Cocoa-laden cadmium threatens human health and cacao economy: A critical view

Highlights

• Environment and cultivars of cacao influence bioconcentration of Cd in beans.

• Trophic Cd transfer to chocolates causes serious global concern in food safety.

• Chronic exposure to Cd results in organ dysfunction, cancers and mortality.

• Aged cacao forms, crop losses and poor maintenance impede sustainable cacao farming.

• Low Cd-uptake cacao clones and site-specific research are therefore greatly warranted.

Abstract

In the recent decades, Cd burden in cocoa-based products threatened global food safety, human health and the future of chocolateries. Increased Cd bioavailability is an acute problem in cacao-based horticulture. Poverty, poor maintenance, unjustified traditional farming, and paucity of knowledge on Cd-binding propensity in cacao discourage the application of risk-mitigation measures. Progressive accumulation of Cd, with a half-life of 10–30 years, in the human body even at ultra-trace levels may lead to serious health complications. If Cd accumulates in the food chain through cocoa products, consequences in children, who are the primary consumers of chocolates, include morbidity and mortality that may result in a significant demographic transition by the year 2050. Developing cacao clones with an innate capability of taking up low Cd levels from soils, and site-specific Cd-cacao research might contribute to limiting the trophic transfer of Cd. This review highlights the possible routes for Cd uptake in cacao plants and discusses the measures to rescue the chocolateries from Cd pollution to promote “healthy” cacao farming. The potential human health risks of chocolate-laden Cd and mitigation strategies to minimize Cd burden in the human body are also presented. The challenges and prospects in Cd-cacao research are discussed as well.

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.