Elsevier

Environmental Pollution

Volume 229, October 2017, Pages 950-963
Environmental Pollution

Cadmium bioaccumulation and gastric bioaccessibility in cacao: A field study in areas impacted by oil activities in Ecuador

https://doi.org/10.1016/j.envpol.2017.07.080Get rights and content

Highlights

  • Cd in cacao beans is enriched 4 times compared to soils contents.

  • Cd bioaccumulates in beans mainly through root uptake regardless of soil pollution.

  • Cd mainly originates from agricultural practices rather than oil activities.

  • In cocoa liquor samples, Cd gastric bioaccessibility is almost 100%.

  • 50% of cacao beans and liquor samples were above the Cd European guidelines.

Abstract

Cacao from South America is especially used to produce premium quality chocolate. Although the European Food Safety Authority has not established a limit for cadmium (Cd) in chocolate raw material, recent studies demonstrate that Cd concentrations in cacao beans can reach levels higher than the legal limits for dark chocolate (0.8 mg kg−1, effective January 1st, 2019). Despite the fact that the presence of Cd in agricultural soils is related to contamination by fertilizers, other potential sources must be considered in Ecuador. This field study was conducted to investigate Cd content in soils and cacao cultivated on Ecuadorian farms in areas impacted by oil activities. Soils, cacao leaves, and pod husks were collected from 31 farms in the northern Amazon and Pacific coastal regions exposed to oil production and refining and compared to two control areas. Human gastric bioaccessibility was determined in raw cacao beans and cacao liquor samples in order to assess potential health risks involved. Our results show that topsoils (0–20 cm) have higher Cd concentrations than deeper layers, exceeding the Ecuadorian legislation limit in 39% of the sampling sites. Cacao leaves accumulate more Cd than pod husks or beans but, nevertheless, 50% of the sampled beans have Cd contents above 0.8 mg kg−1. Root-to-cacao transfer seems to be the main pathway of Cd uptake, which is not only regulated by physico-chemical soil properties but also agricultural practices. Additionally, natural Cd enrichment by volcanic inputs must not be neglected. Finally, Cd in cacao trees cannot be considered as a tracer of oil activities. Assuming that total Cd content and its bioaccessible fraction (up to 90%) in cacao beans and liquor is directly linked to those in chocolate, the health risk associated with Cd exposure varies from low to moderate.

Introduction

Ecuador is ranked as the sixth largest oil producing country in South America and 27th in the world (Ecuador Oil Production, 2016). Since the 1960s, most extraction activities have taken place in the northeastern Amazonian region, while refining occurs in Esmeraldas along the Pacific coast. During operations of the Texaco Oil company (1960s–1992), outdated practices and technologies used for oil production (Buccina et al., 2013) generated millions of gallons of untreated toxic waste, gas and oil, which were partially released into the environment (San Sebastián and Hurtig, 2005). Local populations were and continue to be exposed to a mixture of toxic compounds, such as trace metals and polycyclic aromatic hydrocarbons (PAHs), from water consumption, inhalation of airborne particles or ingestion of contaminated crops.

Although the economy of the country revolves around the oil industry, agriculture is the second most important activity in exportation. Ecuador is currently the fourth largest cacao producer in the world from which 87% is directly exported as cacao beans to Europe, mainly France, Germany and England, as well as to the United States (Anecacao, 2015, ProEcuador, 2013). Theobroma cacao is mostly cultivated in the western part of the country but the growing area now extends to the Amazon region, covering a total area of 433,978 ha. Cacao plantations utilize a wide variety of soils: from clayey highly eroded soils to volcanic sands and silty soils, with pH varying between 4 and 7. Nevertheless, cacao requires depth, well drained and clay loamy soils, with high organic matter content in order to grow in optimal conditions (Quiroz and Agama, 2006).

The cocoa tree, as a plant species, includes a wide range of vastly different varieties. In order to characterize its forms and cultivars, morphological (e.g. flowers), agronomic (e.g. resistance to diseases, fruit shape and grain size) and molecular (e.g. enzymes) properties are frequently used (Dostert et al., 2012). Of all the varieties cultivated in Ecuador, the ‘Nacional fino de aroma’ and CCN-51 are the most appreciated on the international market (Amores et al., 2009, Loor et al., 2009).

However, there is recent international concern regarding the presence of trace metals in cacao tissues. Recent studies have shown that As, Bi, Cr, Cd, and Pb can be accumulated in cacao beans, pod husks, and cacao-based products (Bertoldi et al., 2016, Chavez et al., 2015, Huamani et al., 2012). Among these elements, cadmium (Cd), a non-essential trace metal, seems to accumulate mainly in the edible parts of cacao, which entails potential risks for human health by ingestion of contaminated products. It has been also reported that cacao beans have different Cd concentrations depending not only on the variety but also on the geographical site, with mean concentrations reaching 1.4 mg kg−1 in South America, 0.5 mg kg−1 in East Africa and Central America, 0.3 mg kg−1 in Asia, and 0.09 mg kg−1 in West Africa (Bertoldi et al., 2016).

Indeed, Cd is considered to be one of the most toxic metals that exhibit adverse effects on all biological processes. It reveals very harmful impacts on the environment and food quality (Kabata-Pendias and Szteke, 2015). Based on its carcinogenic effects and, more precisely, the adverse effects observed in the brain, kidneys and bones, the European Union classified Cd and its chlorinated, oxygenated, sulfurated, and sulfate derivatives, into category 1B. Similarly, the International Agency of Research on Cancer (IARC) and the United States Environmental Protection Agency (US EPA) classified Cd into Group 1 and class B, respectively.

In a global context, the major sources of Cd seem to be atmospheric deposition from industries, sewage sludge, and P fertilizers (Kabata-Pendias, 2011). But in Ecuador, Cd can be present in the environment due to natural sources such as volcanic eruptions, which are particularly frequent in the Andes, or the leaching of volcanic rocks, as well as a result of anthropogenic activities including industrial and oil processing (FAO and WHO, 2015). Indeed, it is well known that crude oil can naturally contain metal(oid)s (e.g. As, Cr, Cd, Cu, Co, Ni, Pb, Ti, V, Zn) as a result of the mineral composition of the source rock, or these elements may be added during oil production (e.g. Ba and Mo), refining, transportation, or storage (Fu et al., 2014a, Khuhawar et al., 2012, Lienemann et al., 2007). As a consequence, soils near oil fields can be contaminated by trace metals that are easily transferred to crops (Fu et al., 2014b).

However, to our knowledge, no previous study has investigated the link between Cd bioaccumulation in cacao plants and the proximity of oil production or refinement infrastructures. The Ecuadorian Amazon region houses a vast network of roads, pipelines, and oil facilities (San Sebastián and Hurtig, 2005) that are located close to both large- and small-scale farms, called ‘fincas.’ Along the Pacific coast, the city of Esmeraldas is also exposed to air contamination by organic and inorganic compounds due to emissions from the national oil refinery, while cacao crops are cultivated in the adjacent areas. Even though it is currently well known that cacao tissues can contain high concentrations of Cd, the sources and transfer mechanisms (e.g. by foliar and/or root uptake) and the bioaccumulation processes remain poorly described in the literature and several questions remain unsettled.

It should be noted that 90% of human exposure to Cd for the non-smoking population is related to food products (European Food Safety Agency EFSA, 2012). Cadmium dietary exposure is estimated to about 2.04 μg kg−1 of body weight per week over a lifetime assuming an average life span of 77 years. Within the 20 main groups described in the Foodex (food classification system), vegetables and confectionary products account for 11 and 3% of food exposure to Cd, respectively, and more precisely, cacao beans and chocolate contribute from 4 to 26% and from 15 to 92%, respectively, depending on the consumer's age (European Food Safety Agency EFSA, 2012).

Nevertheless, the determination of the fraction of total Cd concentration that may potentially affect human health after ingestion has not yet been studied in cacao-based products. Beyond the determination of total trace metal concentrations within a given food product, health risk assessments must also consider their gastric bioaccessibility (Caboche, 2009). This parameter indicates the maximum amount of a compound that, after being released from its matrix during digestion, can be absorbed by the human intestinal epithelium and then enter the blood stream (Hu et al., 2013, Intawongse and Dean, 2006, Peixoto et al., 2016).

A large-scale field study in two areas highly impacted by oil activities in Ecuador was therefore conducted in order to determine Cd concentrations in soils from small-scale farms in the northern Amazon region and near the national oil refinery along the Pacific coast. The aims of this study are to (i) investigate if oil activities constitute a real source of Cd contamination in cacao tissues, (ii) better understand the mechanisms of Cd transfer from soils to cacao plants and its potential bioaccumulation in edible parts, and finally (iii) assess the potential health risk involved after ingestion of cacao-based products, taking the gastric bioaccessibility of Cd in raw materials (cacao beans and liquor) into account.

Section snippets

Global localization and site descriptions

Cacao samples and associated soils were collected between 2014 and 2016 in the Ecuadorian provinces of Orellana and Sucumbíos in the northern Amazon region (NAR), close to oil production fields, and in Esmeraldas, along the north Pacific coast (NPC), in a two km radius from the national oil refinery. For comparison, two other provinces were studied: Manabí (MC) in the south of the Pacific coast and Morona-Santiago (MS) in the southern Ecuadorian Amazon. These additional sites were considered

Physico-chemical properties and total Cd contents in soils

As shown in Table 1, soils from the sampling areas are divided into three types according to the USDA classification typically used in Latin America: inceptisols in NAR and its control area (MS); entisols in NPC; and alfisols in the MC control area.

In the MS area, the soil pH varied between 4.15 ± 0.01 and 6.19 ± 0.06 and was more acidic in the first 20 cm. CEC values showed no difference between the first two horizons (0–5 cm and 5–20 cm), varying between 13.2 and 17.5 cmol kg−1, except for

Cadmium bioaccumulation in cacao pods: uptake pathways and influence of external parameters

The mobility of trace metals, including Cd, in soils and their absorption by plants depends on many factors such as soil texture, pH, CEC, organic matter content, total concentrations in the soil, chemical speciation, plant species and varieties, and farming practices (Qasim et al., 2015, Song et al., 2015, Yang et al., 2016). Wang et al. (2012) reported that Cd uptake by plant roots and its transfer to fruits are influenced by soil properties, plant species and varieties, and also by crop

Conclusion

Cadmium distribution in Ecuadorian soils from the Amazon and Pacific coastal regions depends on natural (e.g. soil properties, geochemical background conditions) and anthropogenic (e.g. agricultural practices) factors. Cd concentrations in the first 0–20 cm of soil were typically higher than those in deeper layers, and 39% exceeded the Ecuadorian permissible limit, which suggests anthropogenic sources. Despite its low concentration in most of the study soils, Cd is easily uptaken by roots and

Acknowledgments

The authors would like to thank the French National Agency of Research for the financial aid in the frame of the ANR-MONOIL Project N°ANR-13-SENV-0003-01. We also want to express our gratitude to local small farmers who allowed us to collect samples of their cacao crops, and to the INIAP-Portoviejo engineers for providing us technical information and soil and cacao samples. We sincerely thank the technical team of the GET laboratory for their helpful contribution to the chemical analysis.

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