Food Control 109 (2020) 106909

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Food Control
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Arsenic in Argentinean polished rice: Situation overview and regulatory T

framework
Juan M. Oteizaa,b,c, Patricia A. Barrila,b,∗, César E. Quinteroc,d, Marianela Savioc,e,
Romina Befanic,d, Alicia Fernandez Cirellic,f, Natalia S. Echegarayg, Carolina Muradg,
Ariel Buedog
a
Laboratorio de Microbiología de los Alimentos, Centro de Investigación y Asistencia Técnica a la Industria (CIATI A.C.), Centenario, Neuquén, Argentina
b
Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET), Argentina
c
Red de Seguridad Alimentaria (RSA), CONICET, Argentina
d
Facultad de Ciencias Agropecuarias, Universidad Nacional de Entre Ríos. Paraná, Entre Ríos, Argentina
e
Instituto de Ciencias de la Tierra y Ambientales de La Pampa (INCITAP), CONICET-Universidad Nacional de La Pampa, Santa Rosa, La Pampa, Argentina
f
Instituto de Investigaciones en Producción Animal (INPA), CONICET-Universidad de Buenos Aires, Buenos Aires, Argentina
g
Molinos Río de la Plata S.A, Buenos Aires, Argentina

ARTICLE INFO ABSTRACT

Keywords: The Codex Alimentarius has established a 200 μg kg−1 limit of iAs in polished rice grain, while the Argentine
Oryza sativa Food Code, in accordance with the Mercado Común del Sur (Mercosur), has set an advisory level of 300 μg kg−1
Total arsenic of total As. This study aimed to map the content of arsenic species in polished rice grains of different varieties
Arsenic species and cultivation areas from Argentina. Mean concentrations of total, organic and inorganic As concentrations
Inorganic arsenic (iAs)
were 303 μg kg−1, 222 μg kg−1 and 81 μg kg−1, respectively. Almost 32% of the Argentinean polished rice
HPLC/ICP-MS
samples had total As ≥ 300 μg kg−1. However, 4.7% of the samples had iAs ≥200 μg kg−1; all of them with total
As closed to 1000 μg kg−1. Samples with iAs ≥200 μg kg−1 were obtained from the South of the province of
Corrientes. Competent regulatory bodies should consider a reform of the maximum limits of As in polished rice.

1. Introduction high level of As soil availability is because flooded anaerobic conditions

Arsenic (As), which has been listed as a human carcinogen since
1980 by the International Agency for Research on Cancer (IARC), oc-
curs naturally in many chemical forms. Carcinogenicity is related to the
inorganic arsenicals exposure (namely arsenite – AsIII, and arsenate –
AsV), which are classified in Group 1, while methylated organic species
(monomethylarsonic acid – MMA and dimethylarsinic acid – DMA), are
much less toxic and are classified in Group 2B, as possibly carcinogenic
to humans (International Agency for Research on Cancer, 2012). Other
organic compounds, such as arsenobetaine (AsB) and arsenocholine
(AsC), are practically non-toxic towards living organisms (Caroli, La
Torre, Petrucci, & Violante, 1996). Therefore, the total arsenic content
in a sample does not indicate the level of hazard of the element actually
present, and it is important to determine the various forms of As for
providing a much clearer view of the risk associated with exposure to
As.
It has been observed that rice grain accumulates higher concentra-
tions of As compared to other cereal crops (Williams et al., 2007). The
in rice cultivation facilitates As mobilization in the soil solution, mainly
as AsIII, that is assimilated by rice roots (Xu, McGrath, Meharg, & Zhao,
2008; Zhao, McGrath, & Meharg, 2010). During flooding, the formation
of iron plaque on roots, availability of metal (hydro)oxides (Fe and Mn),
organic matter, clay mineralogy and competing ions and compounds
are all known to influence AsV and AsIII mobility in paddy soil-water
environments. Microorganisms play a key role in As transformation
through oxidation/reduction, and methylation/volatilization reactions,
but transformation kinetics are poorly understood (Kumarathilaka,
Seneweera, Meharg, & Bundschuh, 2018). Despite its high susceptibility
to As accumulation, rice is a staple food for about 50% of the global
population (Chen, Tang, Wang, & Zhao, 2018).
Since toxicity depends on the chemical forms of As, arsenic spe-
ciation in rice can provide useful information for risk assessment and
management. Studies have shown that organoarsenical forms of As
were not toxicologically significant enough at the levels found in rice
grain to be included in the Codex Alimentarius limit (European Food
Safety Agency, 2009). Thus, the Joint Food and Agriculture

∗
Corresponding author. Laboratorio de Microbiología de los Alimentos, CIATI A.C, Expedicionarios del Desierto 1310, 8309, Centenario, Neuquén, Argentina.
E-mail address: patricia.barril@conicet.gov.ar (P.A. Barril).

https://doi.org/10.1016/j.foodcont.2019.106909
Received 11 July 2019; Received in revised form 19 September 2019; Accepted 20 September 2019
Available online 21 September 2019
0956-7135/ © 2019 Elsevier Ltd. All rights reserved.
J.M. Oteiza, et al.
Organization and the World Health Organization (FAO/WHO) Expert
Committee on Food Additives has set advisory levels of 200 μg kg−1
inorganic As (iAs) in polished rice grains (Codex Alimentarius, 2018).
In the same way, the European Commission, through the Regulation
(UE) 2015/1006, established advisory levels of 200 μg kg−1 inorganic
As (sum of AsIII and AsV) in elaborated (polished or white) rice, not
parboiled (Comision Europea, 2015).
On the other hand, the Argentine Food Code (AFC) (2017), through
the Mercosur Resolution 12/11 “Mercosur technical regulation on
maximum limits of inorganic contaminants in food”, has adopted the
determination of total arsenic in rice and its derivatives, except oil, and
has established as maximum limit 300 μg kg−1.
In Argentina, some 200,000 ha of rice are sown in a large produc-
tion area in very heterogeneous environments. Some papers report As
concentrations in Argentinean rice, but only for the southern region
(province of Entre Ríos) (Farías et al., 2015; Quintero et al., 2014).
There are no reports regarding to As concentration in Argentine rice,
which encompass and represent the entire surface.
In this context, the aim of this study was to map total, organic and
inorganic As content in different varieties of Argentinean polished rice,
and to provide information that may be useful in setting future stan-
dards.
2. Materials and methods
2.1. Sample collection
A total of 129 polished rice samples, 1 kg each, of seven different
varieties (Carnaroli, n = 2; Fortuna, n = 6; Ñu Poty, n = 7; Epagri,
n = 8; Puitá, n = 12; Gurí, n = 42; IRGA 424, n = 52) were collected
from producing fields during harvesting in March 2017 (Summer
season) in the Argentinean provinces of Chaco (n = 4), Formosa
(n = 15), Santa Fe (n = 31), Entre Ríos (n = 37) and Corrientes
(n = 42) (Fig. 1). The sample quantities are proportional to the surface
and the varieties planted in each zone.
Entre
Ríos
ARGENTINA
South America
Fig. 1. Sampling geographic area indicated in the map of Argentina.
2
Food Control 109 (2020) 106909
2.2. Sample treatment for As speciation analysis
The digestion method from the U.S. Food and Drug Administration
(FDA), with some internal laboratory modifications, was used
(Kubachka, Shockey, Hanley, Conklin, & Heitkemper, 2012). About
150 g of each sample were ground in stainless steel mill (F100, Numax,
Mumbai, India). Then, rice powder was digested by acid-assisted mi-
crowave (MW) irradiation using a commercially available oven
(MARS6, CEM, Mathews, NC). A sample of 1 g of the rice powder was
exactly weight and was placed in a PTFE vessel with 10 g of nitric acid
0.28 M (Huang, Ilgen, & Fecher, 2010). The vessels were sealed and
then subjected to the MW digestion cycle (95 °C for 90 min). After
reaching the room temperature, the obtained solutions were transferred
to a polypropylene tube. A total of 6.7 ml of deionized distilled water
were added and samples were centrifuged at 2800×g for 20 min. The
supernatant was filtered in a 0.45 μm nylon membrane to obtain a clear
solution without any visible residue.
2.3. As speciation and quantification
As species were determined using a high performance liquid chro-
matography (HPLC) apparatus (1260, Agilent Technologies, Inc., Santa
Clara, CA) for superior resolution, connected to an inductively coupled
plasma – mass spectrometry (ICP-MS) (7700x, Agilent Technologies, Inc.,
Santa Clara, CA), following the U.S. FDA extraction method with some
internal laboratory modifications (Kubachka et al., 2012). The extracted
solution was injected (100 μL) into the HPLC. Speciation of AsIII, AsV,
MMA, DMA, and AsB was performed on an anion exchange column (PRP-
X100, 10 μm, 4.1 × 250 mm, Hamilton®). The mobile phase contained
0.02 M, 1 M and 5 M K2HPO4 (J. T. Baker, Center Valley, PA) and
KH2PO4 (Scharlau Chemie, Barcelona, Spain). NIST Standard Reference
Materials (SRM) 1568a rice flour and 1568b rice flour (National Institute
of Standards and Technology, Gaithersburg, MD) were used as quality
control materials for arsenic speciation, with a rate of recovery of
95 ± 8% (n = 6). Five point calibrations were performed with arsenic
species stock solutions containing AsIII, AsV, MMA, DMA and AsB. Ca-
libration concentrations were 0.4, 1, 5, 10 and 20 μg L−1. The limit of
detection (LOD) was calculated as the relationship between blank and
standard accounts lower than 3, and the limit of quantification (LOQ)
was calculated as the relationship between blank and standard 2 ac-
counts greater than 10. This signal is evaluated each time the analysis is
performed. The LOD and LOQ were 7 μg kg−1 and 20 μg kg−1, respec-
tively, for each of the As species analyzed. Total As was obtained as the
sum of all the arsenic species analyzed.
2.4. Digestion and determination of total arsenic
The total arsenic content in rice was determined in 20% of the
samples, randomly selected, in order to confirm the speciation data.
The determination was done by ICP-MS methodology in accordance
with AOAC 2015.01 guidelines (Briscoe, 2015), employing an Agilent
7700x ICP-MS (Agilent Technologies, Inc., Santa Clara, CA), a collision/
reaction cell gas of He to reduce the polyatomic interference of chloride
(i.e. 40Ar35Cl) on m/z 75, and germanium (Ge: m/z 74) as internal
standard. The system was control with inference check solutions and
NIST SRMs 1568a and 1568b were used as quality control materials for
total As determination.
2.5. Statistical analysis
The one-way ANOVA data analysis (95% confidence level) was
applied to detect significant statistical differences in the As species
concentrations determined in the rice samples. The correlation analysis
was conducted by both Spearman's correlation and Pearson's correla-
tion (95% confidence limit). All statistical analyses were performed
with Infostat (Di Rienzo et al., 2017).
J.M. Oteiza, et al. Food Control 109 (2020) 106909

Table 1
Mean concentration (μg kg−1) ± standard deviation (SD) of total, organic and inorganic arsenic species in polished rice from Argentinean provinces with rice
activity. Minimum and maximum values are shown in brackets.
Province n Total As Organic As Inorganic As

Chaco 4 188 ± 70 (88–252) 87 ± 45 (20–117) 101 ± 29 (68–135)

Formosa 15 92 ± 26 (63–144) 18 ± 7 (10–29) 74 ± 25 (43–124)
Santa Fe 31 108 ± 26 (43–164) 51 ± 27 (10–116) 57 ± 11 (33–79)
Entre Ríos 37 369 ± 245 (83–957) 323 ± 257 (31–947) 47 ± 30 (10–177)
Corrientes 42 459 ± 389 (103–1306) 337 ± 335 (41–1286) 122 ± 104 (10–397)

TOTAL 129 303 ± 302 (43–1306) 222 ± 274 (10–1286) 81 ± 71 (10–397)

3. Results and discussion A)

To validate the extraction effiency of the arsenic species, the NIST 1400
SRM 1568 rice flour was analyzed. Results for speciated and total As in
the standard reference material were in good agreement with certified 1200
values. A mass balance was calculated between the sum of all arsenic

Organic As (ug kg-1)

1000
species detected and the total As determined in each NIST SRM 1568 y = 0,8838x - 45,4219
sample. The average mass balance was 96.7 ± 6.0% for the NIST SRM 800 R = 0,9741
samples, which ensured that the majority of the total arsenic in the
600
samples was accounted for in the speciation analysis.
The concentrations of the arsenic species in the polished rice sam- 400
ples obtained from Argentinean provinces with rice activity are shown
200
in Table 1. A predominance of the DMA organic specie was observed,
seconded by AsIII, while the MMA and AsV were minority, and the AsB 0
was not detected. The mean concentration of total As was 303 μg kg−1, 0 200 400 600 800 1000 1200 1400
and the mean concentrations of organic and inorganic As species were Total As (ug kg-1)
222 μg kg−1 and 81 μg kg−1, respectively. These results show that
73.3% of the As detected in the Argentine rice samples was organic and
B)
26.7% corresponded to inorganic species. Our results were comparable
to the findings of Farías et al. (2015) reporting total As concentrations
of 299 μg kg−1 and iAs of 99 μg kg−1 in rice grown in Entre Ríos, Ar- 500
gentina. However, they were lower than the mean total As of
180 μg kg−1 and iAs of 126 μg kg−1 in rice grown in Santa Fe, reported 400
Inorganic As (ug kg-1)

by Sigrist, Hilbe, Brusa, Campagnoli, and Beldoménico (2016).

The relationships between total As and organic and inorganic As 300
species are shown in Fig. 2. The correlation coefficient (r) between total y = 0,1162x + 45,4219
and organic As was 0.9741 (P < 0.0001), where organic As (especially R = 0,4930
200
DMA) increased linearly with increasing total As concentration
(Fig. 2A). Very similar results were presented by Farías et al. (2015). On 100
the other hand, inorganic As revealed a low/moderate correlation with
total As (r = 0.4930, P < 0.0001) as can be observed in Fig. 2B.
0
Total As values lower than 300 μg kg−1 (maximum limit established 0 200 400 600 800 1000 1200 1400
by the AFC) were found in 68.2% of the samples. However, 31.8% of
the samples, from the provinces of Entre Ríos (n = 18/37, 48.6%) and Total As (ug kg-1)
Corrientes (n = 23/42, 54.8%), exceeded this limit (Table 2). It should
Fig. 2. Correlation between the total arsenic and (A) organic and (B) inorganic
be noted that Entre Ríos and Corrientes are the provinces with major
arsenic species.
rice production in Argentina. In rice samples with total As ≥
300 μg kg−1, the proportion of organic species was 84.4%; meanwhile
in samples with total As < 300 μg kg−1 the proportion of organic spe- the number of samples of each rice variety per province and the results
cies was significantly lower (53.1%). Polished rice samples with iAs obtained through the statistical analysis, the effect of the rice variety
higher than 200 μg kg−1 (maximum limit established by the CODEX could not be assessed. Mean As concentrations for each rice variety are
193–1995) were only found in the province of Corrientes (n = 6/42, shown in Table 3. Carnaroli was the rice variety that revealed the
14.3%). Overall, this value represents a total of 4.7% (n = 6/129) of highest total and organic As levels, followed by Gurí and IRGA 424
the Argentine polished rice samples. All these samples had total As (Table 3A). Overall, 67.5–98.6% of the As found in the varieties IRGA
concentrations closed to 1000 μg kg−1. 424, Fortuna, Gurí and Carnaroli corresponded to organic species
Recent studies have shown that the concentration and speciation of (specially DMA), meanwhile only 40–41.5% of the As detected in the
As in rice varies according to its origin and genetics. Choi et al. (2014) varieties Ñu Poty, Puitá and Epagri was organic. Rice samples grown in
reported that the iAs content of rice varies greatly depending on the the provinces of Entre Ríos and Corrientes showed significantly higher
cultivation country, region, variety, and harvest time. In this study, an total As levels (Tables 1 and 3) in relation to the other provinces,
analysis of variance and test of means was carried out to evaluate the mainly sustained in a higher concentration of organic species
effect of the variables, rice origin (province) and variety, on the As (Table 3B).
concentration. For all the As species, the effect of the province of origin As rice samples from the provinces of Entre Ríos and Corrientes had
was very significant (P < 0.0001). However, given the imbalance of the highest concentrations of As, a separate statistical analysis was

3
J.M. Oteiza, et al. Food Control 109 (2020) 106909

Table 2
Number (and %) of Argentine polished rice samples with total and inorganic arsenic concentrations (μg kg−1) below or above the limits established by the Argentine
Food Code (300 μg kg−1 total As) and CODEX (200 μg kg−1 iAs).
Province n Total As Inorganic As

< 300 300–499 500–1000 > 1000 < 200 200–300 > 300

Chaco 4 4 (100) – – – 4 (100) – –

Formosa 15 15 (100) – – – 15 (100) – –
Santa Fe 31 31 (100) – – – 31 (100) – –
Entre Ríos 37 19 (51.4) 9 (24.3) 9 (24.3) – 37 (100) – –
Corrientes 42 19 (45.2) 10 (23.8) 6 (14.3) 7 (16.7) 36 (85.7) 1 (2.4) 5 (11.9)

TOTAL 129 88 (68.2) 19 (14.8) 15 (11.6) 7 (5.4) 123 (95.3) 1 (0.8) 5 (3.9)

conducted for these two provinces and the two rice varieties most
grown in these areas (Gurí and IRGA 424). In turn, an ecological zoning
was carried out within the provinces (Table 4). The effect of the culti-
vation zones within each of the provinces analyzed was significant. The
highest values of As species were recorded in the South zone of Cor-
rientes, followed by the North zone of Entre Ríos. The other zones
presented significantly lower values. Regarding the content of iAs,
differences were observed both between the geographical zones of
cultivation and between varieties of rice. The Central/North and South
areas of Corrientes showed higher concentrations than the Entre Ríos
zones. The variety IRGA 424 showed significantly higher content of iAs
than the Gurí variety, the first being the only one in which samples with
concentrations higher than 200 μg kg−1 were observed. Genotype, en-
vironment and the interaction of both are highly significant factors that
explain the variations in the concentration of As for same variety sown
on different sites (Duan et al., 2017).
Rice plants are unable to methylate inorganic As in vivo, therefore,
methylated As species present in rice may come through microbial-
mediated methylation in the rhizosphere. Arsenic methylation is a
common strategy to detoxify soil microbial arsenic. The amount of
methylated species in grain, primarily DMA, is directly proportional to
grain total As, although proportionality constants vary regionally (Zhao
et al., 2013). The mechanisms for such differences are not yet well
understood (Reid et al., 2017).
The productive rice regions located at south of Corrientes and north
of Entre Ríos, have very similar conditions. The sediments of the soils
are clayey rich in organic matter. Surely under these conditions, the
methylation of As and the accumulation of organic As in the rice grains
is propitiated. The other regions have more silty to sandy sediments.
The water used for irrigation of rice is not contaminated and does not
have high values of As. Nor are agrochemicals with As used in the crop,
so it is expected that the As comes from the natural soil (Quintero et al.,
2014).
Although the content of arsenic species in Argentinean polished rice
grains was determined in this study, As bio-accessibility in different
types of rice vary greatly depending on the rice and its origin (Althobiti,

Table 3
Mean concentration (μg kg−1) ± standard deviation (SD) of A) total, B) organic and C) inorganic arsenic in different rice varieties in Argentinean provinces with rice
activity. Differences between mean values with common superscripts are not statistically significant (P > 0.05).
A) Rice variety Chaco Formosa Santa Fe Entre Ríos Corrientes TOTAL

Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n

b ab c
Carnaroli – – – – – – 957 ± 0 1 503 ± 0 1 730 ± 321 2
Fortuna – – – – 133 ± 45b 6 – – – – 133 ± 45ab 6
Ñu Poty – – – – 105 ± 9a 7 – – – – 105 ± 9ab 7
Epagri 188 ± 70a 4 73 ± 14a 4 – – – – – – 130 ± 77ab 8
Puitá – – – – 97 ± 19a 12 – – – – 97 ± 19a 12
Gurí – – 112 ± 34a 5 – – 331 ± 236a 30 705 ± 473b 7 383 ± 317c 42
IRGA 424 – – 73 ± 11a 6 109 ± 13a 6 459 ± 152ab 6 425 ± 365a 34 266 ± 329b 52

B) Rice variety Chaco Formosa Santa Fe Entre Ríos Corrientes TOTAL

Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n

b ab c
Carnaroli – – – – – – 947 ± 0 1 493 ± 0 1 720 ± 321 2
Fortuna – – – – 90 ± 40b 6 – – – – 90 ± 40ab 6
Ñu Poty – – – – 42 ± 6a 7 – – – – 42 ± 6ab 7
Epagri 86 ± 45a 4 22 ± 4a 4 – – – – – – 54 ± 45ab 8
Puitá – – – – 39 ± 15a 12 – – – – 39 ± 15a 12
Gurí – – 21 ± 2a 5 – – 279 ± 244a 30 663 ± 485b 7 321 ± 330c 42
IRGA 424 – – 13 ± 8a 6 48 ± 3a 6 437 ± 159ab 6 277 ± 265a 34 194 ± 252b 52

C) Rice variety Chaco Formosa Santa Fe Entre Ríos Corrientes TOTAL

Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n Mean ± SD n

a a a
Carnaroli – – – – – – 10 ± 0 1 10 ± 0 1 10 ± 0 2
Fortuna – – – – 44 ± 6a 6 – – – – 44 ± 6a 6
Ñu Poty – – – – 63 ± 10a 7 – – – – 63 ± 10a 7
Epagri 101 ± 29a 4 51 ± 10a 4 – – – – – – 76 ± 34a 8
Puitá – – – – 58 ± 8a 12 – – – – 58 ± 8a 12
Gurí – – 91 ± 33a 5 – – 53 ± 29a 30 42 ± 30a 7 62 ± 32a 42
IRGA 424 – – 74 ± 6a 6 61 ± 13a 6 22 ± 18a 6 150 ± 104b 34 77 ± 97a 52

4
J.M. Oteiza, et al. Food Control 109 (2020) 106909

Table 4
Mean concentration (μg kg−1) ± standard deviation (SD) of total, organic and inorganic arsenic in Gurí and IRGA 424 rice varieties in different growing zones of the
Argentinean provinces Entre Ríos and Corrientes. Differences between mean values with common superscripts are not statistically significant (P > 0.05).
As specie Rice variety Entre Ríos Corrientes TOTAL

North Central/South Esquina Central/North South

Total Gurí 431 ± 233a 245 ± 210a 114 ± 0a – 804 ± 433b 399 ± 323a
IRGA 424 459 ± 152a – 130 ± 27a 307 ± 99a 687 ± 512ab 396 ± 340a
Organic Gurí 375 ± 251a 195 ± 210a 52 ± 0a – 765 ± 441b 347 ± 332a
IRGA 424 437 ± 159a – 63 ± 22a 200 ± 91a 455 ± 373a 289 ± 256a
Inorganic Gurí 56 ± 41a 51 ± 14a 63 ± 0a – 39 ± 32a 52 ± 30a
IRGA 424 22 ± 18a – 67 ± 4a 111 ± 27a 232 ± 139b 108 ± 107b

Sadiq, & Beauchemin, 2018). Therefore, speciation analysis of the bio-
accessible fraction of As in Argentinean rice should be important for
realistic risk assessment.
4. Conclusion
Argentinean rice producing areas located both at the North of the
province of Entre Ríos and South of Corrientes, presented the greatest
problem linked to the presence of arsenic.
Rice samples with high concentrations of total As had high con-
centrations of organic As. Almost 32% of the polished rice samples had
total As concentrations higher than 300 μg kg−1, which means that they
did not meet the current legislation (Argentine Food Code, 2017).
However, only 4.7% of the samples exceeded the levels of 200 μg kg−1
iAs established by the Codex Alimentarius (2018). Thus, these results
suggest that the competent regulatory bodies should consider a reform
of the maximum limits of arsenic in polished rice, based on CODEX
STAN 193–1995.
Values of iAs higher than 200 μg kg−1 were only found in the
variety IRGA 424 grown in the South area of the province of Corrientes.
This information could be used to implement specific management
actions tending to decrease the content of iAs in this rice production
area.
Declaration of interests
The authors declare that they have no known competing financial
interests or personal relationships that could have appeared to influ-
ence the work reported in this paper.
Funding sources
This work was supported by Molinos Río de la Plata S.A., Argentina.
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