Gap analysis of nickel bioaccessibility and bioavailability in different food matrices and its impact on the nickel exposure assessment

Highlights

• Allergic reaction to nickel can be provoked even via the alimentary routs.

• Plant-based foods, e.g. legumes and nuts, found to have elevated nickel content.

• Overestimation in nickel exposure occurs using the total nickel content in foods.

• Bioavailable fraction should be taken into account for real exposure estimations.

• Studies on nickel intake through different foods, especially in recent years, are still scarce.

Abstract

The metal nickel is well known to cause nickel allergy in sensitive humans by prolonged dermal contact to materials releasing (high) amounts of nickel. Oral nickel exposure via water and food intake is of potential concern. Nickel is essential to plants and animals and can be naturally found in food products or contamination may occur across the agro-food chain. This gap analysis is an evaluation of nickel as a potential food safety hazard causing a risk for human health. In the first step, the available data regarding the occurrence of nickel and its contamination in food and drinks have been collected through literature review. Subsequently, a discussion is held on the potential risks associated with this contamination. Elevated nickel concentrations were mostly found in plant-based foods, e.g. legumes and nuts in which nickel of natural origin is expected. However, it was observed that dedicated and systematic screening of foodstuffs for the presence of nickel is currently still lacking. In a next step, published studies on exposure of humans to nickel via foods and drinks were critically evaluated. Not including bioaccessibility and/or bioavailability of the metal may lead to an overestimation of the exposure of the body to nickel via food and drinks. This overestimation may be problematic when the measured nickel level in foods is high and bioaccessibility and/or bioavailability of nickel in these products is low. Therefore, this paper analyzes the outcomes of the existing dietary intake and bioaccessibility/bioavailability studies conducted for nickel. Besides, the available gaps in nickel bioaccessibility and/or bioavailability studies have been clarified in this paper. The reported bioaccessibility and bioavailability percentages for different food and drinks were found to vary between <LOD and 83% and between 0 and 30% respectively. This indicates that of the total nickel contained in the foodstuffs only a fraction can be absorbed by the intestinal epithelium cells. This paper provides a unique critical overview on nickel in the human diet starting from factors affecting its occurrence in food until its absorption by the body.

Introduction

Elementary nickel (Ni) plays an essential role in the growth of bacteria, plants and animals. The necessity of the Ni for growth of a bacterium, i.e. Alcaligenes, a cyanobacterium, i.e. Oscillatoria, and a green alga, i.e. Chlorella vulgaris, has been proven (Welch, 1981). Furthermore, some pine tree species require Ni for their optimum growth (Welch, 1981). Nickel occurs as a structural component in urease and hydrogenase enzymes involved in the nitrogen fixation in legumes (Lavres, Castro Franco, & de Sousa Câmara, 2016). Thus, nitrogen fixating plants, e.g. soybeans, alfalfa and peanuts, have a high level of naturally occurring Ni. Nickel can also be found in almost all organs of vertebrates (Anke, Groppel, Kronemann, & Grun, 1984). Nickel deficiency may lead to lower life expectancy of the reproducing animals as well as development of anemia through reducing the iron resorption. It can also accelerate parakeratosis-like damages through disturbing calcium incorporation in the skeleton (Anke et al., 1984). However, these deficiency symptoms have not yet been observed in animals and humans since the Ni administered by their body always exceeded the requirements, i.e. 25 to 35 μg/day/person (Anke, Angelow, Glei, Müller, & Illing, 1995). Excess intake of Ni can result in Ni dermatitis in sensitive individuals (Anke et al., 1995). This can occur either via exogenous, i.e. skin contact, or endogenous, i.e. oral and inhalation, exposure. Worldwide prevalence of the dermal Ni sensitivity, i.e. Ni allergy, for adults and children is around 8.6%. The Ni allergy affects females 3–10 times more than males due to their regular daily contact with jewelries and garments. Prevalence of Ni allergy among young females can even increase up to 17% (Torres, Das Graças, Melo, & Tosti, 2009).

Public health agencies are concerned about the presence of essential and toxic trace elements in the diet of the worldwide population. Among different routes of the exposure to the trace elements, e.g. skin contact, oral and inhalation, alimentary routes are the predominant pathway of the trace elements to reach the human body (Aung et al., 2006, EFSA, 2015). Toxic trace elements such as Cd, Pb and Hg were initially in the focus of public health policies since they pose a risk for human health. Thus, these toxic trace elements have been included in legislation and are now monitored in foods. Other trace elements like Ni have recently become the focus of concern as the European Food Safety Authority (EFSA) recently stated that the current level of acute exposure of the population to Ni via alimentary routes may increase the risk of eczematous flare-up skin reactions to occur for Ni sensitized individuals (EFSA, 2015).

A range of different food products and multiple sources of contamination of Ni to food have been reported (Noël et al., 2012). It has been shown that tofu, dark chocolate and cereals are administering the highest level of the Ni into the human body (Noël et al., 2012). Compatible to the study conducted by Leblanc et al., 2005, Noël et al., 2012 stated that the food groups with elevated Ni concentration are nuts, oilseeds, chocolate and breakfasts cereals. There are several (European) studies available evaluating the dietary exposure of the population to Ni in different countries (Alberti-Fidanza et al., 2003, Arnich et al., 2012, Bocio et al., 2005, Rose et al., 2010). Arnich et al. (2012) have reported a Ni dietary exposure level of 2.33 μg/kg bw/day in adults (18–79 years) and 3.83 μg/kg bw/day in children (3–17 years) in France. In the United Kingdom, a mean dietary exposure of 1.49–1.63 μg/kg bw/day was obtained for the adults (Rose et al., 2010). Almost all available dietary exposure estimation studies in different (European) countries are based on the total Ni concentration in food items which is not the most effective fraction.

According to the EFSA opinion on Ni intake via food, the bioaccessibility and bioavailability of Ni in the food matrix needs to be included when an exposure assessment is conducted (EFSA, 2015). The soluble fraction of the total Ni released from the food matrix into the digestive fluids at the time of digestion is the so-called bioaccessible fraction. This is the maximum possible amount of Ni that can be absorbed by body through consuming every food item (Junli et al., 2013). The bioavailability refers to the fraction of the element passing through the intestinal epithelium and entering blood stream (Wei, Shohag, & Yang, 2012). These two fractions, as the most effective fraction causing the health risk, must be taken into account in the Ni exposure assessment study.

Therefore, one of the important objectives of the current review paper is highlighting the importance of the bioaccessibility and bioavailability studies in the exposure assessments and demonstrating the scarcity of the available studies on estimation of the Ni exposure including bioaccessibility and bioavailability of metals.