Waste Management 90 (2019) 72–83

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Waste Management
journal homepage: www.elsevier.com/locate/wasman

Biotechnological approaches for cocoa waste management: A review

Zulma S. Vásquez a, Dão P. de Carvalho Neto a, Gilberto V.M. Pereira a,
Luciana P.S. Vandenberghe a,⇑, Priscilla Z. de Oliveira a, Patrick B. Tiburcio a,
Hervé L.G. Rogez b, Aristóteles Góes Neto c, Carlos R. Soccol a
a
Bioprocess Engineering and Biotechnology Department, Federal University of Paraná (UFPR), 81531-980 Curitiba, PR, Brazil
b
Centre for Valorisation of Amazonian Bioactive Compounds (CVACBA), Federal University of Pará, 66075-750 Belém, PA, Brazil
c
Federal University of Minas Gerais, Institute of Biological Sciences, 31270-901 Belo Horizonte, MG, Brazil

a r t i c l e i n f o a b s t r a c t

Article history: Cocoa beans provide raw materials for global food industries valued in excess of $47 billion in world
Received 11 October 2018 exportations. Through on-farm processing, about 80% of cocoa fruit is discarded as residual biomass,
Revised 9 April 2019 including cocoa pod husks, cocoa bean shells and cocoa sweatings. Farmers routinely discard these
Accepted 13 April 2019
residues/by-products during the initial cocoa bean processing steps, occupying vast areas and raising
Available online 24 April 2019
social and environmental concerns. Alternatively, this residual biomass is used as cocoa tree fertilizer.
However, its disposal is performed without proper treatment, resulting in putrid odors and plant dis-
Keywords:
eases. Recently, some studies have reported the use of cocoa by-products in the production of high-
Cocoa
Cocoa by-products
value-adding molecules with potential applications in the food, pharmaceutical and cosmetic industries.
Residual waste valorization In this aspect, biotechnological approaches have been shown to be a viable alternative for the transfor-
mation of this residual biomass into fine products. This article reviews the biotechnological approaches
implemented for the management and exploitation of cocoa by-product. Related topics on cocoa produc-
tion and residual biomass generation, sustainability and valorization of cocoa chain are addressed and
discussed.
Ó 2019 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 72
2. Cocoa (Theobroma cacao L.) botany and cultivation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
3. Cocoa production chain and residual biomass generation. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 73
4. Sustainability of the cocoa production chain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 74
5. Valorization of cocoa chain residues/by-products . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 75
5.1. Cocoa pod husk . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 76
5.2. Cocoa bean shell . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
5.3. Cocoa sweatings . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
6. Conclusions and future perspectives. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 79
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
Declarations of interest. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 80

1. Introduction

Abbreviations: CPH, cocoa pod husk; CBS, cocoa bean shell; CS, cocoa sweatings. The generation of large amounts of organic waste, currently
⇑ Corresponding author. labeled as residual biomass, is the major drawback faced by
E-mail address: [email protected] (L.P.S. Vandenberghe). agro-industry. The most abundant and problematic crop residues

https://doi.org/10.1016/j.wasman.2019.04.030
0956-053X/Ó 2019 Elsevier Ltd. All rights reserved.
 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83 73

Fig. 1. Production of cocoa beans and generation of residual biomass. Residual biomass data were calculated according to ICCO Quarterly Bulletin of Cocoa Statistics (The
International Cocoa Organization, 2018).

are those of a lignocellulosic nature. This kind of material repre- fruit formation at 3 years and reaches its maximum yield and pro-
sents approximately 60% of vegetal biomass (Rodrigues, 2016), ductivity after 8 to 9 years. The fruit develops on the trunk and
and its disposal usually causes difficulties due to the volume and twigs of the cocoa tree. Botanically, cocoa is considered berry-
recalcitrant structure that characterize it. The food and biofuel like fruit and reaches a length of 15 to 25 cm and a diameter of 8
industries are associated to the huge accumulation of these wastes, to 13 cm (Kim et al., 2011). When mature, the pod contains
such as sugarcane bagasse (Gabov et al., 2017), coffee shells and between 20 and 40 almonds, which are covered by a mucilaginous
husks (Castro et al., 2018; Murthy and Madhava Naidu, 2012), corn pulp (Minifie, 1989). The almonds and pulp are extracted from the
stover (Lizasoain et al., 2017), rice straw (Morone et al., 2017), cocoa fruit and used as raw material for chocolate production.
wheat straw (Motte et al., 2014), and cocoa by-products Cocoa tree cultivation requires a tropical climate for full devel-
(Martínez et al., 2012). Residual biomass has the special character- opment and bean production, with temperatures between 18 and
istic of being cheap, renewable and abundant, which makes it an 32 °C, altitudes below 400 m, rainfall well-distributed throughout
interesting material in various industrial processes. the year and environments with high humidity (70–90%)
Cocoa by-products are originated in the field-processing chain, (Afoakwa, 2010). To achieve these strict edaphoclimatic conditions,
where cocoa beans are removed from the cocoa pod husk, fer- cocoa plantations usually lie between 20 °N and 20 °S of the Equa-
mented and dried for storage and transport. Aside from cocoa tor. During their natural spread, some cocoa hybrids expanded into
beans, the fruit is composed of a pod husk, bean shell and pulp, two directions, resulting in two main cocoa groups: Criollo and
representing together about 70–80% of the fruit in dry weight Forastero. The Forastero was spread towards the south of the Ama-
(Prabhakaran Nair, 2010b). This large-scale generation of residual zon River and for Guyana, and Criollo for the Central America and
biomass represents a critical environmental concern for cocoa- south of Mexico (Ceplac, 2015). Nowadays, Africa, South America
producing countries. and Asia are the main cocoa bean-producing and -exporting
Cocoa beans are mainly used for chocolate and cocoa-derivative regions (The International Cocoa Organization, 2018). Cote d’Ivoire,
food production, including cocoa paste, butter, powder and liquor. Ghana, Cameroon and Nigeria in West Africa are the largest cocoa
These products are largely consumed and appreciated around the producers in the world. However, the expansion of this culture in
world, showing a consumption growth rate in European Union African countries is compromised because the scarcity of regional
and North America (1.7 and 3.6% annually, respectively) (FAO, forests and the protection of the remaining forest fragments by
2003). According to the last report of The International Cocoa national reserves (Franzen and Borgerhoff, 2007). On the other
Organization (2018), the cocoa beans production during the hand, South American countries, such as Brazil and Ecuador, can
2015/16 crop was estimated at 3.9 million tons. In parallel, it is use the large forest extensions still available (i.e., Amazon and
estimated that 16 million tons of residual biomass were produced, Atlantic Rainforest) for the expansion of cocoa culture.
taking in account based on the aforementioned dry weight of the The production of shade-grown cocoa, usually called ‘‘agro-
fruit (80%) (Fig. 1). This article reviews the biotechnological forestry” (Franzen and Borgerhoff, 2007), enables the use of native
approaches implemented for the management and exploitation treetops as natural shading necessary for the full development of
of cocoa by-products, highlighting the importance of its con- cocoa plants (Clay, 2004). This system of cultivation has also been
stituent molecules for the production of value-added products observed and evaluated as a promising alternative for the regions’
with application in several fields of study. biodiversity conservation.

2. Cocoa (Theobroma cacao L.) botany and cultivation 3. Cocoa production chain and residual biomass generation

The Theobroma cacao L. tree is a species of the Malvaceae family, Cocoa consumption dates back 3000 years to the Aztec and
which is native to Central and South America, specifically the Ama- Mayan civilizations. Archaeological reports demonstrate the con-
zon basin (Gonzáles et al., 2013; Oetterer et al., 2006). The cocoa sumption of a beverage produced from cocoa beans, the xocoatl,
plant is a shade-loving plant capable of reaching between 4 and by the Aztecs in 400 B.C. (Beckett, 2009; Dand, 2011). However,
10 m in height (Afoakwa, 2010). Theobroma cacao L. usually begins worldwide cocoa dissemination only occurred in 1519, when the
74 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83

Aztec civilization presented the cocoa seeds to the Spanish over situations related to cocoa production was the study con-
explorer Hernando Cortéz (Dhoedt, 2009). On his return to Spain, ducted by the World Bank (2012) on the agricultural cocoa sector
Cortéz introduced the drink and the first seeds to the continent, in Ghana, one of the world’s most important producers. This report
which, over the years, won the taste of the Europeans. With the concluded that several stages of the cocoa supply chain, such as
cocoa drink’s consumption spreading quickly, the monopoly of production, the market and the environment, were at risk. These
cocoa bean production became unviable, and the Italian, Dutch sectors are strictly associated with the growth and long-term sus-
and Portuguese colonies of West Africa became the main cocoa tainability of the cocoa supply chain. From that moment, this mat-
producers (Afoakwa, 2010). Thus, cocoa along with wine, bread ter became remarkably relevant in policymakers’ and stakeholders’
and beer, is considered one of the oldest fermented foods con- debates over the global cocoa industrial chain. Some characteristics
sumed in the world. of the three spheres of sustainability (social, economic and envi-
Nowadays, cocoa production and its supply chain are one of the ronmental) will be slightly elucidated.
most important around the world due to its familiar-based cultiva- First, the social element of the cocoa industry’s sustainability is
tion and logistics necessary for transportation, commercialization, quite relevant, considering that this sector is characterized by
manufacturing and distribution of the raw material and derived intensive family activity. According to Beg et al. (2017), around
products. However, the cocoa processing chain has remained 40 to 50 million people receive incomes from cocoa farming. In
unchanged for 150 years. The steps to transform the seeds into the 2015/16 crop, the familiar-based cocoa cultivation was respon-
the final products (e.g., chocolate, butter and cocoa liquor) consist sible for a worldwide production of 3.9 million tons and a product
of harvesting, fermentation, roasting, deshelling, grinding and pul- exportation of approximately $47 billion dollars (The International
verization. In each of these steps, a substantial residual biomass is Cocoa Organization, 2018; International Trade Center, 2019a).
generated. Based on these numbers, the guarantee of a decent and fair liveli-
Cocoa fruits are harvested after maturation and the pods are hood for cocoa farmers remains a priority in the sector, along with
opened with a club, knife or machete. The use of sharp objects the importance of education and constant training in cocoa-
requires considerable experience and ability to avoid damaging growing communities.
the seeds. A longitudinal cut is made in the pod husk to expose Secondly, regarding economics, the cocoa industry faces diffi-
the cocoa beans and the pulp. Cocoa beans, along with the sur- culties such as cocoa bean price fluctuation and speculation, low
rounding mucilaginous pulp, are distributed in heaps for further investments, exorbitant taxes, variations in global economic
fermentation. Pod husks are then disposed of directly in the soil. growth and fluctuations in the U.S. dollar against other major cur-
The pulp, in contact with metallic tools or impurities from rencies (Boas, 1989). Moreover, political and social instabilities in
boxes, is exposed to a consortium of microorganisms (e.g., lactic the main producing countries influence cocoa prices (The
acid bacteria, acetic acid bacteria, yeasts and filamentous fungi), International Cocoa Organization, 2012). Thirdly, the environmen-
which promote several physical and chemical changes in both pulp tal aspects of the cocoa industry present some relevant issues, such
and beans. Fermentation is usually carried out for 8 days, exhibit- as (i) the necessity of environmental instructions for better admin-
ing a diverse group of microorganisms and peaks of varying istration of natural resources (i.e., land and water), (ii) regulation of
metabolites (i.e., ethanol, lactic acid, acetic acid) (Schwan and the use of agrochemicals to reduce the negative effects on the envi-
Wheals, 2004). In the post-harvest stage, the excess juice, which ronment and farmers’ health without affecting expected produc-
is the resultant of pulp-pectin degradation at low pH and negative tivity (Wessel and Quist-Wessel, 2015), (iii) conservation of local
pressure, is drained through fissures in the fermentation boxes and ecosystems and biodiversity (Baker, 2000) and (iv) improving the
discarded in the soil. capacity to respond to possible climatic changes and eventually
The fermented beans are then processed on an industrial scale, adequately managing the waste generated during cocoa produc-
generating cocoa products (e.g., cocoa powder, butter and liquor). tion (Ntiamoah and Afrane, 2008).
Cocoa beans pass through thermal shock for removal of the sur- Considering this brief description, it is possible to understand
rounding shells and later are subjected to a stream of air (winnow- that this sector is vulnerable to agro-ecological, social and eco-
ing), which promotes their separation from the cleansed nomic conditions. Therefore, efforts must be oriented to improve
cotyledons (nibs), allowing for a homogeneous roasting (Biehl process conditions and respond to the market’s demands. Some
and Ziegleder, 2003). Nibs are roasted at temperatures between of the established endeavors to improve the cocoa supply chain’s
120 and 150 °C with varying heating ramps depending on the current situation can be summarized as (i) creation of policies that
bean’s maturation level and the desired final product (Schwan benefit the industry and establishment of organizations to verify
and Wheals, 2004). High roasting temperatures promote a series its compliance, (ii) private and public investments, (iv) studies
of complex Maillard reactions, resulting in the conversion of free and promotion of findings related to cocoa research, (v) establish-
amino acids and reduction of sugars into aldehydes, pyrazines ment of traceability systems, (vi) determination of priority areas
and higher alcohols that directly influence the development of for action throughout the chain and (vii) development of certifica-
cocoa’s flavors (Aprotosoaie et al., 2016; Schwan and Wheals, tion standards to improve the supply chain practices and their
2004). implementation.
Today, various certification schemes are used as a tool in the
cocoa industry to ensure the application of some fundaments for
4. Sustainability of the cocoa production chain the sustainable cocoa production. Among them, it is possible to
highlight the FairtradeÒ, Rainforest AllianceTM and UTZTM. Certifi-
At the beginning of the 21st century, international media cation schemes have been considered effective instruments to
focused on the cocoa supply chain due to irregular work situations. foment sustainability in the cocoa value chain. However, cocoa
Subsequently, the International Cocoa Agreement advocated for producers are unsure of the real benefit at the farm level due to
the development of a sustainable cocoa economy (United the involved financial responsibilities. In 2012, KPMG Advisory
Nations, 2001). Some studies were carried out to identify child was commissioned by The International Cocoa Organization (ICCO)
labor activities (Abenyega and Gockowski, 2001; Schrage and to conduct a study on the costs, advantages and disadvantages of
Ewing, 2005), gender inequality (Hiscox and Goldstein, 2014) and cocoa certification. This analysis found that although little avail-
unfair working conditions for thousands of workers (Fromm able is information about this subject, the advantages of imple-
et al., 2013), mainly in Africa. Another result of the great concern menting certification schemes for cocoa production are much
 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83 75

higher than the disadvantages of adhering to this system (Basso agro-industrial residues with lignocellulosic characteristics have
et al., 2012). In any case, importing countries’ demands for certified occurred. Biofuels, chemical products, biological hydrogen, energy,
cocoa continue to increase, probably because it is one of the most animal nutrition products and biomaterials have been produced in
concrete instruments that, in theory, allows for the increase of pos- the last few years after meticulous research on the potential of
itive impacts at all levels for cocoa producers. According to The residual biomass from sugarcane, palm oil, cassava, corn, coffee
International Cocoa Organization (2017), the improvement of pro- and rice, among others (Islam et al., 2018; Ngaosuwan, 2015; Nie
duction conditions would have a significant impact on the three et al., 2015; Saidi et al., 2018; Soccol et al., 2017).
main production areas, allowing a superior social and economic By definition, bioactive compounds are essential and non-
development. essential nutritional constituents that occur in small quantities in
One way to improve this important food chain’s sustainability is food and confer benefits for human health (Biesalski et al., 2009;
to properly manage the produced residual biomass through the Kris-Etherton et al., 2002). These compounds have been evaluated
biotransformation of cocoa fruit. Actions to improve this aspect to prove their anti-inflammatory effects (Kim et al., 2010, 2004;
would result in less phytosanitary problems and would simultane- Rao et al., 2008), protective properties against cardiovascular dis-
ously produce new incomes for farmers, considering the resulting eases (Hung et al., 2000; Yochum et al., 1999), and other bioactive
valorization of the residual biomass that has been slightly used characteristics. The cultivation and use of cocoa for nutritional and
so far. The implementation of biotechnological tools and extraction medicinal purposes date back over 3000 years, with the first
techniques could be a relevant and effective way to obtain value- reports related to the Mayan and Aztec civilizations (Scapagnini
added products from cocoa production chain residues. The most et al., 2014). The presence of bioactive compounds in cocoa beans
relevant results of research related to this topic are described and their products (e.g., chocolate, butter, essential oil) has been
below. extensively evaluated, as described by Ellam and Williamson
(2013). These compounds (mainly polyphenols) are responsible
5. Valorization of cocoa chain residues/by-products for the antioxidant (Davison et al., 2012; Gu et al., 2006; Othman
et al., 2007; Schinella et al., 2010), antitumor (Khan et al., 2015;
During the last few decades, technological advances on cocoa Preza et al., 2010), antimicrobial (Smullen et al., 2007) and antiviral
cultivation did not accompany the increasing consumption rate, activities (Kamei et al., 2016) of cocoa products. However, the
and international demand has raised socio-environmental con- applicability of cocoa’s residual biomass has only been slightly
cerns, which are now attracting the interest of the various actors studied. These bio-compounds or value-added molecules can be
in the cocoa production and supply chain. Recently, greater inter- obtained by bioconversion and extraction. Fig. 2 summarizes the
est has been given to the use of cocoa by-products. In 2017, the main products and bio-compounds obtained through both routes
value of exported cocoa shells, husks, skins and other cocoa waste using the residual biomass from the cocoa production chain.
was approximately US$ 244 million, with Côte d’Ivoire, Sierra Extraction is a simple and inexpensive technique for the
Leone, and the Netherlands as the main exporting countries. In removal of organic compounds of interest by the use of solvents
the same year, Spain, the Netherlands and Malaysia were the main that allow facilitated diffusion. Although the low cost initially
importers (International Trade Center, 2019b). These figures sug- seems attractive, the extensive generation of toxic wastes and
gest that companies around the world are taking advantage of costly treatment of the effluents made this practice undesirable
these residual materials to develop various products on an over the years. Bioconversion technology can be defined as the
industrial scale (e.g., feed and complements for animal nutrition, transformation of biomass (i.e., plant or animal residues) into prod-
fertilizers). Similar successful cases of industrial exploitation of ucts or compounds of high added value through microbiological or

Fig. 2. Main products and bio-compounds obtained from cocoa residual biomass.
76 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83

Table 1
Cocoa by-products for biomolecules and compounds production using chemical extraction.

By-product Extract/Fraction Application Outcome Refs.

Bean shell Methanolic extracts Functional food Extracts showed a protective activity to ischemic damage; (Arlorio et al.,
the bioactive compounds are polymeric polyphenols (e.g. 2005)
procyanidins).
Bean shell Ethanol extract Antimicrobial potential Mouth rinse (final concentration of 1 mg/mL in 0.1%) with (Badiyani et al.,
antimicrobial activity, highly effective reducing 32.25% S. 2013)
mutans counts in contaminated toothbrushes.
Bean shell Supercritical carbon Food industry Theobromine and caffeine (Brunner et al.,
dioxide extract 1992)
Bean shell Cocoa bean shell Environmental decontamination Natural adsorbent to entrap pollutants such as heavy metal (Fioresi et al.,
powder ions, gases or industrial dye. 2017)
Bean shell Acetone: ethanol Dental health The extracts showed 2 and 12 times higher inhibitory activity (Kim et al., 2004)
extract against glucosyltransferase and similar polyphenol content
compared to two other commercially available products.
Bean shell Dietary fiber Antioxidant potential Product with intrinsic antioxidant activity and physico- (Lecumberri et al.,
chemical properties similar to commercial dietary fiber. 2007)
Bean shell Ethanol extract In vitro and in vivo antimicrobial ; Streptococcus mutans total count and plaque deposit when (Matsumoto et al.,
activity used as mouth rinse on 68% of the tested subjects 2004)
Bean shell Acetone extract Antimicrobial activity ; Minimum inhibitory concentration against E. coli, (Nsor-Atindana
Staphylococcus aureus, Salmonella and Bacillus cereus et al., 2012)
Bean shell Ethanol extract Antimicrobial and anti- Decrease of the growth rate of the streptococci strains; (Ooshima et al.,
glucosyltransferase activity reduced the synthesis of insoluble glucan through the action 2000)
of glucosyltransferase enzyme.
Bean shell Cocoa bean shell Precursor of binderless carbon Carbon monolith, that when is activated, count with a higher (Plaza-Recobert
powder monoliths micro-pore volume and good mechanical performance. et al., 2017)
Bean shell 0.1% cocoa bean extract Antimicrobial activity Cocoa bean husk extract mouthrinse can be used in children (Babu et al., 2011)
as an alternative to chlorhexidine mouthrinse as it has
similar antimicrobial properties and evades the side effects of
the latter.
Bean shell, pod Dietary fiber Antioxidant potential " Cocoa pod husk antioxidant activity with significantly (Martínez et al.,
husk and pulp higher total phenolic content on methanol: ethanol extract 2012)
when compared with other by-products
Pod husk Ethanol extract Antioxidant potential " Antioxidant activity and collagenase inhibition activity (Karim et al.,
2014)
Pod husk NaOH extract Antiviral, antibacterial and Anti-HIV, anti-Influenza activity and enhancement of vitamin (Sakagami et al.,
radical scavenging C radical scavenging 2008)
Pod husk Organic extract Potassic fertilizer " dry mass of the aerial parts (Sodré et al., 2012)
Pod husk Pectin Highly acetylated pectin forms Suggest the use of pectin from cocoa pod husk as a gelling or (Vriesmann et al.
gel thickening additive (2011))
Pod husk Dietary fiber Antioxidant activity " Non-starch polysaccharide and total phenolic content (Yapo et al., 2013)

enzymatic processes. Although microbial bioconversion was environmental conditions, plagues and mechanical damage. CPH
employed as early as 6000 B.C. in the production of wine, cheese is obtained after the removal of the beans and represents 70–80%
and bread (Legras et al., 2007; Nielsen, 2002; Salque et al., 2013), in dry weight of the fruit (Prabhakaran, Prabhakaran Nair,
only after the 18th century, with the industrial revolution and 2010a), which implies a wide area for its disposal and a serious
the homologation of microbiology as a branch of science, the use challenge in waste management.
of microorganisms become pragmatic. The chemical composition of CPH is summarized in Table 2. CPH
The by-products cocoa pod husk (CPH), cocoa bean shell (CBS) has a lignin-rich composition, non-starch polysaccharides (cellu-
and cocoa sweatings (CS) have been commercially and industrially lose, hemicelluloses and pectin), terpenoids (crysoplenol), flavo-
explored through research and patent development to take advan- noids kaempferol derivatives, rhamnetin), phenolic and
tage of their complex compositions. As shown in Tables 1 and 3, carboxylic acids (protocatechuic acid, salicylic acid, citric acid
the results of recent studies on these materials’ biotechnological and tartaric acid) and some free amino acids (glutamine, asparagi-
potential are broad and involve various applications. As an exam- nes, serine and lysine) (Adomako, 1972; Donkoh et al., 1991; Osei
ple of industrial interest in one of the cocoa by-products, Table 4 et al., 1991; Serra Bonvehí and Ventura Coll, 1999). Serra Bonvehí
presents a brief list of patents related to the use of CBS, one of and Ventura Coll (1999) evaluated CPH samples from fruit grown
the most exploited cocoa by-products. The registration and legal in Côte d’Ivoire, Nigeria, Cameroon, Colombia, Ecuador, Guinea
protection of the knowledge developed around cocoa by-product and Brazil. The study showed that the amount of protein ranges
exploration are essential and relevant. Thus, this residual biomass from 12.5 to 17.60 g 100 g of CPH
1. The amounts of several free
has been used to develop new processes applied to the food, cos- amino acids, lipids and total free sugars and starch were on average
metic, pharmaceutical and biomaterial industries. In the following 315 mg, 3.0 g and 2.8 g 100 g of CPH
1, respectively (Serra Bonvehí
sections, some studies related to the chemical composition of these and Ventura Coll, 1999). Recently, Vriesmann et al. (2011) investi-
by-products (cocoa pod husk, cocoa bean shell and cocoa ‘‘sweat- gated the composition of CPH from crops in northeastern Brazil.
ings”) and potential applications will be described. This study demonstrated that ions of calcium, iron, potassium,
and sodium are found in significant concentrations (mg 100 g of
5.1. Cocoa pod husk CPH
1), and ions of copper, magnesium, selenium and zinc are
found as trace elements (mg Kg of CPH
1).
The CPH is the outer part of the fruit (exocarp) and is rough, Many farmers opt to discard this biomass in the soil or burn it.
oval-shaped and relatively thick. It displays a diversity of colors Under favorable climatic conditions, CPH may become a reservoir
(depending on cocoa species), which promotes protection from of undesirable fungi pathogens, such as Marasmius perniciosus, Phy-
 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83 77

Table 2
Chemical composition of cocoa pod shell (g100 g
1 dry matter), bean shell (% dry matter), and sweatings (%).

Compounds Cocoa by-product References

Pod Husk Bean shell Sweatings
Carbohydrates 29.04–32.3 17.8–23.17 10.7–68.35 (Anvoh et al., 2009; Dias et al., 2007; Gyedu, 2001; Igbinadolor, 2009;
Martínez et al., 2012; Schwan and Wheals, 2004; Vriesmann et al., 2011)
Cellulose 24.24–35.0 15.1 – (Grillo et al., 2019; Mansur et al., 2014; Ofori-Boateng and Lee, 2013)
Hemicellulose 8.72–11.0 – –
Lignin 14.6–26.38 32.41 – (Lecumberri et al., 2007; Mansur et al., 2014; Ofori-Boateng and Lee,
2013; Vriesmann et al., 2011)
Total proteins 4.21–10.74 15.79–18.1 0.41–5.56 (Anvoh et al., 2009; Arlorio et al., 2001; Gyedu, 2001; Igbinadolor, 2009;
Lecumberri et al., 2007; Martínez et al., 2012; Nsor-Atindana et al., 2012;
Ofori-Boateng and Lee, 2013; Vriesmann et al., 2011)
Lipids 1.5–2.24 2.02–6.87 1.91–3.54 (Anvoh et al., 2009; Arlorio et al., 2001; Lecumberri et al., 2007; Martínez
et al., 2012; Nsor-Atindana et al., 2012; Prabhakaran Nair, 2010b;
Vriesmann et al., 2011)
Pectin 6.1–9.2 4.7–6.0 0.57–1.5 (Anvoh et al., 2009; Arlorio et al., 2001; Dias et al., 2007; Mansur et al.,
2014; Prabhakaran Nair, 2010b; Schwan, 1998; Vriesmann et al., 2011)
Ash 6.7–10.02 5.96–11.42 3.7–7.68 (Anvoh et al., 2009; Igbinadolor, 2009; Lecumberri et al., 2007; Mansur
et al., 2014; Martínez et al., 2012; Nsor-Atindana et al., 2012; Ofori-
Boateng and Lee, 2013; Prabhakaran Nair, 2010b; Vriesmann et al., 2011)
Total dietary fiber 36.6–56.10 18.6–60.6 16.89 (Arlorio et al., 2001; Lecumberri et al., 2007; Martínez et al., 2012;
Prabhakaran Nair, 2010b; Vriesmann et al., 2011)
Organic acids (mg L
1) – – (Anvoh et al., 2009)
Malic acid – – 3.6
Lactic acid – – 1.23
Oxalic acid – – 1.27
Citric acid – – 9.14
Acetic acid – – 2.28
Theobromine 0.34 1.3 – (Arlorio et al., 2001; Ofori-Boateng and Lee, 2013; Prabhakaran Nair,
2010b)
Caffeine – 0.1 – (Prabhakaran Nair, 2010b)
Total phenolics* 4.6–6.9 1.32–5.78 – (Arlorio et al., 2001; Lecumberri et al., 2007; Lessa et al., 2018; Lu et al.,
2018; Vriesmann et al., 2011; Yapo et al., 2013)
**
Anthocyanins – 0.4 – (Lessa et al., 2018)
Tannins 5.2 3.3–4.46 – (Lecumberri et al., 2007; Prabhakaran Nair, 2010b; Yapo et al., 2013)
Flavonols** – 1.5 – (Lessa et al., 2018)
Minerals (mg 100 g
1 dry matter) – (mg L
1)
3230.85 – 1297.07 (Anvoh et al., 2009; Vriesmann et al., 2011)
Ca 254.0 – 171.5
Cu 6.18 – –
Fe 5.8 – –
K 2768.0 – 950.0
Mg 110.9 – 82.5
Mn 35.72 – –
Na 10.5 – 30.5
P – – 62.47
Se 0.01 – –
Zn 39.74 – –
*
(g Gallic Acid Equivalent/100 g).
**
(mg quercetin/100 g cocoa shell).

Table 3
Current strategies for biotransformation of cocoa by-products.

By-product Fermentation Product Microorganism Reference

Pod husk Solid state Feedstuff for livestock Pleurotus ostreatus (Alemawor et al., 2009)
Pod husk Solid state Fructosyltransferase Rhizopus stolonifer (Lateef et al., 2008)
Pod husk Semi-solid Xanthan gum Xanthomonas campestris (de Diniz and Druzian et al., 2012)
Sweatings Solid state Lipase Aspergillus niger (Amorim et al., 2012)
Sweatings Submerged Cocoa wine S. cerevisiae (Dias et al., 2007)
Sweatings Submerged Fruit wine S. cerevisiae (Duarte et al., 2010)
Sweatings Submerged Cocoa beverage Kefir grains (Puerari et al., 2012)
Sweatings Submerged Alcoholic beverage S. cerevisiae, Psilocybe mexicana, Candida carpophila (Takrama et al., 2015)
and Khodamaea ohmeri

tophthora palmivora and P. megakarya. The Phytophthora spp. are the devastating witches’ broom fungus (Moniliophthora perniciosa),
responsible for pod rot, or black pod, a disease that affects suscep- which killed thousands of trees and significantly reduced almond
tible cocoa plant genotypes, causing small dark lesions on the pod production for almost two decades. It is believed that one of the
that spread rapidly over the fruit’s surface and internal tissues (i.e., causes of this phytosanitary problem was the inadequate disposal
beans and pulp) (Guest, 2007). In the 80s, Brazil faced the spread of and management of cocoa waste. The incorrect disposal of CPH
78 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83

Table 4 the presence of theobromine, which is considered a detrimental

Patents related to use of cocoa bean shell. compound in animal nutrition (Alexander et al., 2008). Taking into
Code Application Reference account this fact, CPH could be a valuable source of dietary fiber,
CN100394860C Extract of cacao bean husk with (Jingxuan et al., which, combined with other properties, can transform this by-
inhibitory effects on carcinogenesis. 2008) product in an attractive complementary nutrition source for ani-
EP2174557A1 A food comprising at least 30 mass % (Brandstetter mals (Adomako, 1972; Donkoh et al., 1991 Osei et al., 1991).
alkalized cocoa shells based on the et al., 2008) CPH molecules with functional activity have been identified,
total mass of alkalized cocoa shells
and cocoa powder in the food.
extracted and tested in various studies through the application of
ES2539845B1 Procedure and synthesis of activated (Alcañiz, 2015) chemical techniques of extraction or the use of biotechnological
carbon monoliths from cocoa husk tools. Some of these molecules are phenols, flavonoids and
US4908212 Chewing gum designed to prevent (Kwon et al., terpenoid-derived metabolites. Moreover, research has proven that
tooth decay, for which a cacao bean 1990)
CPH is a potential source of renewable energy and can improve
husk is extracted.
JPH06125710A Cocoa husk extract with cocoa (Masanori et al., wastewater treatment.
flavor. 1992) It has been verified a rich diversity of phenolic compounds
RU2392954C2 Theobromine-enriched or (Bradberi and retained in CPH lignin fraction, which shows high antimicrobial
polyphenol-enriched composition Kopp, 2005) and antiviral activities due to a sum of physic-chemical factors
extracted from cocoa bean pod.
(e.g., higher solubility, optimal molecular size). Some cocoa husk
US006159451A A manufacturing process of (Kim et al.,
glucosyltransferase inhibitors from 2000) components showed promising results when tested against HIV-
cocoa bean shell. 1 virus in in vitro MT-4 cells assay (Sakagami et al., 2008). Consid-
US20100040734A1 Water-soluble dietary fiber. (Nakamura ering the high mutation rate and resistance to pathogens, these
et al., 2010)
findings are important because of the urgent necessity of screening
US20120318176A1 Cocoa husk as a raw matter to (Gotou et al.,
develop a burned material and a 2008) antimicrobial compounds from new sources (e.g., plants and fungi
heat conducting material. metabolites) for various applications.
US4532147A Tasteless and odorless colorant (Jonas et al., CPH has also been used in the food, pharmaceutical and cos-
material extracted from cocoa bean 1985) metic industries as a pectin source. Pectin, which is present in high
shell.
quantities in CPH, is a complex polysaccharide that is known for its
US6743450B2 Extraction of sterols from cocoa (Romanczyc
hulls. and McClelland, gelling properties. Several studies have identified considerable
2011)) concentrations of pectin in CPH and analyzed various extraction
WO2012130278A1 Tea made of cacao bean peels, the (Marcolini, conditions and its chemical, physicochemical and antimicrobial
method for producing same, and to 2011)
properties (Table 2).
the uses thereof in pharmaceuticals,
cosmetics, and food.
According to Karim et al. (2014), the chemical composition of
cocoa pod extract allows it to inhibit the action of some enzymes
that are responsible for skin aging since its high concentration of
antioxidant compounds. The obtained extract showed a higher
may compromise the next harvest’s crop quality and plant health, diversity of flavonoids and terpenoid-derived metabolites when
generating a significant economical deficit. In nature, the decom- compared to the pine bark extract, which is a common ingredient
position of CPH occurs when it is exposed to physical, chemical in cosmetic products. The same authors analyzed CPH extract’s
and biological factors. Physical factors are generally temperature inhibition effect on the enzymes elastase, collagenase (associated
and light exposure, and the chemical factor is basically moisture. with skin aging) and tyrosinase (implicated in wrinkle formation)
Decomposing microorganisms, such as bacteria and fungi, repre- and on the absorption of UV light. The results showed a high inhi-
sent the biological factors. Bacteria have less effect in the case of bition of collagenase and a significant absorption of the UVB light
decomposing plant residues due to their difficulty in digesting cel- frequency (10–380 nm).
lulose, hemicelluloses and lignin. Therefore, fungi are the most The use of agro-industrial waste biomass is increasing as an
common and capable biological factor in the decomposition of alternative to non-renewable energy sources and as an origin of
these complex structures, using them as a nutritional source. As valuable chemicals, requiring analysis for direct combustion,
demonstrated by Rahim et al. (2015), several fungus species colo- pyrolysis and anaerobic digestion. In their work, Syamsiro et al.
nize and decompose plant stems in cocoa crops. Therefore, the pro- (2012) used CPH as a source of renewable energy and analyzed
duction of high-value-added bioactive compounds by in natura its behavior in a chamber. Milled husks were carbonized at
microflora could be an interesting strategy for the use of CPH in 400 °C for 2 h, resulting in a higher heating value (17 MJ kg
1) with
bioconversion processes (Table 3). high ash content. Ofori-Boateng and Lee (2013) assayed CPH as a
A practical and easy alternative for farmers is the use of cocoa solid base catalyst for the transesterification of soybean oil into
waste in soil fertilization considering the husks’ high concentration biodiesel. According to this study’s results, potash from CPH could
of minerals. Sodré et al. (2012) conducted a study to characterize be a viable base catalyst and can generate high yields in biodiesel
the resulting organic extract compost from CPH and assess of the production, providing better engine performance similar to petro-
extract’s applicability as a potassium fertilizer for the soil in cocoa leum diesel. In a study by Khanahmadi et al. (2015), CPH was used
seedling growth. The researchers found that it is feasible to use the for lipase immobilization through cross-linking enzyme aggregate
extract obtained from CPH as a source of potassium at a concentra- technology. The results revealed that the immobilized enzyme was
tion of 391.6 mg of K dm
3 in the soil, resulting in a significant a potential catalyst for biodiesel production by transesterification
increase in the size of seedlings due to the potassium contained of Jatropha curcas oil. Moreover, Mansur et al. (2014) produced use-
in the extract. ful chemicals, such as ketones, carboxylic acids, aldehydes, furans,
Another common application of CPH is livestock feeding as an heterocyclic aromatics, alkylbenzenes, phenols and benzenediols,
alternative to the substantial accumulation of waste in cocoa plan- through the conversion of CPH by pyrolysis and catalytic reactions.
tations and its minimal processing requirements (Bonadona et al., CPH’s physical and chemical properties are potential adsorbing
1963; Braude, 1942). Protein, energy and some micronutrients of agents to remove undesirable compounds in industrial wastewater
CPH make it an ideal addition to animal feed (Nortey et al., treatment. Meunier et al. (2003) found that CPH was efficient to
2015). However, it must be used in low concentrations in view of remove lead from acidic solutions. Bello and Ahmad (2011) tested
 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83 79

CPH as a dye removal agent in textile effluent (remazol brilliant products (Redgwell et al., 2003). Antioxidants are used in food to
black reactive). The pod husk, with a particle size between 1 and protect as dietary supplements to neutralize the adverse effects
2 mm, was activated with reactive orange and carbonized at of oxidative stress (Shahidi, 2015). The antioxidant activity of
500 °C and 700 °C in a second step. The kinetics demonstrated that cocoa by-products (pod husk, bean shell and mucilage) was con-
the material is an effective adsorption agent with a maximum firmed and attributed to the presence of polyphenols (catechin,
adsorption of 111 mg g
1. In the same way, Pua et al. (2013) suc- epicatechin and procyanidin B2) (Lecumberri et al., 2007;
cessfully tested CPH alkaline-treated with NaOH as an adsorbent Martínez et al., 2012). All these beneficial attributes indicate that
to remove methylene blue, another textile dye, from aqueous solu- this product might be of great interest for the food industry, con-
tions. In Krishna’s (2014) work, the CPH was used as a precursor for sidering its potential application as a functional ingredient in con-
activated carbon for dye removal from textile manufacturing fectioneries and baked goods or in the preparation of low-fat, high-
wastewater. The best results were obtained with activated carbon fiber dietetic products (Lecumberri et al., 2007).
produced from CPH, which was chemically activated with ZnCl2 Theobromine is extracted commercially and methylated to form
and further carbonized. Removal levels reached up to 80% in less caffeine, which is in greater demand than theobromine (Prab-
than an hour with pores sizes between 0.25 and 0.5 mm and 0.5 hakaran, Prabhakaran Nair, 2010a). According to Rusconi and
to 1 mm. Conti, (2010), the cocoa fruit (dry and fat-free) has a concentration
of theobromine, in the range of 2.4–3.2 g 100 g
1 and of caffeine
5.2. Cocoa bean shell between 0.3 and 1 g 100 g
1. Zheng et al. (2004), studied the cocoa
fruit at various growth stages, finding that the major purine alka-
CBS is obtained after the separation of the seed during the pro- loid in young small fruits (mainly in pericarp or cocoa bean shell)
cessing step of winnowing, and this residual biomass is usually dis- was theobromine (0.7 mmol g
1 fresh weight), followed by caffeine
carded or sold as agricultural mulch. It is composed of a lignin- (0.09 mmol g
1 fresh weight). In their study, Brunner et al. (1992),
cellulosic complex particularly rich in dietary fiber (18–60%) and through the use of a carbon dioxide extraction technique, detected
other components that are described in Table 2. CBS residue has theobromine (1.2 wt%) and caffeine (0.12 wt%) in CBS.
been studied in the last few years due to its chemical composition
and wide range of potential uses in various industries, such as
5.3. Cocoa sweatings
chemical, food, environmental, and human health. Traditionally,
CBS has been applied in gardening as a raw material in mulch
Visually, pulp or mucilage is characterized by a white mass that
(The International Cocoa Organization, 2003) considering its long
surrounds the cocoa beans. During the post-harvest process, this
decomposition process, acting as a humus-forming base. However,
mass releases a turbid liquid called cocoa pulp juice or ‘‘sweating”
because of its chemical composition and structural features, signif-
(CS) (Oddoye et al., 2013). The mucilage layer is removed by the
icant potential applications for CBS are observed in environmental
action of microorganisms (yeasts and acidophilus bacteria) present
decontamination, food additives and human health (Table 4).
in the fruits and processing sites (Escalante et al., 2013; Oddoye
Studies related to the environment have revealed some of the
et al., 2013). This process generates a range of microbial-derived
characteristics of CBS, such as adsorption capacity, high degree of
metabolites, which diffuse into the seeds and have an impact on
porosity, mechanical stress and low ash content (Adegoke and
the final cocoa quality (Endraiyani et al., 2017).
Bello, 2015). These characteristics are interesting for its use as a
During the fermentation process, approximately 100–150 L of
lignocellulosic precursor of binderless carbon monoliths, with a
CS per ton of wet cocoa almonds is generated (Oddoye et al.,
higher micro-pore volume and good mechanical performance
2013). The inappropriate disposal of this material contaminates
(Plaza-Recobert et al., 2017) or as an efficient raw material to fab-
the soil and waterways, becoming a threat to the cocoa crop due
ricate a low-cost adsorbent to entrap pollutants, such as heavy
to the high risk of infestation by plagues (Dwapanyin et al.,
metal ions, gases or industrial dyes (Fioresi et al., 2017). CBS has
1991). Similar to other cocoa by-products, the CS has great poten-
also been assayed as a fuel due to its calorific value (approximately
tial to be employed as a rich medium for the development of
7400–8600 BTU), which is slightly superior to that of wood (Prab-
microorganisms of industrial interest. CS had a rich composition
hakaran, Prabhakaran Nair, 2010a), and could be considered an
of sugars and minerals, physical and chemical characteristics and
environmentally friendly source of alternative energy.
absence of alkaloids and other toxic substances (Table 2). For
Regarding human health, it has been demonstrated that frac-
example, Adomako (1972) demonstrated that the CS can be an
tions and extracts of CBS show positive properties, such as inci-
alternative source of commercial pectin similar to those extracted
dence reduction of chronic diseases (viz., obesity, diabetes, and
from apples and lemons. CS has also been tested to produced alco-
cancer) (DeVries, 2003; Kris-Etherton et al., 2002), more control
holic beverages with standard levels of volatile compounds (i.e.,
in eating disorders (Bessesen, 2001; Johnson, 2004) and protective
higher alcohols, esters and aldehydes), low concentration of
activity against ischemic damage in human cells (Arlorio et al.,
methanol and high acceptability concerning aroma and general
2005). Other studies have been carried out to verify the effective-
acceptability compared to that of other fruit wines (Table 3)
ness of CBS extracts in dental health due to their biological func-
(Takrama et al. 2015; Igbinadolor, 2009; Dias et al., 2007; Duarte
tions against glucosyltransferase (GTF) (Kim et al., 2004;
et al., 2010). Other products generated from CS (i.e., carbonated
Matsumoto et al., 2004; Ooshima et al., 2000; Osawa et al., 2001)
and kefir beverages, marmalade) displayed high acceptability and
and antimicrobial activity (Babu et al., 2011; Badiyani et al., 2013).
a nutritional value equivalent to that of commercial brands
The growing demand for natural products is driving the food
(Afolabi et al., 2015; Anvoh et al., 2009; Escalante et al., 2013;
industry to invest in by-product recovery to obtain dietary fiber,
Puerari et al., 2012). However, more studies on product develop-
antioxidants, flavorings and preservatives (Guerrero et al., 2008).
ment are needed to elucidate the visibility, acceptance and com-
The dietary fibers (DF) consist of polysaccharides, lignin and
mercial value of CS products.
related substances that are resistant to hydrolysis by human
enzyme action. Some studies demonstrated significant DF content
in CBS (Lecumberri et al., 2007; Martínez et al., 2012). The interest 6. Conclusions and future perspectives
in functional foods and the focus on potential health benefits of
elevated DF levels in the human diet invite the speculation that This review showed that cocoa pod husks, bean shells and
CBS could provide a ready source of inexpensive DF in chocolate sweatings have great potential as raw matters for extraction and
80 Z.S. Vásquez et al. / Waste Management 90 (2019) 72–83

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