The Global Rice Science Partnership, (GRiSP; 2013) reported that the majority of the Asian population, about half a billion poor people, use rice as their daily food staple. The ICAR-NRRI Annual Report (2020), notes that 102 million tons of rice were consumed in India during 2018–2019 compared to 146.7 million tons in China during the same period. Beside India and China, many countries rely heavily on rice as a staple: Bangladesh, Indonesia, Philippines, Thailand, and Vietnam. These countries together are responsible for more than 80% of worldwide rice production (ICAR-NRRI Annual Report, 2020). Zhao et al. (2010) noted that the level of As in unpolluted soil ranges from 0.1 to 10 mg kg− 1 globally. According to European Union (EU), the level of As should be restricted to 20 mg kg− 1 in agricultural fields (Hussain et al. 2021; Rahman et al. 2013; Rahman et al. 2007). Japan recommends that As levels in paddy soil should not exceed 15 mg kg− 1 (Ministry of Environment, Japan, 2021).
In this study, we have conducted meta-analyses on As accumulation in rice grains from several published studies on indica and japonica rice cultivars; results are summarized in Table 2 for each rice subspecies and their subgroups, where we reported the estimated effect size and 95% CI along with the no. of studies used.
Groups
|
No. of studies
|
Estimated effect size
(µg kg− 1)
|
95% confidence interval or CI
(µg kg− 1)
|
Table 2
Arsenic concentrations based on meta-analysis results obtained from the fixed effect models for different groups
Indica all
|
48
|
141.63
|
135.48–147.78
|
Indica polished
|
27
|
103.72
|
96.33–111.11
|
Indica unpolished
|
21
|
227.08
|
215.99–238.18
|
Japonica all
|
55
|
208.48
|
204.71–212.25
|
Japonica polished
|
40
|
207.22
|
203.34–211.09
|
Japonica unpolished
|
15
|
231.95
|
215.27–248.63
|
Japonica longer
|
34
|
232.48
|
227.82–237.13
|
Japonica shorter
|
21
|
162.63
|
156.20–169.07
|
Aromatic all
|
17
|
77.42
|
73.90–80.94
|
3.1. Indica group
The estimated average As accumulation in the grains of indica rice cultivars was (rounded) 142 µg kg-1 and 136 to 148 µg kg-1 at the 95% confidence interval (Table 2). Generally, inorganic As, which is more toxic than organic As, accumulates more in rice plants as compared to many other crops (Chen et al. 2018; Su et al. 2010). Previous studies have reported that the daily intake of As is higher via the consumption of cooked rice as compared to drinking water in some countries (Kumarathilaka et al. 2019; Rahman et al. 2011; Pal et al. 2009; Ohno et al. 2009); this is indeed true for India, especially West Bengal (Halder et al. 2013). According to the World Health Organization (WHO), the permissible limit of As in drinking water is 10 µg L-1 and the provisional tolerable daily intake (PTDI) for human health is 0.0021 mg kg-1 of body weight (WHO, 2001). There exists a global threat where daily intake of As exceeds the WHO limit via the consumption of cooked rice grains (BBS, 2011; FAO, 2002). Meharg et al. (2008) and Williams et al. (2005) determined the levels of As in rice in different countries (in increasing amounts): 46 µg kg-1 As in rice from India; 65 µg kg-1 from Canada; 131 µg kg-1 from Bangladesh; 140 µg kg-1 from Thailand; 160 µg kg-1 in polished rice from Italy; 180 µg kg-1 in polished rice from Spain; 280 µg kg-1 in polished rice from France; and 383 µg kg-1 from China. Differences in rice grain As concentrations are highly dependent on genetic factors (Verma et al. 2020; Carracelas et al. 2019; Kumarathilaka et al. 2018b; Sandhi et al. 2017; Bhattacharya et al. 2013; Norton et al. 2009).
Rice grain texture (polished vs unpolished) has a significant impact on As accumulation. According to FAO/WHO and Codex Alimentarius Commission, the maximum permissible limit of As in polished rice is 200 µg kg-1 and in unpolished rice is 300 µg kg-1 (Atiaga-franco et al. 2019; FAO, 2014; JECFA, 2012). The European Commission has restricted the level of As in food for children and infants at 100 µg kg-1 (European Commission, 2015) and they note that eating rice grains is the main source of As toxicity in human health (Samal et al. 2010; Lee et al. 2008). This study shows that As concentrations in the grain of indica polished rice was 104 µg kg-1 (estimated effect size), and as high as 227 µg kg-1 in indica unpolished rice; the respective 95% confidence intervals are 96 to 111 µg kg-1 and 216 to 238 µg kg-1(Table 2). These data (95% CI) show that As is significantly higher in the indica unpolished rice as compared to the indica polished rice, at the 5% level of statistical significance, which is consistent with earlier studies (Li et al. 2015; Rahman et al. 2014; Meharg et al. 2008). Forest plots of different subgroups of Indica rice (Fig. 1) show that BRRI dhan 32 is a low As accumulator compared to BRRI dhan 30 and BRRI dhan 33, even though these three rice cultivars were developed in Bangladesh. The amount of As accumulation is highly variable for BRRI dhan 28 (from Bangladesh). The majority of Chinese rice, polished subgroup cultivars, are high As accumulators (Fig. 1A), whereas unpolished cultivars from China had greater variability across most studies (Fig. 1B). These Chinese cultivars were obtained from different regions and provinces of China, viz., Anhui, Chongqing, Fujian, Guangdong, Guangxi, Henan, Hubei, Hunan, Jiangxi, Jiangsu, Jilin, Liaoning, Sichuan, Yunnan, and Zhejiang (Li et al. 2015). Differences in As concentrations in rice grain within or between varieties and between different geographies may be due to geogenic settings, bioavailability based on As speciation, the intensity of anthropogenic activities which involve fluxes of As to near surface ecosystems and/or inherent differences in varietal genetics.
3.2. Japonica group
Japonica rice is a popular subspecies throughout Eastern and South-Eastern Asia. The most well-known japonica rice varieties are Arborio, Carnaroli, Ribe, Risotto, Roma, Sushi and Vialone Nano, etc., cultivated in Australia, China, Japan, Italy, UK and many other countries (Fransisca et al. 2015; Somella et al. 2013; Padovani et al. 2006). In this study, the overall estimated As accumulation in the grains of japonica rice cultivars was 208 µg kg-1 and the corresponding 95% confidence interval was 205 to 212 µg kg-1(Table 2), and therefore higher than Indica rice grain at the nominal 5% level of statistical significance.
The japonica rice group was subdivided with respect to grain texture and size to access their relative As accumulation. The As level in Japonica polished rice grain was 207 µg kg-1 (effect size in the subgroup meta-analysis) and the corresponding 95% confidence interval was 203 to 211 µg kg-1; unpolished japonica rice grain accumulated 232 µg kg-1 As, and the associated 95% confidence interval 215 to 249 µg kg-1(Table 2). As with the indica rice, polished grains accumulate significantly less As compared to unpolished grains for the japonica species. According to Li et al. (2015), lower concentrations of As in polished samples is the result of mechanical removal of surface As during the polishing process. Among polished japonica rices, the Arborio rice varieties and a few Australian varieties showed greater variability in As concentrations, and sushi varieties from China and the USA were lower As accumulators (Fig. 2A). Most white rice cultivars from the USA are high As accumulators, some accumulated greater than 350 µg kg-1 As in their grain. Fransisca et al. (2015) found that Chinese sushi rice accumulated less As compared to Australian sushi rice and higher variability was present for the USA sushi rice. Japonica unpolished rice cultivars have comparatively greater variability in As accumulation than japonica polished rice (Fig. 2B). Among unpolished japonica rice, the levels of As is higher in brown rice cultivars from the USA; which is significant in European countries and the USA, where the average is 140 g of brown rice consumed per day (Williams et al. 2005; Robberecht et al. 2002; Tao et al. 1999).
Subgroup meta-analysis based on grain sizes of japonica rice, show that As accumulation in longer grains is significantly higher than in shorter grains. The level of As in japonica rice varieties with longer grains is (on average) 232 µg kg− 1 and its 95% confidence interval is 228 to 237 µg kg− 1 (Fig. 3) while in shorter japonica rice grains the level is 163 µg kg− 1 with the associated 95% confidence interval being 156 to 169 µg kg− 1 (Table 2). These findings are consistent with other work (e.g., Fransisca et al. 2015) which demonstrated that the size of grains correlates with the level of As accumulation. A few cultivars of Australian rice (both white and brown) accumulated relatively less As although the corresponding studies (Fransisca et al. 2015; Rahman et al. 2014) had higher variability in the reported grain As accumulations (Fig. 3A). Most long grained cultivars of US white rice (Williams et al. 2005) had higher levels of As in their grain while cultivars from Italy like Ribe, Roma (Sommella et al. 2013) and a specific Spanish rice (Williams et al. 2005) were less As accumulators. As concentrations varied significantly for cultivars from China (Fransisca et al. 2015), for both shorter and longer grains. Within the pool of japonica rice varieties with shorter grain sizes, Chinese sushi rice accumulated less As whereas Texas and Australian sushi were high As accumulators (Fig. 3B).
3.3. Arsenic accumulation in aromatic rice grains
Generally, aromatic rice is medium to long grained. According to Civáň et al. (2019), this type of rice is not identical with indica or japonica rice based on genetic variability. There are many varieties of aromatic rice such as basmati, jasmine, badshabhog, tulsibhog, gobindobhog, radhunipagol, sona masuri, chinigura, kalijira, tulaipanji, etc. In this study, the estimated overall level of As accumulation in aromatic rice cultivars was 77 µg kg− 1 with the corresponding 95% confidence interval being 74 to 81 µg kg− 1 (Table 2). The literature notes that aromatic rice varieties exhibit some typical characteristics in terms of amylose content, phenol reaction etc. and this type of rice could be an intermediary rice types between japonica and indica (Bhattacharjee et al. 2002). From our analyses, we found that the kalijira rice cultivars showed greater variability whereas basmati rice cultivars were lower As accumulators (Fig. 4). In general, the As levels do not affect the aromatic rice as much. Islam et al. (2017) demonstrated that the As level in the aromatic rice variety was only 58 µg kg− 1. According to Sandhi et al. (2017), the human consumption of aromatic rice is safer for human consumption due to its potentiality to accumulate less As. Aromatic rice grown in India, Bangladesh, and Pakistan were identified as low As accumulators and hence potentially safer for human consumption globally (Rahman et al. 2014).
3.4. A Comparative overview
In order to make an overall comparison of the grain effect-size impact on As accumulation for all three rice species (indica, japonica and aromatic) and their subgroups, we have represented the resulting 95% confidence intervals for each case in Fig. 5 (data from Table 2). It is evident from this comparison that the aromatic rice varieties are significantly lower As accumulators compared to both indica and japonica varieties, at 5% level of significance, and hence they are the safest option for human consumption to avoid As toxicity. Sandhi et al. (2017) also concluded from analysing the accumulation factor of As, that aromatic rice cultivars accumulated less As than other rice cultivars with high yield capacity. However, the consumption of aromatic rice is still significantly low compared to other common rice varieties (including indica and japonica) possibly due to its higher price.
Figure 5 also shows that unpolished rice cultivars should be avoided, particularly when there is a potential risk of As contamination due to cultivation practices. Japonica longer grains do not differ significantly from the unpolished rice cultivars in terms of As accumulation, at 5% level of statistical significance; polished rice cultivars are a relatively safe option. Unless shorter grain size, even polished japonica rice cultivars are not necessarily a good option considering their As levels. Conversely, indica polished rice cultivars are far better with much lower As accumulation; consumptions of indica polished rice would be the next best option, after aromatic rice, to combat As toxicity from rice-based products.