Elsevier

Chemosphere

Volume 119, January 2015, Pages 757-762
Chemosphere

Westernized diets lower arsenic gastrointestinal bioaccessibility but increase microbial arsenic speciation changes in the colon

https://doi.org/10.1016/j.chemosphere.2014.08.010Get rights and content

Highlights

  • Effect of diet matrix on bioaccessibility of different arsenic species in diet.

  • Effect of diet matrix on biotransformation of different arsenic species in diet.

  • The difference in formation of new toxic arsenic species basing on diet matrix.

  • How difference in diet matrix might be important in case of oral arsenic exposure.

Abstract

Arsenic (As) is an important contaminant present in food and water. Several studies have indicated that the occurrence of As based skin lesions is significantly different when root and gourd rich diets are consumed compared to meat rich diets. Additionally, urinary As speciation from orally exposed individuals appears to depend on the composition of the diet. These observations imply that diet composition can affect both the bioavailable As fraction as the As speciation in the body. In this study, we used the in vitro gastrointestinal method (IVG) to evaluate how an Asian type diet (fiber rich) and a Western type diet (fat and protein rich), differ in their capability to release inorganic As (iAsV) and dimethyl arsinate (DMAV) from a rice matrix following gastrointestinal digestion. Moreover, we used a validated dynamic gut simulator to investigate whether diet background affects As metabolism by gut microbiota in a colon environment. An Asian diet background resulted in a larger As bioaccessibility (81.2%) than a Western diet background (63.4%). On the other hand, incubation of As contaminated rice with human colon microbiota in the presence of a Western type diet resulted in a larger amount of hazardous As species – monomethyl arsonite and monomethylmonothio arsonate – to be formed after 48 h. The permeability of these As species (60.5% and 50.5% resp.) across a Caco-2 cell line was significantly higher compared to iAsV and DMAV (46.5% and 28% resp.). We conclude that dietary background is a crucial parameter to incorporate when predicting bioavailability with bioaccessibility measurements and when assessing health risks from As following oral exposure.

Introduction

Arsenic (As) is a naturally occurring element in food, soil, air, and water. The major sources of exposure are from food and water. A variety of adverse health effects, e.g., skin and internal cancers, cardiovascular, and neurological effects, have been attributed to As exposure (Chen et al., 1992).

Human health effects from chronic As exposure have also been reported mainly in populations with low socioeconomic status and high levels of malnutrition. Diet composition has a significant effect on contaminant bioaccessibility and thereby also oral bioavailability. We previously (Alava et al., 2012a) demonstrated that lipids have a large impact on arsenic bioaccessibility, but also that this depends on the As speciation. Some other studies stated that in protein rich rice (Narukawa and Chiba, 2010) AsIII is tightly bound to the thiol groups of the proteins and may influence its bioaccessibility. Previous studies demonstrated a relationship between diet composition and levels of MMAIII found in urine after ingesting inorganic As (Steinmaus et al., 2005). Additionally, some studies reported that people, who consumed diets relatively high in roots and gourds as opposed to meat or other kinds of vegetables, were less likely to develop As-related skin lesions and also showed different metabolic rate of consumed arsenic (Lammon and Hood, 2004).

Differences in dietary matrix composition may affect release of As from the food source after ingestion. Food contains both organic and inorganic As, whereas drinking water primarily contains inorganic forms of As. In a scenario of dietary As exposure, rice has been demonstrated to be one of the major foodstuffs contributing to human As exposure (Williams et al., 2007) and also widely consumed (Raab et al., 2009). Interestingly, As biotransformations by human gut microbiota are even reported in case of As contaminated rice (Sun et al., 2012). Moreover, rice is an important carbohydrate sources in both Asian and Western style diets. Trenary et al. reported bioaccessibility of arsenic species from different types of rice in USA by using in vitro setup. These people extended their results to estimate the exposure level to American people by using probabilistic exposure model. All these above observations and reports lead to an interesting and important question; what is the effect of diet matrix on bioavailability of arsenic from rice?

As extension to the above question the second part to focus is presystemic metabolism. Upon oral exposure of As contaminated food, gastrointestinal digestion may release a fraction of the matrix-bound As: this is termed the bioaccessible fraction, which is considered a conservative estimator of the oral bioavailable As fraction. The As fraction that is not absorbed across the small intestinal epithelium and the remaining matrix-bound As will reach the colon region. Here, microbial breakdown of the remaining food matrix may further contribute to As release, while the released As in general may get subjected to the diverse metabolic potency of the vast endogenous microbial community. Such conversion of As by colon microbiota is termed presystemic metabolism. Notably, some studies have revealed that microorganisms are important contributors to arsenic speciation changes. A wide range of microbial metalloid biotransformations have been revealed, including oxidation, reduction, methylation and thiolation (Diaz-Bone and Van de Wiele, 2010). Recently, As biotransformations by human gut microbiota have been characterized using As contaminated soils and rice (Van de Wiele et al., 2010, Alava et al., 2012b).

Summarizing the above paragraphs; as rice being one of the major source of arsenic through food and diet components like lipids and fiber affecting the bioaccessibility of ingested arsenic species we aimed to study whether and how bioaccessibility of As is affected by diet composition and further how these diets effect the biotransformations of ingested As. Arsenic through rice is major problem in western countries like America (Trenary et al., 2012) and Eastern countries like Bangladesh, India and Taiwan (Meharg and Rahman, 2003, Chowdhury et al., 2000a, Chowdhury et al., 2000b, Pal et al., 2009), and there is significant difference between diet compositions of these two regions; Asian diet (low in fat, protein and high in carbohydrate) and Western diet (high fat and protein) (Suhana et al., 1999, Park et al., 2006). We choose these two diet compositions to elucidate whether and how bioaccessibility of As is affected by diet composition, further how these diets effect the biotransformations of As.

Section snippets

Arsenic standards and samples

Standards used were: NaAsO2 solution (VWR, Belgium) for Arsenite (AsIII), Na2HAsO4⋅7H2O (Fluka, Switzerland) for Arsenate (AsV), (CH3)2AsO2Na⋅3H2O (Fluka, Switzerland) for dimethyl arsinous acid (DMAV), and (CH3)AsNa2O3⋅6H2O (Chemservice, Belgium) for mono methyl arsonous acid (MMAV). Monomethylmonothioarsinic acid (MMMTA) was prepared in the lab. Stability, purity and procedure were already published (Alava et al., 2012). The structure of the product was checked by LC–ESI–MS and MS/MS. MMAIII

Analysis of rice samples for As content

Arsenic was extracted from all rice types using microwave digestion. Extraction efficiencies were calculated on a NIST 1568a certified reference rice matrix and were found to be almost 100% (Table 3). The digested solution was analyzed for total As content and As speciation. The total amount of arsenic was 395.1 ± 8.3 μg kg−1 in basmati rice (Table 3). DMAV represented the most abundant species followed by AsV and AsIII (Table 3). The distribution of organic versus inorganic As was around 70%

Discussion

A first important observation in this study is that methylation of inorganic As appeared to be a diet dependent process with the Western diet displaying a delayed but more efficient methylation (P < 0.05) than Asian diet. Although higher absolute amounts of bioaccessible As reached the colon upon incubation of Asian diet, the more efficient methylation during colon digestion of Western diets finally resulted in a higher production of trivalent and thiolated methylarsenicals (Table 4). Human gut

Acknowledgement

This study was funded by Federal public service of health, food chain safety and environment Contract (BIOTRAS RF 6247).

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