect, Embellish, Remedy, Sanitize, Odorize, Condition (PERSOC), and the results of the Coffea Products Sustainability model (COPS) analysis are shown in Tables 3–5. Statistical analysis of the articles according to coffee genotype and part, and cosmetic production, application area, and formulation development within the PERSOC classification are shown in Tables 6, 7.
Table 3. Data extraction and COPS classification of the 14 papers classified according to PERSOC where “Protect” is perceived as the dominant aim.
Table 4. Data extraction and COPS classification of the 25 papers classified according to PERSOC where “Remedy” is perceived as the dominant aim.
Table 5. Data extraction and COPS classification of the 13 papers classified according to PERSOC where “embellish,” “sanitize,” “odorize,” or “condition” are perceived as the dominant aim.
Table 6. Selected statistics of overall articles.
Table 7. Application area of the selected papers according to the PERSOC classification and the percentage of formulation development in each segment.
General Findings
Over 90% of the selected articles (k = 47) were conducted in the last decade (Tables 3–5). The country of origin showed a heterogeneous distribution with Brazil being the foremost contributor for this topic (k = 10; 19.23%), followed by Indonesia (k = 8; 15.38%), Portugal (k = 7; 13.46%), South Korea (k = 5; 9.61%), and Thailand and United States (both with k = 4; 7.69%). In terms of study design, 81% (k = 42) described in vitro, non-human participant in vivo, characterization, or a combination of these methods, many of which were carried out to assess the safety or irritability that products with the addition of coffee extracts could cause. The remaining studies 19% (k = 10) reported clinical trials (k = 7) and other studies involving participants (N = 309).
Coffee Use in PERSOC Products
The 52 articles were categorized using PERSOC (section Classification of articles; Figure 2) as follows: Protect (k = 14; 27%); Embellish (k = 2; 4%); Remedy (k = 25; 48%); Sanitize (k = 3; 6%), Odorize (k = 2; 4%); and Condition (k = 6; 11%) (Tables 3–5). Coffee has multi-functional properties, thus the PERSOC categories can overlap. Here, anti-aging effects are categorized as protective where anti-UV properties or anti-oxidant properties are reported as dominant, and remedial where cell renewal (e.g., anti-wrinkle), healing, anti-inflammatory, and/or anti-microbial effects are highlighted. A schematic of potential applications of coffee in personal care products according to PERSOC is found in the Figure 4.
Figure 4. Schematics of main cosmetic applications of coffee bean plant extracts. Created with BioRender.com. This schematic explores applications of coffee phytochemicals in personal care products using the PERSOnal Care products and ingredients classification (PERSOC) (see Figure 2).
The major application segments and the proposition of formulated cosmetics containing coffee extracts revealed anti-aging (k = 19) as the main cosmetic application, followed by sunscreen (k = 8), hydration (k = 6), and hyperpigmentation (k = 3) (Table 7). A majority of studies (60%) elaborated cosmetic formulations containing coffee parts or its extracts accounted (k = 31) (Table 7). Phenolic compounds, including chlorogenic acids, flavonoids, and terpenes, were the main phytochemicals identified 73% (k = 37). Oil fraction, composed mainly of triacylglycerols (TAG) such as linoleic, linolenic, and oleic acids, and caffeine, was reported in 6 publications (Tables 3–5). Eleven papers did not inform or propose any bioactive compounds responsible for the observed results.
Coffea arabica (Arabica) and C. canephora (Robusta) were specified as investigated by most studies 62% (k = 32), but 38% (k = 20) did not specify the species. Wagemaker et al. (2011) was the only research that included eight other coffee species (C. congensis, C. eugenioides, C. heterocalyx, C. kapakata, C. liberica, C. racemose, C. salvatrix, and C. stenophylla). Green or roasted coffee beans were the main parts investigated as potential natural substituents of synthetic active ingredients in cosmetic formulations (k = 29; 56%), followed by by-products (k = 13; 25%), and leaves (k = 5; 10%) (Table 6). Only four studies evaluated the use of end products (i.e., milled roasted coffee and instant coffee): two as potential hair colorants (Singh et al., 2015; Gonot-Schoupinsky and Gonot-Schoupinsky, 2020), one as a lipstick herpes remedy (Toscano, 2015), and one as a sunscreen (Conney et al., 2007).
Classification of Data According to COPS
Evaluation of impact of article findings using COPS scoring (section Critical assessment relating to sustainability) rated 35% (k = 18) as having a potentially high sustainability impact, 54% (k = 28) as a medium, and 11% (k = 6) as a low impact (Tables 3–5).
Discussion
This systematic scoping review is, to the best of our knowledge, the first to investigate the beneficial and sustainable use of coffee as a natural ingredient in personal care formulations. Our assessment of 52 empirical studies showed coffee has wide-ranging potential as a natural and beneficial source of bioactive compounds that can be of great interest to the cosmetic industry. Results are discussed according to: (1) active biocompounds; (2) applications of coffee extracts in the cosmetic and personal care industry; and (3) sustainability implications.
Active Compounds as Replacement for Synthetic Substances
The prospection of plant-derived metabolites in the cosmetic industry can be related to green label certifications. Although these date to 1992, commercial interest in natural and organic ingredients gathered pace in 2008 when the NATRUE Standard and Label by the International Natural and Organic Cosmetics Association called for the proportion of natural or organic compounds to be at least 75% (Cervellon and Carey, 2011). This may explain the scarcity of research we found prior to 2008. We report on three groups of bioactive compounds: phenolic compounds, triacylglycerols, and caffeine.
Phenolic Compounds
Phenolic compounds are a ubiquitous class of secondary metabolites found in virtually all structures of coffee plants. Although found in higher concentration on seeds, the exocarp, silverskin, spent coffee grounds also contains appreciable amounts (10.70 ~ 15.82% weight) of these molecules (Murthy and Naidu, 2012; Janissen and Huynh, 2018). A recent study revealed that young leaves also contain high concentrations of phenolic compounds (Ngamsuk et al., 2019). Chiang et al. (2011) and Segheto et al. (2018) suggested the coffee leaf as an appropriate source of bioactive compounds, proposing the applicability of leaf extract as an anti-inflammatory and to prevent photo-damaged skin. Challenges of using phenolic compounds in cosmetic formulations include (i) addition of surfactants or solid carriers to increase the migration of polyphenols into the skin and prevent its precipitation; and (ii) the interaction with proteins and saccharides from the final product, which may lead to the immobilization of these molecules (Zillich et al., 2015).
Among the several classes of phenolic compounds are flavonoids (e.g., kaempferol, catechin, and epicatechin) and phenolic acids (e.g., chlorogenic, caffeic, ferulic, and coumaric acids), molecules well-known for their high antioxidant activity via donation of a hydrogen atom from its hydroxyl group to the reactive oxygen species (ROS) and free radicals (Minatel et al., 2017; Santos-Sánchez et al., 2019). This radical scavenging ability is known as a defense mechanism against lipid oxidation and UV-protection in plant tissues (Minatel et al., 2017). Topical administration is commonly associated with a sunscreen effect, the reduction of oxidative stress, and antioxidant and antimicrobial properties (Zhang et al., 2015; Abdel-Daim et al., 2018). The characterization and in vitro studies performed by Cho et al. (2017) and Farris (2007) showed that the presence of chlorogenic and ferulic acids can also increase the sun protective factor in human cells through inhibition of ROS.
Chlorogenic acids (CGA) are the most abundant of phenolic compounds in coffee fruit with concentrations ranging from 0.98 to 46.14 mg/g of coffee beans according to the species (Ayelign and Sabally, 2013; Lemos et al., 2020). Although over 69 CGA were already identified in green coffee beans (Jaiswal et al., 2010), 3-caffeoylquinic acid, 3,4-dicaffeoilquinic acid, and 5-caffeolylquinic acid are commonly reported in the literature due to its higher concentrations and impacts on coffee beverage quality (Santos et al., 2021). Our study revealed that CGA present in coffee bean extract, residual press cake, and spent coffee grounds were successfully applied in in vitro trials to reduce skin hyperpigmentation and promote skin wound healing (Affonso et al., 2016; Ribeiro et al., 2018; Aulifa et al., 2020).
Flavonoids are another clade of secondary metabolites in plants produced under biotic or abiotic stress factors with a phenyl benzopyran basic structure (C6-C3-C6) (Górniak et al., 2019). Flavonoids can be use as natural organic dyes, but these heterocyclic pigments are not stable to light and other chemicals (Pozharskii et al., 2011). Color fixation issues have been observed when using coffee as hair dye (Singh et al., 2015; Gonot-Schoupinsky and Gonot-Schoupinsky, 2020). A patented and commercialized product containing coffee bean extracts rich in quercetin derivates (ECOHAIR®) showed significant hair growth in volunteers with alopecia eyebrow growth and thickness in pre- and post-menopausal women (Alonso and Anesini, 2017; Alonso et al., 2019). In the coffee plant, flavan-3-ols [e.g., (+)-catechin and (–)-epicatechin], and kaempferol are the main representants identified in coffee beans, silverskin, and spent coffee grounds (Mussatto et al., 2011; Nzekoue et al., 2020). Some of the investigated studies associated the presence of flavonoids in leaves and soluble coffee extracts to the increase in sun protective factor in cosmetic formulations and anti-viral properties against the herpes virus (Toscano, 2015; Sandoval et al., 2020).
Titanium dioxide (TiO2), a biologically inert material with ability to confer opacity to cosmetic formulations, is widely applied as an inorganic ingredient in sunscreens. Although the use of TiO2 has been authorized since 1999 by the Food and Drugs Administration (FDA), recent studies revealed that nanoparticles of this inorganic material may lead to induced oxidative stress (Kim et al., 2010; Shrivastava et al., 2014), genotoxicity (Ghosh et al., 2010; Charles et al., 2018), and neurotoxic effects (Song et al., 2015). As polyphenols are natural pigments, these compounds are able to completely absorb the UV-B spectrum and partially the UV-A and UV-C spectra when applied topically, being a suitable replacer for TiO2 nanoparticles (Nichols and Katiyar, 2010; Tomazelli et al., 2018). Studies analyzed in our work demonstrated the safety and efficiency of polyphenols present in coffee extracts through the absence of cytotoxic effects in mouse fibroblast (CCRF) and human epidermal keratinocyte (HaCaT) cell lines, and increase in SPF in cosmetic formulations (Choi et al., 2015; Cho et al., 2017; Sandoval et al., 2020).
The constant use of synthetic phenolic antioxidants SPA, an extremely varied molecular weight class synthesized through catalytic reactions between a phenolic group with oleofins, can result in harmful and carcinogenic effects in personal care products (Vandghanooni et al., 2013; Yang et al., 2018; Ham et al., 2020; Liu and Mabury, 2020). In this sense, coffee beans, leaves, and processing by-products are a potential source of renewable phenolic and antioxidant compounds for the cosmetic industry to replace SPA.
Triacylglycerols
Triacylglycerols are a rich and complex mixture of free fatty acids in a combined state with glycerol, including palmitic, oleic, linoleic, linolenic, and stearic acids, which are concentrated in the endosperm (99.6%) (Cheng et al., 2016). The oil fraction in coffee plants ranges between 7 and 17%, being significantly influenced by the genotype, fruit maturity, altitude of cultivation, and edaphoclimatic conditions (Villarreal et al., 2009). Sterols, tocopherols, and diterpene alcohols are least found. A small portion of the oil fraction is found in outer layers of the fruit (e.g., silverskin, parchment, and husk) and in spent coffee grounds, namely coffee wax, with a similar constitution in TAG (Speer and Kölling-Speer, 2006).
In cosmetic industries, mineral oils and waxes provide viscosity and consistency or lubricating and protective properties, being classified as mineral oil saturated hydrocarbons (MOSH) or mineral oil aromatic hydrocarbons (MOAH) (Chuberre et al., 2019). These substances are commonly obtained from the purification of crude petroleum oil (Cosmetics Europe, 2018). The MOAH fraction represents a public health risk (Chuberre et al., 2019). TAG are increasingly applied as emulsifiers in cosmetic formulations due to the rheological similarities with mineral oil and the absence of toxicity (Alvarez and Rodríguez, 2000; Burnett et al., 2017). Classified as a saponifiable lipid, TAG can easily penetrate lipophilic fraction of the epidermis and create a barrier to promote water retention (Burlando et al., 2010).
Characterization studies analyzed in this systematic scoping review showed a rich composition of TAG in green coffee oil, including linoleic, palmitic, stearic, oleic, arachidi, gadoleic, and linolenic acids (Wagemaker et al., 2011, 2015a). The presence of such compounds provided desirable organoleptic and physico-chemical characteristics in cosmetic formulations, besides enhancing the hydration of the skin (Pereda et al., 2009; Diamantino et al., 2019; Hilda et al., 2021). An in vivo study revealed that the combination of coffee and algae oil can mitigate trans-epidermal water loss, skin erythema, melanin formation, subcutaneous blood flow, and induced apoptosis of melanoma cells in UVA-induced BALB/c mice (Yang et al., 2017). To the best of our knowledge, the evaluated studies did not demonstrate any cytotoxic effects, which supports the use of coffee oil or wax as a mineral oil substitute in cosmetics.
Caffeine
Caffeine is a natural alkaloid produced in the aerial and germinative regions of the Coffea plant, which is accumulated in both internal and external structures of the fruit during the development as a defensive mechanism against insect attacks. This compound has a neurostimulatory effect on humans and it is associated with the bitter taste in coffee beverages (Pereira et al., 2020). Besides these well-known characteristics, caffeine has also demonstrated anti-inflammatory and antioxidant activity (Devasagayam et al., 1996; Horrigan et al., 2006; Köroglu et al., 2014), prevention of skin cancer (Kerzendorfer and O'Driscoll, 2009; Song et al., 2012), and potential weight loss (Greenway, 2001; Boozer et al., 2002). This versatility has also been observed in our study, since caffeine was associated with cellulitis reduction (Rodrigues et al., 2016a; Ngamdokmai et al., 2018), inhibition and induced apoptosis of melanomas (Conney et al., 2007), reduction of hyperpigmentation (Kiattisin et al., 2016), and anti-aging properties (Iriondo-DeHond et al., 2016; Xuan et al., 2019a). However, it is important to highlight that this alkaloid tends to precipitate depending on the vehicle used, necessitating the use of carriers or micelles for an optimum dispersion in topical formulations (Fernandes et al., 2015).
Major Applications of Coffee Extracts in Cosmetic and Personal Care Industry
Active ingredients in the coffee plant present wide-reaching application opportunities for personal care products. We found evidence for this in particular regarding the development of cosmetic products with protective and healing properties. This finding reflects the worldwide trend that these two categories constituted the major cosmetic market share in 2019 (Chouhan et al., 2021). Key applications are described for all six of the PERSOC categories.
Sunscreen (PERSOC: Protect)
The development of sunscreens was the main product investigated, comprising 23.08% (k = 12) of studies (Table 3). Although most studies are categorized as fundamental research (i.e., characterization, in vitro), their results confirmed the safety assessment and identification of the active photoprotective ingredients. An in vitro study performed by Cho et al. (2017) evaluated the absorbance capacities of green coffee extracts extracted fractions in the UV-B wavelength range (290-320 nm). The results revealed a dose-dependent sun protective factor (SPF) of the chlorogenic acid content in the green coffee extracts. This absorbance capacity was associated with the presence of conjugated double bonds in chlorogenic acid structure, which were previously reported as efficient absorbers of the UV-A and UV-B wavelength ranges (Korać and Khambholja, 2011; Yuan and Cao, 2016). Sandoval et al. (2020) demonstrated the synergistic effect between Coffea leaves and seed extract with a cream-like formulation containing 2.5% of each extract showing a SPF 6.5-times superior to one containing only ethanolic extracts of coffee leaves. Despite the lack of identification of the compounds present in the extracts, the authors attributed the photoprotective effect to the presence of phenolic compounds.
Coffee bean oil, rich in palmitic acid, also displayed strong potential as a natural sunscreen, revealing high sun protective factor when used as a sole active ingredient in cosmetic formulations (Wagemaker et al., 2011, 2015b; Yang et al., 2017) or when enhancing the protection through synergistic interactions with synthetic sunscreen (ethylhexyl methoxycinnamate) (Chiari et al., 2014). However, the presence of palmitic acid alone does not explain the increase in SPF, since this fatty acid only shows absorption capacity at short-wavelength 210 nm (Cason and Sumrell, 1951).
An in vitro study performed by Iriondo-DeHond et al. (2016) evaluated the cytotoxic and sun protective effect of coffee silverskin ethanolic extract in UV-induced photodamaged cells of C. elegans. According to the results, chlorogenic acids and caffeic acid from coffee silverskin extracts diminished UV-induced photoaging by inhibiting the action of matrix metalloproteinases, a group of enzymes expressed during UV-B radiation exposure that promotes the breakdown of elastin fibers, and through ROS scavenging. Such studies demonstrate a tangible possibility of creating a sustainable and complementary process between the coffee and cosmetic industries.
Anti-aging (PERSOC: Protect or Remedy)
Degradation of elastin and type-I collagen are the main effects of prolonged exposure to UVB radiation. Sagging skin and premature wrinkle formation is enhanced by the overexpression of matrix metalloproteinases (MMP-1, MMP-3, and MMP-9) and elastase mediated by UVB radiation exposure (Ra et al., 2006). Several studies revealed that phenolic compounds are able to reduce or inhibit the MMP to prevent accelerated skin aging. Chiang et al. (2011) evaluated the potential of coffee leaf extracts and its hydrolysates on the inhibition of enzymes of MMP complex and elastase in UVB-induced human foreskin fibroblasts. The results revealed that the coffee leaf extracts were able to reduce significantly (p < 0.001) the activity of MMP-1, MMP-3, and MMP-9. The authors attributed this inhibition to the presence of caffeic acid and chlorogenic acids present in coffee leaves. Interestingly, the coffee leaf extracts were able to restore of type-I procollagen, a precursor, in human foreskin fibroblast cells in 60% in comparison to the UV-control treatment. Similar in vitro results were also observed using coffee beans and spent coffee grounds extracts (Choi et al., 2015; Cho et al., 2017; Wu et al., 2017).
The use of coffee oil fraction as a substituent for mineral oil in the cosmetic industry is a new and prosperous avenue, since studies have demonstrated the absence of cytotoxic effect due to a composition similar to edible oils (Wagemaker et al., 2015a, 2016). This commercial trend is also reflected in the academic field. In our review 21.15% of articles reported TAG as the principal active ingredient responsible for the protective properties (Tables 3–5). An in vivo study performed by Choi et al. (2015) evaluated the effects of topical application of a basic cream formulation containing oil fraction of spent coffee grounds in photoaged hairless mice. The results showed that the TAG from coffee wax prevented wrinkle formation by reducing epidermal thickness, decrease erythema area, and increasing water holding capacity.
Four participant studies were performed concerning the applicability of coffee extracts for the reduction of fine lines, wrinkles, and skin roughness. The first (n = 69; healthy women aged 42 to 64) evaluated the anti-aging effect against lines, wrinkles, and loss of skin tone of active biocellulose masks containing, amongst other phytochemicals, Coffea arabica seed-cake extract (Perugini et al., 2020). Volunteers applied the masks three times a week for 1 and 2 months, and pre-post 3D images of the forehead and cheekbones were taken and compared. Significant decreases in skin roughness and wrinkles area were observed in both periods. Skin thickness and homogeneity also showed a significant increase following the treatment. Although the authors do not directly attribute the effects to a specific extract, it is possible to speculate that the coffee-seed cake extract was able to inhibit MMP enzymes, as previously discussed in in vitro studies (Chiang et al., 2011).
The second, a clinical trial (n = 30), investigated the use of a commercial product, CoffeeBerry®, manufactured with Coffea arabica seeds extracts, and revealed a significant reduction of fine lines, wrinkles, pigmentation, and overall appearance in all subjects after 6 weeks (McDaniel, 2009). The third, a clinical trial, used volunteers (n = 20) with visible wrinkles. It found that the use of coffee silver skin as a cosmetic active ingredient had similar effects as that of hylauronic acid (Rodrigues et al., 2016c). In the fourth, also a clinical trial (n = 40), Palmer and Kitchin (2010) evaluated the efficiency of a skin care system composed of facial wash, day lotion, night crème, and eye serum containing immature coffee bean extracts against wrinkles, blotchy redness, hyperpigmentation, tactile roughness, and flaccidity. Volunteers had Fitzpatrick skin types II and III and a specific test regiment for each formulation. After instrumentation (e.g., cutometer, photography, and corneometer measures) and self-assessment evaluations, the study revealed statistically significant results in the appearance of photo damaged skins, including improved hydration, skin extensibility, and the reduction of the appearance of wrinkles, blotchy redness and hyperpigmentation without any adverse events. The safety and efficiency demonstrated in this study supported the creation of the REPLERE® skin care line for photodamage prevention.
In our review, anti-aging products was the most prospected topic in the application of coffee extracts in cosmetic formulation with 18 such studies classified, in “Protection” or “Remedy” depending on the perceived dominant ingredient agency. Of these, 60% proposed or evaluated the formulation of cosmetics with coffee extracts, enabling the conduction of in vivo tests and clinical trials. The interaction between base and applied studies also helped to elucidate the biochemical mechanisms associated with the amelioration of photodamaged skin, which directly contributed to the development of a commercial product.
Anti-cellulite (PERSOC: Remedy)
Cellulite is an alteration on the skin topography, resulting in swelling in the subcutaneous region, enlargement and thickening of the vascular endothelium, and alterations from the adipocytes (Tokarska et al., 2018). Although the causes are considered multifactorial and unclear, studies indicate that the fat deposition on the dermal-subcutaneous interface is one of the main causes (Hexsel et al., 2009; Hamishehkar et al., 2015). This condition affects millions of women worldwide and the existent laser, ultrasound, and radial pulses treatments are considered expensive and, its effectiveness, doubtful (Tokarska et al., 2018). However, studies evaluating the topical application of coffee extracts containing caffeine on the affected area showed promising results.
A clinical trial (n = 21) conducted in Thailand used a hot herbal compress containing milled coffee beans in the lateral, posterior, inner, and anterior thigh surfaces and the results were compared with a placebo compress during a 9 week interval (Ngamdokmai et al., 2018). The results showed a significant (p < 0.05) reduction on the measurements of the skin-fold thicknesses and circumferences. The action mechanism of caffeine in the reduction of cellulite is associated with the promotion of lipolysis in adipocytes through the increase of phosphorylation in hormonesensitive lipases via cAMP (Diepvens et al., 2007) or through the blockage of α-adrenergic receptors, thus preventing the fat deposition (Panchal et al., 2012). An in vitro study conducted in Brazil revealed the safety of the topical application of caffeine extracted from silverskin and the efficiency of nanostructured lipid carriers (NLC) in crossing the skin barrier (Rodrigues et al., 2016a). The increase of hydrophobicity in NLC-conjugated caffeine improves the topical absorption of caffeine and, thus, increases the local lipolytic activity without requiring a systemic distribution of the substance (Santos et al., 2021).
Hair Coloration (PERSOC: Embellish)
Gray hair (canities) can impact quality of life and well-being, and result in psychological effects (psychocanities) including low self-esteem; hair loss (alopecia) can also impact everyday life (Gonot-Schoupinsky and Gonot-Schoupinsky, 2020). Alternative hair dying options are relevant as some are considered cytotoxic and are associated with acute toxicity, contact allergy, and genetic toxicity (Nohynek et al., 2004). However, natural organic alternatives can be less persistent in color as previously mentioned (Pozharskii et al., 2011; Singh et al., 2015; Gonot-Schoupinsky and Gonot-Schoupinsky, 2020).
Gonot-Schoupinsky and Gonot-Schoupinsky (2020) investigated (n = 2) the use of a pure instant coffee solution as an alternative stain for dark brown hair and to mask the gray hair. Despite the low persistence in tone, the 7-month treatment was acceptable. One participant reported decreased scalp irritability, probably due to anti-inflammatory activities of the phenolic compounds. Singh et al. (2015) proposed fourteen hair colorants containing extracts from several plants, including roasted coffee beans. After in vitro assessments with wool fibers, six colorant formulations with desired fixation were tested with volunteers (n = 25). All but one of the five formulations containing coffee powder, including the most accepted with a percentage of 96%, were effective.
The toning capability of roasted coffee beans can be associated with melanoidin, a polymeric, high molecular weight molecule originated from non-enzymatic Maillard reactions between carbohydrates and compounds with a free amino residue during the roasting process (Chandra et al., 2008; Moreira et al., 2012). These studies open new avenues for the exploration of coffee as a natural source of hair colorants; however, coffee by-products (including silverskin and spent coffee grounds) can be a more sustainable alternative, as residual wastes are also rich in coffee melanoidins (Jiménez-Zamora et al., 2015).
The commercial product ECOHAIR®, elaborated with extracts of Coffea arabica and Larrea divaricate, was investigated in two clinical trials to evaluate the efficiency of the product in (i) patients with non-cicatricial alopecia during a 3-month treatment, and (ii) eyebrow and eyelash growth in healthy pre- and post-menopausal women (Alonso and Anesini, 2017; Alonso et al., 2019). In the first study, volunteers (n = 52) applied the product once a day during 90 days and overall volume, appearance, and thickness of hair, and decrease of dandruff were determined by ocular inspection aided by a magnifying glass. The authors reported an overall improvement on hair appearance in 50 participants and the visual reduction of dandruff in 45. These characteristics were attributed to coffee bean extracts stimulating the hair growth in the anagen phase and inhibiting the growth of Malassezia furfur, a yeast associated with alopecia and dandruff, as reported in participants of the same group. The other study, Alonso et al. (2019) evidenced a significant eyelash and eyebrows in 100 and 80% of their participants (n = 10) after a 2- and 3-month treatment with the product, respectively.
Soaps and Scrubs (PERSOC: Sanitize)
Research relating to the application of coffee by-products (Delgado-Arias et al., 2020) and coffee beans (Hilda et al., 2021) for body scrubs report satisfactory results. The abrasive nature of the coffee grinds likely work in conjunction with the bioactive compounds. A novel use for coffee husks to make potash, a raw material for soap, was reported by researchers in Cameroon (Pauline et al., 2010) reflecting the potential for inexpensive and sustainable solutions using coffee for basic and necessary personal care products. A recent study conducted by Deotale et al. (2019) revealed that chlorogenic acids and hydrocarbons in coffee oil are able to self-assemble, create stable micelles and reduce the surface tension. Despite coffee oil being a natural surfactant, its use for this application in soaps was not highlighted in the review findings.
Anti-microbial (PERSOC: Odorize)
Unpleasant odors in the human body can be caused by several factors, including normal sweat and sebaceous gland secretions. However, when the odors generate discomfort and embarrassment it can be associated with the proliferation of common skin-resident bacteria (Nestora et al., 2016). The Staphylococcus epidermis plays a major role in foot odor through the conversion of leucine, present in the sweat, into isovaleric acid, a volatile organic compound with a sour and pungent odor (Ara et al., 2006). Methylparaben is a common substance added to cosmetics with antimicrobial activity through the disruption of the plasmatic membrane and the denaturation of enzymes (Soni et al., 2002). Although there are no studies showing the acute toxicity or accumulation of this substance in animal models (Soni et al., 2002), research relating to the replacement or reduction of this chemical for plant-extracted compounds is on-going. An in vitro research conducted by Santoso and Riyanta (2019) in Indonesia revealed that a foot sanitizer spray using the ethanolic extract from coffee beans and ginger showed significant antimicrobial activity against S. epidermis. Although not being fully elucidated, the antimicrobial activity could be correlated with the high concentration of chlorogenic acid and caffeine found in the coffee beans (Duangjai et al., 2016). In this sense, polyphenolic-rich coffee by-products could be explored in further studies as a source material for sanitizing cosmetic formulations.
Hydration (PERSOC: Condition)
Moisturizing cosmetics are developed to replace the intracellular lipids removed during the cleansing or exfoliation of the skin's surface, and retard the transepidermal water loss through the formation of a thin lipophilic film on the surface of the skin (Draelos, 2018). This role is performed by occlusive substances, including hydrocarbons, stearic acid, linolenic acid, and sterols, commonly found in plants oils. The coffee bean has been extensively investigated as a natural ingredient in moisturizing cosmetics due to its rich oil composition and antioxidant activity (Pereda et al., 2009; Chaiyasut et al., 2018; Diamantino et al., 2019; Putri et al., 2019). However, recent studies also demonstrated the effectiveness of hydro-alcoholic extracts of coffee silverskin as an occlusive agent (Rodrigues et al., 2016b,d). In a single blinded study (n = 20), Rodrigues et al. (2016c) evaluated the effect of coffee silverskin on skin hydration with promising results (note that a clinical trial also described in this article is discussed under “Remedy” and the article is categorized under “Remedy”). In vitro studies performed using human immortalized non-tumorigenic keratinocyte and foreskin fibroblasts cell lines showed no cytotoxicity when compared to the control. Long-term organoleptic characteristics, pH, microbial count, and antioxidant activity were stable both at 20 and 40°C during 180 days, showing that coffee silverskin extract is suitable as an active ingredient in cosmetic formulations (Rodrigues et al., 2016b).
Sustainability Implications
Cosmetic companies are challenged to drive innovation-oriented investments but also to appeal to green consumers, and take responsibility for sustainable, social, economic, and environmental solutions. The industry must thus develop products that are commercially attractive, natural, non-toxic, and sustainable (McEachern and McClean, 2002; Feng et al., 2018). Recent interest in sustainability has led to increased attention in the use of molecules from raw plant materials and by-products of food processing due to their rich composition in bioactive compounds, including phenolic compounds and fatty acids, affordable costs, and high availability (Nunes et al., 2017). Our critical evaluation using COPS assessed firstly the development of non-toxic products; secondly the potential of coffee waste as renewable sources of natural active ingredients; and, thirdly, new environmentally friendly income sources for coffee producers and their environmental impact.
The assessment of new organic molecules in coffee components capable of replacing synthetic chemicals showed satisfactory results. Of the 52 articles, only six (11.54%) had a low impact regarding the non- or partial replacement of synthetic components (Chiari et al., 2014; Marto et al., 2016a; Safrida and Sabri, 2017; Handayani et al., 2019; Putri et al., 2019; Santoso and Riyanta, 2019). This finding is extremely favorable, but our review suggests that the “green label” term may be used in a unilateral way. Many articles met the criteria of proposing or performing the total substitution of synthetic compounds in formulations. However, the majority used coffee beans as raw material, which has a low impact on the social and environmental sustainability of this cosmetic-coffee industry interrelation, leading to half of the studies being classified as medium (50.00%; k = 26).
The environmental and social sustainability pillars of the coffee industry must also be pursued, and it may require a more transparent position from the cosmetic industry regarding the production process using coffee extracts and wastes to avoid “greenwash” (Cervellon and Carey, 2011). The coffee industry generates over 6 million tons of solid residual waste yearly that are processed using basic waste management techniques (Blinová et al., 2017; Pereira et al., 2020). Nevertheless, the involvement of some global coffee producers in the search for the valorisation of coffee residues in high-added value products may accelerate sustainable solutions. According to our research, 16 papers (30.77%) proposed the prospection of residues as a reliable source of active ingredients and achieved a high COPS score concerning the environmental sustainability. Interestingly, our findings found residual wastes and leaf extracts were explored mainly by producing countries (e.g., Brazil, Taiwan, Indonesia, and Thailand) and South Korea (Tables 3–5). According to the Observatory of Economic Complexity (OEC, 2019), South Korea imported over US$ 1.3 million in coffee husks in 2019, indicating a growing interest in the potential applications of the rich composition of this agro-industrial waste.
Finally, when the economically cosmetic appealing “green” label also addresses the social sphere, bilateral sustainability can be achieved. A recent techno-economic analysis revealed that coffee beans produced with dry or wet processing methods generate an economic profit that is not socially sustainable (Magalhães Júnior et al., 2020). The use of coffee beans as raw material for active ingredients in the cosmetic industry could follow two possible scenarios: (i) part of the green bean production could be redirected to a new market niche; or (ii) investments in infrastructure, equipment, and technology could enable the processing plants to carry out extraction processes from coffee beans. Neither scenario is ideal. The first would not provide significant changes in sales prices; while the second requires high initial investment, excluding approximately 25 million smallholder farmers (Vanderhaegen et al., 2018). Therefore, the exploitation of leaves and residual wastes would better represent an additional and significant source of income in either one of the described scenarios due to their abundance and lack of a consolidated commercialization. This can also assist the disposal of coffee residues and solve the economic and ecological imbalance in the cosmetic-coffee industries relationship. Once these issues are addressed, commercial products containing coffee bean extracts as active ingredients, can present a higher sustainability impact. Despite these bottlenecks, it is possible to observe a paradigm shift as 16 studies conducted in the last 5 years were classified as “high” according to the COPS scale due to the valorization of coffee by-products or leaves.
Future Areas for Research
Research in this area is in its infancy, and there is great potential, in terms of investigating active ingredients within coffee, of which there are over 1,000 (Pereira et al., 2019), of exploring their PERSOC applications, and in finding solutions for sustainability problems. Furthermore, the Coffea genus includes 124 wild species (Davis et al., 2019), and while Arabica and Robusta varieties comprise 94% of worldwide coffee production, which explains the clear research focus on these varieties, investigation of other species may bring additional perspectives, uncover additional active ingredients, and save them from extinction.
Future research can focus on prioritizing sustainable ways to harness bioactive compounds, and filling in the many gaps that are suggested by the review results. For instance, we did not find any articles relating to the use of coffee flowers. Sweet smelling, like jasmine, coffee flowers contain a range of bioactive compounds (Pinheiro et al., 2021). Another gap was the use of coffee oil as a surfactant, for instance in soaps, or as an emulsifying agent in cosmetics. There is a need to conduct well-designed and well-populated in vivo and clinical trials to assess the safety, investigate the mechanisms of action, and characterize the market potential of these new green products. All applications merit further exploration. One example is the need to fully elucidate the action mechanism involving coffee oil fraction on UVA and UVB absorbencies. Another area of focus is how to harness coffee as a more effective pigment to provide a natural solution for hair coloring and care. Although hair care products were less explored than skin care (Table 6), our review suggests studies in this segment of the cosmetics industry are gaining attention. However, it is necessary to carry out more studies, including in vivo and in vitro tests in order to identify the bioactive molecules responsible for the hair growth stimulation and antimicrobial activity; thus, enabling the elaboration of a more efficient extraction process and the use of coffee processing residues.
Further studies should also be conducted to assess the effectiveness of cellulite reduction in clinical trials. Although caffeine concentration is superior in coffee beans, the NLC-conjugated caffeine extracted from silverskin represents a more sustainable alternative for the formulation of cosmetics. There are many academic fields that can play an important role in future research including biochemistry, waste management, food science, dermatology, trichology, health psychology, environmental science, integrative medicine, and also business and management fields. As well as scientific collaborations, cooperation between academia, industry, and farmers, is necessary to encourage the development of non-toxic products, the utilization of coffee industry waste, and encourage new income streams for coffee farmers.
Limitations of the Review
A more comprehensive search strategy would have been preferable, as only two databases were searched. However, the purpose of this review was not to be exhaustive, but rather to give insight into the wide-ranging developments relating to the use of coffee active ingredients in personal care products, and to highlight the sustainability issues that this raises. Critical appraisal of research quality was not undertaken due to our concern being more to critique the research in terms of their implications on sustainability issues. The PERSOC classification gives an alternative perspective, but as coffee compounds manifest high multi-functionality categories can overlap.
Conclusions
The results of this systematic scoping review highlighted coffee as a naturally beneficial and potentially sustainable ingredient in personal care products. Coffee bean extracts, oils, leaves, and by-products provide an important source of bioactive compounds due to their desirable antioxidant, antimicrobial, anti-aging, and anti-inflammatory effects. Using the PERSOnal Care products and ingredients classification (PERSOC) we found that coffee constituents had beneficial applications in a wide range of personal care products that protect, embellish, remedy, sanitize, odorize, and condition the skin, hair, and face.
Despite the relevance of these findings, research into coffee bioactives for cosmetic purposes is still under development, and there are still many gaps. Of the studies reviewed (k = 52), only ten studies involved participants (N = 309), and only three discussed commercially available products containing coffee derivates. However, critical evaluation using the Coffea Products Sustainability (COPS) model, suggests the results are promising; moreover, by-products of the coffee processing chain represented almost 25% of the raw materials in the studies. Effective management of coffee waste is crucial for environmental and social-economic impact to result in a sustainable producing chain and additional and alternative income for coffee producers. Furthermore, as shown in this review, the use of coffee phytochemicals can be a very effective and accessible way of extending innovation within the personal care products industry, and enabling new non-toxic products for discerning consumers.
Data Availability Statement
The original contributions presented in the study are included in the article/supplementary material, further inquiries can be directed to the corresponding author/s.
Author Contributions
DC and FG-S: conceptualization, methodology, systematic scoping review data–acquisition and eligibility, writing–original draft, and writing–review and editing. XG-S: conceptualization, methodology, systematic scoping review data–acquisition and eligibility, and writing–review and editing. All authors contributed to the article and approved the submitted version.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's Note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Footnotes
*^Featured in systematic scoping review (with asterix before).
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Keywords: phytocosmetics, Coffea, green cosmetics, coffee by-products, phytochemicals, sustainability
Citation: Carvalho Neto DPd, Gonot-Schoupinsky XP and Gonot-Schoupinsky FN (2021) Coffee as a Naturally Beneficial and Sustainable Ingredient in Personal Care Products: A Systematic Scoping Review of the Evidence. Front. Sustain. 2:697092. doi: 10.3389/frsus.2021.697092
Received: 18 April 2021; Accepted: 29 September 2021;
Published: 28 October 2021.
Edited by:
Carmen Sofia da Rocha Freire, University of Aveiro, PortugalReviewed by:
Saurabh Pratap, Indian Institute of Technology (BHU), IndiaFrancisca Rodrigues, LAQV Network of Chemistry and Technology, Portugal
Fernando M. Nunes, University of Trás-os-Montes and Alto Douro, Portugal
Copyright © 2021 Carvalho Neto, Gonot-Schoupinsky and Gonot-Schoupinsky. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Dão Pedro de Carvalho Neto, ZGFvLm5ldG8mI3gwMDA0MDtpZnByLmVkdS5icg==; Freda N. Gonot-Schoupinsky, RnJlZGEuUmVzZWFyY2gmI3gwMDA0MDtnbWFpbC5jb20=
†ORCID: Dão Pedro de Carvalho Neto orcid.org/0000-0002-7164-2196
Xavier P. Gonot-Schoupinsky orcid.org/0000-0002-5444-696X
Freda N. Gonot-Schoupinsky orcid.org/0000-0002-2427-6218
‡These authors have contributed equally to this work