Cadmium bioaccumulation and gastric bioaccessibility in cacao: A field study in areas impacted by oil activities in Ecuador☆
Graphical abstract
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 During operations of the Texaco Oil company (1960s–1992), outdated practices and technologies used for oil production (Buccina et al., 2013) generated millions of gallons of untreated toxic waste, gas and oil, which were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.
References (97)
- et al.
Multielemental fingerprinting and geographic traceability of Theobroma cacao beans and cocoa products
Food control.
(2016) - et al.
Accounting for the environmental impacts of Texaco's operations in Ecuador: chevron's contingent environmental liability disclosures
Acc. Forum
(2013) - et al.
Morphological, biochemical, molecular and ultrastructural changes induced by Cd toxicity in seedlings of Theobroma cacao L
Ecotoxicol. Environ. Saf.
(2015) - et al.
Concentration of cadmium in cacao beans and its relationship with soil cadmium in southern Ecuador
Sci. Total Environ.
(2015) - et al.
Accumulation of atmospheric deposition of As, Cd and Pb by bush bean plants
Environ. Pollut.
(2015) - et al.
Bioaccessibility, solid phase distribution, and speciation of Sb in soils and in digestive fluids
Chemosphere
(2009) - et al.
Spatial distribution patterns and potential sources of heavy metals in soils of a crude oil-polluted region in China
Pedosphere
(2014) - et al.
Metal concentration and bioaccessibility in different particle sizes of dust and aerosols to refine metal exposure assessment
J. Hazard. Mater
(2016) - et al.
Cadmium uptake by cocoa trees in agroforestry and monoculture systems under conventional and organic management
Sci. Total Environ.
(2017) - et al.
Soil biogeochemistry, plant physiology, and phytoremediation of cadmium-contaminated soils
Bioaccessibility, dietary exposure and human risk assessment of heavy metals from market vegetables in Hong Kong revealed with an in vitro gastrointestinal model
Chemosphere
In-vitro testing for assessing oral bioaccessibility of trace metals in soil and food samples
Trac. Trends Anal. Chem.
Environmental risks of trace elements associated with long-term phosphate fertilizers applications: a review
Environ. Pollut.
Assessing human exposure risk to cadmium through inhalation and seafood consumption
J. Hazard. Mater
Soil contamination with cadmium, consequences and remediation using organic amendments
Sci. Total Environ.
Cadmium in plants on polluted soils: effects of soil factors, hyperaccumulation, and amendments
Geoderma
Effects of different copper fungicide application rates upon earthworm activity and impacts on cocoa yield over four years
Eur. J. Soil Biol.
Inputs of trace elements in agricultural soils via phosphate fertilizers in European countries
Sci. Total Environ.
Study of the factors influencing the bioaccessibility of 10 elements from chocolate drink powder
J. Food Compos. Anal.
Photosynthetic, antioxidative, molecular and ultrastructural responses of young cacao plants to Cd toxicity in the soil
Ecotoxicol. Environ. Saf.
Particle size effects on bioaccessible amounts of ingestible soil-borne toxic elements
Chemosphere
Cadmium accumulation in three contrasting New Zealand soils with the same phosphate fertilizer history
Geoderma Reg.
Oil development and health in the Amazon basin of Ecuador: the popular epidemiology process
Soc. Sci. Med.
Foliar or root exposures to smelter particles: consequences for lead compartmentalization and speciation in plant leaves
Sci. Total Environ.
Metal and metalloid foliar uptake by various plant species exposed to atmospheric industrial fallout: mechanisms involved for lead
Sci. Total Environ.
Foliar heavy metal uptake, toxicity and detoxification in plants: a comparison of foliar and root metal uptake
J. Hazard. Mater
Using DGT to assess cadmium bioavailability to ryegrass as influenced by soil properties
Pedosphere
Bioaccessibility of cadmium in fresh and cooked Agaricus blazei Murill assessed by in vitro biomimetic digestion system
Food Chem. Toxicol.
Toxic trace elements at gastrointestinal level
Food Chem. Toxicol.
Bioaccessibility of arsenic and cadmium assessed for in vitro bioaccessibility in spiked soils and their interaction during the Unified BARGE Method (UBM) extraction
Chemosphere
Regional accumulation characteristics of cadmium in vegetables: influencing factors, transfer model and indication of soil threshold content
Environ. Pollut.
Trace elements in cocoa solids and chocolate: an ICPMS study
Talanta
Assessment of influences of cooking on cadmium and arsenic bioaccessibility in rice, using an in vitro physiologically-based extraction test
Food Chem.
Toxicological Profile for Cadmium. US
EET575 y EET576 Nuevos clones de cacao Nacional para la zona de Manabí (Boletín Divulgativo No. 346)
Asociación Nacional de Exportadores de Cacao-Ecuador
Aprovechamiento de la cascara de la mazorca de cacao como adsorbente
Genetic characterization of the cacao cultivar CCN 51: its impact and significance on global cacao improvement and production
J. Am. Soc. Hortic. Sci.
Validation d’un test de mesure de bioaccessibilité. Application à 4 éléments traces métalliques dans les sols: As, Cd, Pb et Sb (Obtention du grade de Docteur)
Total and extractable nickel and cadmium contents in natural soils
Commun. Soil Sci. Plant Anal.
Avances en investigación del Cd en el cultivo de Cacao en el Ecuador
Ecophysiology of the cacao tree
Braz. J. Plant Physiol.
Vivo validation of the unified BARGE method to assess the bioaccessibility of arsenic, antimony, cadmium, and lead in soils
Environ. Sci. Technol.
Hoja Botánica: Cacao
Trading econ
Monitoreo de calidad del aire en el área de influencia de la Refinería Esmeraldas: Resumen del Monitoreo desde enero 2012 hasta enero 2013
Cited by (71)
The distribution of cadmium in soil and cacao beans in Peru
2023, Science of the Total EnvironmentRevealing the pathways of cadmium uptake and translocation in cacao trees (Theobroma cacao L.): A <sup>108</sup>Cd pulse-chase experiment
2023, Science of the Total Environment
- ☆
This paper has been recommended for acceptance by Dr. Yong Sik Ok.