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Arsenic in Rice - Rahman, Rahman, Naidu
Arsenic in Rice - Rahman, Rahman, Naidu
Arsenic in Rice - Rahman, Rahman, Naidu
28
Arsenic in Rice: Sources and Human Health
Risk
Mohammad Azizur Rahman*, Mohammad Mahmudur Rahman†, Ravi Naidu†
*University of Technology, Centre for Environmental Sustainability, Faculty of Science, Sydney, New South Wales,
Australia, †University of South Australia, Center for Environmental Risk Assessment and Remediation (CERAR),
Mawson Lakes, South Australia, Australia; and Cooperative Research Centre for Contamination Assessment and
Remediation of the Environment (CRC-CARE), Salisbury South, South Australia, Australia
region, particularly in Bangladesh and West Bengal et al.30 reported 0.57–0.69 μg/g dry wt of arsenic in rice
(India), is between 400 and 650 g.34 Therefore, second to collected from a highly arsenic-contaminated area of the
water, rice constitutes the largest dietary source of arse- country. All these studies have revealed high arsenic lev-
nic for humans.35 When the high concentration of iAs,36 els in Bangladeshi rice grain.
cooking method, and high consumption rate are taken Rice from the Indian state of West Bengal also con-
into account, rice is considered to be a major threat to tains high levels of arsenic. Williams et al.27 reported
human health in arsenic-endemic S and SE Asia. 0.05 μg/g dry wt of arsenic (0.03–0.08 μg/g dry wt) in
Arsenic poisoning is greatest in Bangladesh, followed white basmati rice collected from Indian supermarkets.
by West Bengal, India. However, numerous cases have Meharg et al.20 found 0.07 μg/g dry wt of arsenic (0.07–
now been reported from many countries, including 0.31 μg/g dry wt, n = 133) in Indian white rice. Other
Chile, Cambodia, Laos, Burma, Pakistan, Nepal, Viet- studies also reported high levels of arsenic in rice grain
nam, Taiwan, Iran, Argentina, Finland, the United States, from West Bengal (0.11–0.44 μg/g dry wt53 and 0.03–
several provinces in China, and several other Indian 0.48 μg/g dry wt).52 The Nadia district in West Bengal
states. Arsenic exposure to humans is not restricted to the is one of the highly arsenic-contaminated areas in India,
arsenic-contaminated countries. Hundreds of thousands and arsenic concentrations in rice grain (either collected
of people worldwide are also facing slow poisoning and directly from farmers or purchased from local markets)
risk of death from arsenic in their daily diets. The pos- ranged between 0.02 and 0.17 μg/g dry wt with a mean
sibility of human exposure to arsenic is increasing with of 0.13 μg/g dry wt (n = 50).39
the expansion of the global food trade. Arsenic in foods A number of studies have shown high levels of arsenic
from arsenic-endemic areas will pose a potential health in Taiwanese rice. Rice collected directly from Taiwanese
risk for the people of those countries where arsenic con- farms was reported to have an arsenic concentration of
tamination of drinking water is not reported. Thus, arse- 0.76 μg/g dry wt.49 A market basket survey, conducted
nic in foods and its subsequent impacts on human health by Lin et al.,50 reported < 0.10–0.63 μg/g dry wt of arse-
is not a regional issue but an important global issue. In nic in Taiwanese rice, which is a comparable level to that
this chapter, the sources of arsenic in rice and the health reported by Williams et al.27 The concentration of arsenic
risk of arsenic from a rice diet are discussed. in Vietnamese rice was found to be 0.03–0.47 μg/g dry
wt.27,51 Thai rice has also been reported to contain high
levels of arsenic (0.11 ± 0.01 μg/g dry wt).27 A recent mar-
ARSENIC IN RICE GRAIN ket basket survey reported that arsenic concentrations in
Thai rice ranged between 0.01 and 0.39 μg/g dry wt, with
The significant number of articles published on arse- a mean of 0.14 μg/g dry wt (n = 54).20 Comparing this
nic concentrations in rice grain in recent years implies with the previous reports of Williams et al.27, the higher
that the dietary intake of arsenic form rice has received arsenic concentrations in Thai rice found in a recent study
the attention of the wider scientific community.13,27,30,36–42 by Meharg et al.20 suggest that arsenic levels in Thai rice
The high arsenic content in rice is a significant concern have increased in recent years. A considerable amount of
for arsenic-affected countries, as well as for countries arsenic has also been found in rice from the USA. A mar-
that import rice from arsenic-affected countries. Arsenic ket basket survey conducted by Schoof et al.23 reported
concentrations in rice grain from diverse origins is pre- that total arsenic concentrations in rice from the USA
sented in Table 28.1.11,13,20,21,23,27,39,43–54 (“American rice”) were 0.20–0.46 μg/g dry wt, while
Bangladesh is one of the highly arsenic-contaminated Heitkemper et al.45 found levels of 0.11–0.34 μg/g dry wt.
countries.55 Rice grain collected from the arsenic-con- A recent study reported 0.03–0.66 μg/g dry wt of arse-
taminated western part of Bangladesh had arsenic lev- nic in American rice,20 which is much higher than that
els of 0.03–1.84 μg/g dry weight (dry wt).11 In another reported by Williams et al.27 The studies reveal that arse-
study, arsenic concentrations in rice collected from the nic-contaminated rice is a significant source of dietary
fields of the southern part of Bangladesh were found to arsenic for the people of arsenic-affected areas, as well as
be between 0.04 and 0.92 μg/g dry wt.13 However, arse- for people of those countries that import rice from con-
nic concentrations in rice collected from markets across taminated regions.
the country were found to be 0.18–0.31 μg/g dry wt.13
It is interesting that arsenic concentrations in rice vary
with the sampling site and rice growing season, both ARSENIC SPECIATION IN RICE GRAIN
of which are related to the arsenic concentration in irri-
gation water. Other studies also showed high levels of Inorganic arsenic (iAs) species are more toxic than
arsenic in Bangladeshi rice. For example, Islam et al.56 orgAs species.57,58 Pentavalent methylarsenic species
reported 0.05–2.05 μg/g dry wt of arsenic in rice grain (DMAAV and MMAAV) are considered to be non-toxic.59
collected from southern Bangladesh, while Rahman Therefore, arsenic speciation in rice is considered to be
Origin Mean Range Mean Range Mean Range Mean Range Reference
Europe 0.15 0.13–0.20 0.08 0.06–0.10 0.04 0.04–0.06 52 44–62 Ohno et al.44
367
(Continued)
TABLE 28.1 Total (tAs), Inorganic (iAs), and Organic (orgAs) Arsenic Concentrations (μg/g dry wt.) in Rice Grain from Different Countries—cont’d
368
tAs iAs orgAs % of iAs
Origin Mean Range Mean Range Mean Range Mean Range Reference
grain and 27–60% higher than that in rice cooked with considered likely to increase in this region in the com-
excess water.30 Cooking rice with excess water results ing years in order to increase crop production to meet
in a decrease in the concentrations of total and iAs in the demands of the increasing population. This practice
cooked rice when the gruel is discarded, while arsenic may increase additional arsenic deposition in paddy
concentration increases significantly when rice is cooked soil. Thus, inorganic arsenic-rich underground irrigation
with limited water and the gruel is not discarded after water is the main source of arsenic in rice in Asian arse-
cooking. For example, Raab and colleagues68 found that nic-endemic countries. On the other hand, arsenical pes-
cooking rice with excess water reduced total and iAs in ticides are the main source of arsenic for American rice.
cooked rice by 35% and 45%, respectively, while cooking In addition, microbial methylation of inorganic arsenic
with limited water did not remove arsenic substantially. to orgAs in the rice field (in water and rhizosphere soil)
would also contribute to the orgAs content in rice.
* The WHO recommended MTDI value of iAs has been withdrawn recently. The MTDI is based on iAs concentration (%) in rice grain, a body weight of 60 kg, a consumption rate
of 0.5 kg rice grain per day, and bioavailability of iAs in cooked rice (90%).48
highest (17.80%) total arsenic uptake values in the study, about 185% for Quest if the MTDI calculation were based
it was estimated that daily consumption of 5.7 kg or 1.2 kg on arsenic speciation and bioavailability data, which
cooked rice containing 4.21 ± 0.09 or 2.29 ± 0.05 μg/g dry is comparable to white rice of Taiwan origin (190%;
wt, respectively, would be required to reach the WHO Table 82.343) even though the tAs concentration in Quest
recommended maximum tolerable daily intake (MTDI) rice is two-fold greater than that in white rice. Thus, cal-
of iAs (2.1 μg/d per kg body weight13). However, the culation of MTDI values considering the tAs concentra-
WHO recommended MTDI value of iAs has been with- tion in rice grain significantly overvalues arsenic intake
drawn recently. An adult male consumes about 1.5 kg for varieties that mainly contain orgAs species (e.g.,
cooked rice (0.5 kg rice grain) a day in arsenic-endemic Quest rice contains 86% orgAs).43 On the other hand, if
South Asian countries, indicating that the people of this only iAs concentration in rice is considered in the MTDI,
region may reach the MTDI of arsenic just from their the calculation would not reflect the real amount of arse-
rice diet. The contribution of iAs to MTDI, in rice from nic intake from high iAs-containing rice varieties (e.g.,
a range of countries, is listed in Table 28.2.13,20,27,45,47,48 Asian rice). Therefore, the MTDI should be calculated
Another study by Williams et al.13 showed that the based on arsenic concentration, speciation, and the bio-
contribution of iAs in rice to the MTDI of arsenic for a availability of arsenic species.
Bangladeshi adult (assuming the body weight is 60 kg)
would be 55–79%, depending on iAs concentration in
rice and rice type. The MTDI may exceed the 100% level MITIGATION OF ARSENIC EXPOSURE
when the concentration of iAs in rice is high.21,44,49 FROM RICE
In another study, Juhasz et al.43 investigated the bio-
availability of arsenic in rice and its significance for human It has been confirmed by a number of research groups
health risk. In that study, the absolute bioavailability of that rice represents a major route of arsenic exposure in
arsenic species (AsV, AsIII, MMAA, and DMAA) was populations that depend on a rice diet,38,39,41 and con-
determined using a swine animal model. The absolute sumption of rice containing a high level of arsenic, par-
bioavailability of iAs was highest (103.9% and 92.5% for ticularly the highly toxic and bioavailable iAs species,
AsIII and AsV, respectively) followed by DMAA (33.3%) poses a potential health risk to human.54,83 Therefore,
and MMAA (16.7%).43 The contribution of rice consump- how to mitigate or reduce arsenic exposure from rice
tion to MTDI was also estimated in cooked rice of differ- is an important concern in the scientific community. A
ent varieties from diverse origins. Results showed that range of methods, from agronomic measures and plant
the consumption of Quest rice of Australian origin may breeding to genetic modification, may be employed to
contribute 438% of the arsenic MTDI based on tAs con- mitigate arsenic exposure from rice. Some of the impor-
centration. However, the arsenic MTDI value would be tant and effective methods of arsenic exposure mitigation
TABLE 28.3 Assessment of the Contribution of Rice Consumption to Maximum Tolerable Daily Intake (MTDI Based on the
Bioavailability of Arsenic Species)*
* The contribution to MTDI (%) was calculated based on the concentration (μg/g dry wt) of arsenic species in rice grain, a body weight of 60 kg, a consumption rate of 0.42 kg dry
rice grain per day, and bioavailability factors of 0.33 and 1.0 for organic arsenic (orgAs) and inorganic arsenic (iAs), respectively, in cooked rice.43
involve agronomic measures, breeding rice varieties, Iron is believed to be an important factor in regulating
and cooking methods. arsenic bioavailability and uptake in rice.90–92 Rice plants
carry oxygen from the air down their stems, and dis-
charge it in the rhizosphere through the roots.71 This cre-
Agronomic Measures
ates an oxidized zone around the roots in which iron is
The main sources of arsenic in rice grain are arsenic- oxidized and precipitated to form a coating.92 AsV has a
rich paddy soils and irrigation water. Arsenic chemistry high binding affinity with precipitated iron hydroxides,
in paddy soils is extremely complex because of frequent which act as an arsenic filter to reduce arsenic uptake in
redox cycles in the soil, and arsenic uptake in rice from rice.90 However, sulfur was found to enhance the forma-
soil is influenced by a range of factors, including bio- tion of iron plaque in the rhizosphere and reduce arse-
availability, rhizosphere processes, and metabolism in nic accumulation in rice.87 In another study, phosphate
rice plants.84 Therefore, agronomic measures such as fertilizer was found to decrease iron plaque formation
water management55,85,86 and fertilization practices86–88 on rice roots and increase arsenic uptake in rice plant.88
would be effective methods to reduce arsenic uptake in The addition of nitrate also decreases iron plaque for-
rice grain. mation on the rice root surface; however, the addition
Rice is usually grown in anaerobic (flooded) condi- of nitrate reduced arsenic uptake by rice plant. These
tions in which arsenic exists mainly as dissolve AsIII results suggest that nitrate may inhibit Fe(III) reduction
form and is readily taken up by the rice plant. There- and/or stimulate nitrate-dependent Fe(II) oxidation,
fore, rice grown under flooded conditions was found to leading to arsenic co-precipitation with, or adsorption
accumulate much more arsenic than that grown under to, Fe(III) minerals in the soil.84 Two silicon transporter
aerobic conditions.89 AsV was found to be the main arse- proteins, Lsi1 and Lsi2, which are highly expressed in
nic species in the aerobic soil, and arsenic accumulation rice roots, can transport AsIII. Lsi2 in particular plays
in rice grain was observed to be 10- to 15-fold higher in an important role in the root-to-shoot transport of AsIII
flooded than in aerobically grown rice.89 Maintaining and arsenic accumulation in rice grains.93 Therefore,
aerobic conditions during either the vegetative or the silicon is another important nutrient that controls arse-
reproductive stage of rice growth decreases arsenic accu- nic uptake in rice grains. Silicon fertilization decreases
mulation in rice grain significantly compared with rice the total arsenic concentration in straw and grain by
grown under flooded conditions.86 78% and 16%, respectively, even though the addition of
19. Kemper K, Minnatullah K. Towards a More Effective Operational Re- 39. Mondal D, Polya DA. Rice is a major exposure route for arsenic in
sponse Arsenic Contamination of Groundwater in South and East Asian Chakdaha block, Nadia district, West Bengal, India: A probabilistic
Countries. Water and Sanitation Program: World Bank; 2005. risk assessment. Appl Geochem 2008;23(11):2987–98.
20. Meharg AA, Williams PN, Adomako E, Lawgali YY, Deacon C, 40. Rahman MA, Hasegawa H, Rahman MM, Miah MA. Accu-
Villada A, et al. Geographical variation in total and inorgan- mulation of arsenic in tissues of rice plant (Oryza sativa L.)
ic arsenic content of polished (white) rice. Environ Sci Technol and its distribution in fractions of rice grain. Chemosphere
2009;43(5):1612–7. 2007;69(6):942–8.
21. Sun GX, Williams PN, Carey AM, Zhu YG, Deacon C, Raab A, 41. Rahman MA, Hasegawa H, Rahman MM, Miah MAM, Tasmin A.
et al. Inorganic arsenic in rice bran and its products are an or- Arsenic accumulation in rice (Oryza sativa L.): Human exposure
der of magnitude higher than in bulk grain. Environ Sci Technol through food chain. Ecotoxicol Environ Saf 2008;69(2):317–24.
2008;42(19):7542–6. 42. Williams PN, Villada A, Deacon C, Raab A, Figuerola J, Green AJ,
22. Torres-Escribano S, Leal M, Velez D, Montoro R. Total and inor- et al. Greatly enhanced arsenic shoot assimilation in rice leads to
ganic arsenic concentrations in rice sold in Spain, effect of cooking, elevated grain levels compared to wheat and barley. Environ Sci
and risk assessments. Environ Sci Technol 2008;42(10):3867–72. Technol 2007;41(19):6854–9.
23. Schoof RA, Yost LJ, Eickhoff J, Crecelius EA, Cragin DW, Meacher 43. Juhasz AL, Smith E, Weber J, Rees M, Rofe A, Kuchel T, et al.
DM, et al. A market basket survey of inorganic arsenic in food. Food In vivo assessment of arsenic bioavailability in rice and its sig-
Chem Toxicol 1999;37(8):839–46. nificance for human health risk assessment. Environ Health Persp
24. Das HK, Mitra AK, Sengupta PK, Hossain A, Islam F, Rabbani GH. 2006;114(12):1826–31.
Arsenic concentrations in rice, vegetables, a fish in Bangladesh: A 44. Ohno K, Yanase T, Matsuo Y, Kimura T, Hamidur Rahman M,
preliminary study. Environ Int 2004;30(3):383–7. Magara Y, et al. Arsenic intake via water and food by a population
25. Booth B. Arsenic speciation varies with type of rice. Environ Sci living in an arsenic-affected area of Bangladesh. Sci Total Environ
Technol 2008;42(10):3484–5. 2007;381(1-3):68–76.
26. Booth B. Arsenic in US rice varies by region. Environ Sci Technol 45. Heitkemper DT, Vela NP, Stewart KR, Westphal CS. Determina-
2007;41(7):2075–6. tion of total and speciated arsenic in rice by ion chromatography
27. Williams PN, Price AH, Raab A, Hossain SA, Feldmann J, and inductively coupled plasma mass spectrometry. J Anal Atomic
Meharg AA. Variation in arsenic speciation and concentration Spectrom 2001;16(4):299–306.
in paddy rice related to dietary exposure. Environ Sci Technol 46. Xie ZM, Huang CY. Control of arsenic toxicity in rice plants grown
2005;39(15):5531–40. on an arsenic-polluted paddy soil. Commun Soil Sci Plant Anal
28. Musaiger AO, D’Souza R. The effects of different methods of cook- 1998;29(15):2471–7.
ing on proximate, mineral and heavy metal composition of fish 47. Liu H, Probst A, Liao B. Metal contamination of soils and crops
and shrimps consumed in the Arabian Gulf. Arch Latinoam Nutr affected by the Chenzhou lead/zinc mine spill (Hunan, China). Sci
2008;58(1):103–9. Total Environ 2005;339(1-3):153–66.
29. Ohno K, Matsuo Y, Kimura T, Yanase T, Rahman MH, Magara Y, 48. Laparra JM, Velez D, Barbera R, Farre R, Montoro R. Bioavailabil-
et al. Effect of rice-cooking water to the daily arsenic intake in ity of inorganic arsenic in cooked rice: Practical aspects for human
Bangladesh: Results of field surveys and rice-cooking experiments. health risk assessments. J Agric Food Chem 2005;53(22):8829–33.
Water Sci Technol 2009;59(2):195–201. 49. Schoof RA, Yost LJ, Crecelius E, Irgolic K, Goessler W, Guo HR,
30. Rahman MA, Hasegawa H, Rahman MA, Rahman MM, Miah et al. Dietary arsenic intake in Taiwanese districts with elevated
MAM. Influence of cooking method on arsenic retention in cooked arsenic in drinking water. Hum Ecol Risk Ass 1998;4(1):117–35.
rice related to dietary exposure. Sci Total Environ 2006;370(1):51–60. 50. Lin HT, Wong SS, Li GC. Heavy metal content of rice and Shellfish
31. Signes A, Mitra K, Burlo F, Carbonell-Barrachina AA. Effect in Taiwan. J Food Drug Anal 2004;12(2):167–74.
of cooking method and rice type on arsenic concentration in 51. Phuong TD, Chuong PV, Khiem DT, Kokot S. Elemental content of
cooked rice and the estimation of arsenic dietary intake in a Vietnamese rice. Part 1. Sampling, analysis and comparison with
rural village in West Bengal, India. Food Addit Contam: Part A previous studies. Analyst 1999;124(4):553–60.
2008;25(11):1345–52. 52. Pal A, Chowdhury UK, Mondal D, Das B, Nayak B, Ghosh A, et al.
32. Signes A, Mitra K, Burlo F, Carbonell-Barrachina AA. Contribution Arsenic burden from cooked rice in the populations of arsenic
of water and cooked rice to an estimation of the dietary intake of affected and nonaffected areas and Kolkata city in West-Bengal,
inorganic arsenic in a rural village of West Bengal, India. Food Addit India. Environ Sci Technol 2009;43(9):3349–55.
Contam: Part A 2008;25(1):41–50. 53. Roychowdhury T, Uchino T, Tokunaga H, Ando M. Survey of ar-
33. Farmer J, Johnson L. Assessment of occupational exposure to in- senic in food composites from an arsenic-affected area of West Ben-
organic arsenic based on urinary concentrations and speciation of gal, India. Food Chem Toxicol 2002;40(11):1611–21.
arsenic. Br J Ind Med 1990;47(5):342. 54. Rahman MA, Hasegawa H. High levels of inorganic arsenic in rice
34. Duxbury JM, Mayer AB, Lauren JG, Hassan N. Food chain aspects in areas where arsenic-contaminated water is used for irrigation
of arsenic contamination in Bangladesh: Effects on quality and pro- and cooking. Sci Total Environ 2011;409(22):4645–55.
ductivity of rice. J Environ Sci Health A 2003;38(1):61–9. 55. Khan MA, Islam MR, Panaullah GM, Duxbury JM, Jahiruddin M,
35. Chen S, Yeh S, Yang M, Lin T. Trace element concentration and ar- Loeppert RH. Accumulation of arsenic in soil and rice under wet-
senic speciation in the well water of a Taiwan area with endemic land condition in Bangladesh. Plant Soil 2010;333(1-2):263–74.
Blackfoot disease. Biol Trace Elem Res 1995;48(3):263–74. 56. Islam M, Jahiruddin M, Islam S. Assessment of arsenic in the
36. Meharg AA. Arsenic in rice – understanding a new disaster for water-soil-plant systems in Gangetic floodplains of Bangladesh.
South-East Asia. Trends Plant Sci 2004;9(9):415–7. Asian J Plant Sci 2004;3(4):489–93.
37. Bae M, Watanabe C, Inaoka T, Sekiyama M, Sudo N, Bokul MH, 57. Ng JC. Environmental contamination of arsenic and its toxicologi-
et al. Arsenic in cooked rice in Bangladesh. Lancet 2002;360(9348): cal impact on humans. Environ Chem 2005;2(3):146–60.
1839–40. 58. Meharg AA, Hartley Whitaker J. Arsenic uptake and metabolism
38. Mondal D, Banerjee M, Kundu M, Banerjee N, Bhattacharya U, Giri in arsenic resistant and nonresistant plant species. New Phytol
AK, et al. Comparison of drinking water, raw rice and cooking of 2002;154(1):29–43.
rice as arsenic exposure routes in three contrasting areas of West 59. Jain CK, Ali I. Arsenic: Occurrence, toxicity and speciation tech-
Bengal, India. Environ Geochem Health 2010;32(6):463–77. niques. Water Res 2000;34(17):4304–12.