ReviewCocoa-laden cadmium threatens human health and cacao economy: A critical view
Graphical abstract
Introduction
Seeds of Theobroma cacao (Malvaceae family), called cacao beans, are often used to make chocolate liquor, cocoa solids, cocoa butter and chocolates. Côte d'Ivoire, Ghana, Indonesia, Ecuador and Cameroon are the principal cocoa-producing countries in the world (FAO, 2015) (Fig. 1a), and 68% of world's cocoa comes from Africa, while Asia/Oceania and Americas contribute 17 and 15%, respectively (Beg et al., 2017) (Fig. 1b). The region-wise cacao bean consumption is: Europe (48%), North America (25%), Asia and Oceania (15%), South America (9%) and Africa (3%) (Fig. 1c). In Côte d'Ivoire, the world's largest cocoa producer, cacao bean yield has been substantially increased by >48% in the last five years. Thus, the productivity of cacao beans in this country increased from ~1.5 million metric tons (MMt) in 2012–2013 to 2.1 MMt in 2018–2019 which implies the greater demand for cocoa (Wessel and Quist-Wessel, 2015; Shahbandeh, 2019). As indicated in Fig. S1, the two terms, ‘cacao’ and ‘cocoa’, have been specifically used throughout the text since both are interchangeably used in the literature.
Currently, the serious global concern is the presence of trace metals in cacao tissues and consequently in cocoa products, and their effects on human health. In the recent past, several investigations revealed the accumulation of arsenic (As), bismuth (Bi), chromium (Cr), cadmium (Cd) and lead (Pb) in cacao beans and pod husks as well as products of cocoa (Huamaní-Yupanqui et al., 2012; Villa et al., 2014; Chavez et al., 2015; Bertoldi et al., 2016; Barraza et al., 2017), and this perilous situation alerts to think about human health-risk and food safety. Cd is a non-essential, invasive and highly toxic trace metal that readily accumulates in the edible parts of cacao and pose serious health problems upon ingestion of Cd-containing cocoa products (Barraza et al., 2017). Therefore, Cd elicits problems in cocoa irrespective of any geographic origin such as Africa (Odoh et al., 2019), South America (Pereira de Araújo et al., 2017), Central America (Gramlich et al., 2018) and Asia (Bertoldi et al., 2016), indicating that there is a strong link between cacao plants and Cd availability throughout the globe (Fig. 2), and multiple factors might be responsible for the appearance of Cd in cacao tissues including beans.
Cd tends to accumulate in the body, and chronic exposure at even low levels may result in serious health consequences (WHO, 2007; Tchounwou et al., 2012) due to its biological half-life of 10–30 years (Alissa and Ferns, 2011). Exposure to even trace quantitites of Cd is a severe problem in children. Since children are often the major consumers of chocolates, cocoa products can be an immediate source of Cd to them. There is a high Cd intake even in adults through food in countries consuming large number of cocoa products. For instance, the top three European Union (EU) importers of cacao beans (in € million) are Netherlands (1597), Germany (490) and Belgium (434) (EU, 2010), and the corresponding range of Cd intake values (μg week−1) are 150–200, 100–150 and 0–50, respectively (WHO, 2007). There is a high-level of organ dysfunction (e.g., kidney failure) by Cd poisoning because of its severe toxic effects on body tissues and function (Godt et al., 2006; Szefer and Nriagu, 2007; Jarup and Akesson, 2009). In view of the harmful impacts on human health, environment and food quality (Kabata-Pendias, 2011), there exists a growing global concern about Cd, and this drives to list Cd as one of the priority pollutants by many international organizations. Likewise, EU, International Agency of Research on Cancer (IARC), and United States Environmental Protection Agency (USEPA) have recognized Cd as Category 1B, Group 1, and Class B carcinogenic metal, respectively (Barraza et al., 2017), consequently drawing the attention of researchers towards Cd and its toxicity.
It is very clear from the above that the cocoa industry is in deep trouble with formidable challenges like food safety and human health risk. Although these issues have been investigated practically and addressed theoretically, yet some gaps remain that hinder the growth and sustainability of cocoa industry. So far, research devoted in this direction unveiled the riddle of cacao-Cd linkage. Thus, cocoa content and Cd concentrations in chocolates were compared (Villa et al., 2014). Under cacao farming, soil amendments were evaluated for the restoration of Cd-contaminated soils (Chavez et al., 2016a). The impact of Cd speciation (Chavez et al., 2016b) and areas of oil activities (Barraza et al., 2017) have also been investigated to evaluate the plant-available Cd. Recent studies highlighted the heavy metal absorbing propensity of cacao (Arévalo-Gardini et al., 2017), linkage between soil Cd and cacao Cd (Chavez et al., 2015; Gramlich et al., 2018), and conventional and organic management techniques versus Cd uptake by cacao (Gramlich et al., 2017; Arguello et al., 2019).
Recent reviews focused on Cd bioavailability and uptake by plants (Shahid et al., 2016), the role of Cd-resistant plant growth-promoting rhizobacteria in minimizing plant-Cd (Sharma and Archana, 2016), and risks associated with Cd in cacao beans and cocoa-based foods (Anyimah-Ackah et al., 2019). Nonetheless, there is no detailed information to figure out the complex linkage between Cd and cocoa in order to address several issues: Is Cd sorption an inherent property of cacao tissue? What are the immediately available strategies to mitigate the translocation of Cd into cacao plant? What extent of cocoa-laden Cd threatens human health in the next decade? Do the existing regulations protect human health from Cd associated with cocoa products? How should research be navigated hereafter for sustainable cacao farming? Such unanswered questions not only threaten global health, but also impede the cacao economy (ICCO, 2014). These unresolved issues prompted us to consolidate the recent information, for the first time, from a critical perspective that could be of immense use to the researchers and cacao farmers. The present review thus provides comprehensive information on Cd uptake propensity of cacao, emphasizes the need for ‘organic cacao farming’, and highlights the effect of Cd in cocoa products on human health in the immediate future. In addition to outlining challenges and future directions of cacao research, brief guidelines are proposed for the cocoa producers or chocolate makers to minimize the amount of Cd entering chocolate.
Section snippets
Role of natural and anthropogenic factors in Cd accumulation
Cd is one of the most phytoavailable heavy metals that enter the food chain through dietary intake (McKenna et al., 1993; Chen et al., 2019; Hamid et al., 2019; Ismael et al., 2019). Cacao, being a small evergreen tree, has high propensity of Cd uptake (Chavez et al., 2015; Gramlich et al., 2017). Accumulation of Cd in soil and/or cacao bean can be related to many natural factors such as geogenic origin (Arguello et al., 2019), low soil zinc (Vatamaniuk, 2017), soil parent material (Gramlich et
New regulations on cacao/cocoa importing
Due to lack of domestic cocoa production and massive consumption of chocolates (half of world's production), the main destination market for cacao beans is the Europe, which is also a leading cacao bean processor (Fig. S3) with ~50% of the world's cocoa exports (Arguello et al., 2019). The consumption of cacao bean region-wise also indicates that world's leading cacao producer is the lowest cocoa consumer (Fig. 1c). New regulations, set by European Commission (EC), to put cocoa products in the
Trophic transfer of Cd through chocolate-based food
Despite the major proportion of diet-Cd comes from cereals, vegetables, potatoes, shellfish, liver, kidney, oil seeds and certain wild mushrooms (Åkesson and Chaney, 2019), the cocoa-laden Cd (so called Cd in chocolates) threatens the human health due to increasing number of chocolate lovers (Konar et al., 2016) as children are the primary clients of chocolateries (USFDA, 2006; Orisakwe et al., 2019). In the USA alone, the number of craft chocolatiers has been dramatically increased from 7 to
Natural and anthropogenic soil amendments
Minimizing Cd accumulation in plants is vital for better food safety. Though there are many non-essential heavy metals, Cd is the most attracted heavy metal in soil science and plant nutrition due to its potential human toxicity (McLaughlin and Singh, 1999). In view of the relative soil-plant mobility of Cd (David et al., 1995), it is really challenging to mitigate Cd bioconcentration in various categories of vascular plants (including agricultural and horticultural) in the interest of human
Challenges and future directions
Mitigation of Cd pollution in the environment is a challenging issue in the context of human health protection. Although cacao bean production is significantly increasing, challenges for its sustainable market still exist (Fig. S5). Most Cd-mitigation strategies need proper validation for the efficacy of Cd-controlling approaches in cacao in diversified regions and/or environments across the globe besides addressing the contradictory results in this area of research, since certain strategies
Conclusions
This review identifies that Cd in cacao bean is origin-dependent, and local geographical and environmental conditions in tandem with cacao cultivars are the vital factors affecting bioaccumulation of Cd in plant tissues. The use of Cd-contaminated amendments could completely mislead the facet of ‘organic farming’ in this field. Therefore, the use of genetic approaches through the manipulation of a gene encoding Cd-binding protein looks quite promising to clone low Cd-uptake cacao cultivars.
Declaration of competing interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Acknowledgements
NRM and LCG greatly acknowledge the Universidad Técnica de Manabí, Portoviejo, Ecuador, for the facilities and encouragement and their colleagues in the Instituto de Investigación, for their help in literature collection.
References (199)
- et al.
Acid-tolerant microalgae can withstand higher concentrations of invasive cadmium and produce sustainable biomass and biodiesel at pH 3.5
Bioresour. Technol.
(2019) - et al.
Simultaneous mitigation of cadmium and drought stress in wheat by soil application of iron nanoparticles
Chemosphere
(2020) - et al.
Cadmium exposure in the environment: dietary exposure, bioavailability and renal effects
- et al.
Nickel, cadmium and lead phytotoxicity and potential of halophytic plants in heavy metal extraction
S. Afr. J. Bot.
(2017) - et al.
Heavy metal accumulation in leaves and beans of cacao (Theobroma cacao L.) in major cacao growing regions in Peru
Sci. Total Environ.
(2017) - et al.
Soil properties and agronomic factors affecting cadmium concentrations in cacao beans: a nationwide survey in Ecuador
Sci. Total Environ.
(2019) - et al.
Converging farmers' and scientists' perspectives on researchable constraints on organic cocoa production in Ghana: results of a diagnostic study
NJAS – Wagen. J. Life Sci.
(2004) - et al.
Cadmium bioaccumulation and gastric bioaccessibility in cacao: a field study in areas impacted by oil activities in Ecuador
Environ. Pollut.
(2017) - et al.
Distribution, contents and health risk assessment of metal(loid)s in small-scale farms in the Ecuadorian Amazon: an insight into impacts of oil activities
Sci. Total Environ.
(2018) - et al.
Status, supply chain and processing of cocoa - a review
Trends Food Sci. Technol.
(2017)
Multielemental fingerprinting and geographic traceability of Theobroma cacao beans and cocoa products
Food Control
Renal effects of cadmium body burden of the general population
Lancet
Concentration of cadmium in cacao beans and its relationship with soil cadmium in southern Ecuador
Sci. Total Environ.
Chemical speciation of cadmium: an approach to evaluate plant-available cadmium in Ecuadorian soils under cacao production
Chemosphere
Trace element contents in foods from the first French total diet study on infants and toddlers
J. Food Compos. Anal.
Effective methods to reduce cadmium accumulation in rice grain
Chemosphere
Effects of boron, silicon and their interactions on cadmium accumulation and toxicity in rice plants
J. Hazard. Mater.
Selenium reduces cadmium uptake into rice suspension cells by regulating the expression of lignin synthesis and cadmium-related genes
Sci. Total Environ.
Lead, cadmium and nickel in chocolates and candies from suburban areas of Mumbai, India
J. Food Compos. Anal.
Cadmium accumulation and allocation in different cacao cultivars
Sci. Total Environ.
Current context on chocolate flavor development – a review
Curr. Opin. Food Sci.
Chapter 1 - contribution of organic farming towards global food security: an overview
Bacterial mediated alleviation of heavy metal stress and decreased accumulation of metals in plant tissues: mechanisms and future prospects
Ecotoxicol. Environ. Saf.
The impact of contracts on organic honey producers’ incomes in southwestern Ethiopia
Forest Policy Econ.
Cadmium uptake by cocoa trees in agroforestry and monoculture systems under conventional and organic management
Sci. Total Environ.
Soil cadmium uptake by cocoa in Honduras
Sci. Total Environ.
Cadmium exposure and cognitive abilities and behavior at 10 years of age: Aprospective cohort study
Environ. Int.
An explanation of soil amendments to reduce cadmium phytoavailability and transfer to food chain
Sci. Total Environ.
Exogenous malic and acetic acids reduce cadmium phytotoxicity and enhance cadmium accumulation in roots of sunflower plants
Plant Physiol. Biochem.
Governmental and private certification labels for organic food: consumer attitudes and preferences in Germany
Food Policy
Current status of cadmium as an environmental health problem
Toxicol. Appl. Pharmacol.
Jointed toxicity of TiO2 NPs and Cd to rice seedlings: NPs alleviated Cd toxicity and Cd promoted NPs uptake
Plant Physiol. Biochem.
Glutamate alleviates cadmium toxicity in rice via suppressing cadmium uptake and translocation
J. Hazard. Mater.
Organic farming and small-scale farmers: main opportunities and challenges
Ecol. Econ.
Host plant growth promotion and cadmium detoxification in Solanum nigrum, mediated by endophytic fungi
Ecotoxicol. Environ. Saf.
Soil contamination with cadmium, consequences and remediation using organic amendments
Sci. Total Environ.
Burder of cadmium in early childhood: longitudinal assessment of urinary cadmium in rural Bangladesh
Toxicol. Lett.
Improving functionality of chocolate: a review on probiotic, prebiotic, and/or synbiotic characteristics
Trends Food Sci. Technol.
Geochemical associations and availability of cadmium (Cd) in a paddy field system, northwestern Thailand
Environ. Pollut.
Nickel, cadmium and lead levels in raw cocoa and processed chocolate mass materials from three different manufacturers
J. Food Compos. Anal.
Heavy metal (Cu, Zn, Cd and Pb) partitioning and bioaccessibility in uncontaminated and long-term contaminated soils
J. Hazard. Mater.
Chloride salinity reduces cadmium accumulation by the Mediterranean halophyte species Atriplex halimus L
Environ. Exp. Bot.
Intra- and inter-annual variation of Cd, Zn, Mn and Cu in foliage of poplars on contaminated soil
Sci. Total Environ.
Cadmium and lead in cocoa powder and chocolate products in the US market
Food Addit. Contam. B
Metal fractionation in soils collected from selected cocoa plantations in Ogun State, Nigeria
World Appl. Sci. J.
Heavy metal poisoning and cardiovascular disease
J. Toxicol.
Risk assessment of cadmium and chromium from chocolate powder
Food Addit. Contam. B
Associations of cadmium, zinc, and lead in soils from a lead and zinc mining area as studied by single and sequential extractions
Environ. Monit. Assess.
Exposures and risks of arsenic, cadmium, lead, and mercury in cocoa beans and cocoa-based foods: a systematic review
Food Qual. Saf.
Australia New Zealand Food Standards Code - Standard 1.4.1 - Contaminants and Natural Toxicants. Standard 1.4.1 Published in the Commonwealth of Australia Gazette No. P 30 on 20 December 2000. Canberra, Australia and Wellington, New Zealand
Cited by (62)
Environmental cadmium inhibits testicular testosterone synthesis via Parkin-dependent MFN1 degradation
2024, Journal of Hazardous MaterialsThe in vitro metabolism of GMDTC in liver microsomes of human, monkey, dog, rat and mouse: Metabolic stability assessment, metabolite identification and interspecies comparison
2023, Journal of Pharmaceutical and Biomedical AnalysisFoliar application of nanoceria attenuated cadmium stress in okra (Abelmoschus esculentus L.)
2023, Journal of Hazardous MaterialsEffect of fermentation stages on the nutritional and mineral bioavailability of cacao beans (Theobroma cacao L.)
2023, Journal of Food Composition and Analysis