You are on page 1of 9

Journal of Environmental Science and Health, Part A

Toxic/Hazardous Substances and Environmental Engineering

ISSN: 1093-4529 (Print) 1532-4117 (Online) Journal homepage: http://www.tandfonline.com/loi/lesa20

Health risks for human intake of aquacultural fish:


Arsenic bioaccumulation and contamination

Sandeep Kar , Jyoti Prakash Maity , Jiin-Shuh Jean , Chia-Chuan Liu , Chen-
Wuing Liu , Jochen Bundschuh & Hsueh-Yu Lu

To cite this article: Sandeep Kar , Jyoti Prakash Maity , Jiin-Shuh Jean , Chia-Chuan Liu , Chen-
Wuing Liu , Jochen Bundschuh & Hsueh-Yu Lu (2011) Health risks for human intake of aquacultural
fish: Arsenic bioaccumulation and contamination, Journal of Environmental Science and Health,
Part A, 46:11, 1266-1273, DOI: 10.1080/10934529.2011.598814

To link to this article: http://dx.doi.org/10.1080/10934529.2011.598814

Published online: 31 Aug 2011.

Submit your article to this journal

Article views: 342

View related articles

Citing articles: 29 View citing articles

Full Terms & Conditions of access and use can be found at


http://www.tandfonline.com/action/journalInformation?journalCode=lesa20

Download by: [IIT Indian Institute of Technology - Mumbai] Date: 07 September 2017, At: 09:59
Journal of Environmental Science and Health, Part A (2011) 46, 12661273
Copyright C Taylor & Francis Group, LLC

ISSN: 1093-4529 (Print); 1532-4117 (Online)


DOI: 10.1080/10934529.2011.598814

Health risks for human intake of aquacultural fish: Arsenic


bioaccumulation and contamination
SANDEEP KAR1, JYOTI PRAKASH MAITY2, JIIN-SHUH JEAN1, CHIA-CHUAN LIU1,
CHEN-WUING LIU3, JOCHEN BUNDSCHUH1,4,5 and HSUEH-YU LU2
1
Department of Earth Sciences, National Cheng Kung University, Tainan, Taiwan
2
Department of Earth and Environmental Sciences, National Chung Cheng University, Ming-Shung, Chiayi County,
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

Taiwan
3
Department of Bioenvironmental Systems Engineering, National Taiwan University, Taipei, Taiwan
4
Institute for Applied Research, Karlsruhe University of Applied Sciences, Karlsruhe, Germany
5
KTH-International Groundwater Arsenic Research Group, Department of Land and Water Resources Engineering,
Royal Institute of Technology (KTH), Stockholm, Sweden

Aquacultural tilapia (Oreochromis mossambicus L.) and shrimp (Penaeus monodon L.) from groundwater-cultured ponds in south-
western Taiwan were analyzed to estimate arsenic (As) bioaccumulation and the potential health risk to human intake. Most of
aquacultural ponds exhibited higher arsenic than maximum allowed concentrations (50 g L1) in pond water of Taiwan. Arsenic
levels in tilapia in Budai, Yichu and Beimen were 0.92 0.52 g g1, 0.93 0.19 g g1 and 0.76 0.03 g g1, respectively and in
shrimp was 0.36 0.01 g g1 in Beimen. Total arsenic in tilapia is highly correlated (R2 = 0.80) with total arsenic concentration
of pond water. Total arsenic in fish showed high correlation with that in bone (R2 = 0.98), head (R2 = 0.97) and tissue (R2 = 0.96).
Organic arsenic species (DMA) was found higher relative to inorganic species of As(III) and As(V). The average percent contribution
of inorganic arsenic to total arsenic in fish samples was 12.5% and ranged between 11.7 to 14.2%. Bioaccumulation factors (BAFs)
for total arsenic in fish ranged from 10.3 to 22.1, whereas BAF for inorganic arsenic ranged from 1.33 to 2.82. The mean human
health cancer risk associated with the ingestion of inorganic arsenic in the fish was estimated at 2.36 104 0.99 104, which is
over 200 times greater than a de Minimus cancer risk of 1 106. The mean human health hazard quotient associated with ingesting
inorganic arsenic in the fish was 1.22 0.52, indicating that expected human exposure exceeds the reference dose for non-cancer
health effects by 22%. These results suggest that the inhabitants in this region are being subjected to moderately elevated arsenic
exposure through the consumption of tilapia and shrimp raised in aquaculture ponds.
Keywords: Groundwater arsenic, tilapia, shrimp, bioaccumulation, health risk.

Introduction arsenic, even at low levels, increases the risk of contracting


cancer.[67]
The distribution of arsenic (As) in environmental samples Epidemiological studies have demonstrated the carcino-
is very heterogeneous, with the element being present in di- genic effect of As on humans[8] and have associated the
verse chemical forms. As a toxic and carcinogenic element, element with numerous other skin diseases.[9] Populations
arsenic poses a significant human health concern.[1] Among exposed to arsenic-contaminated water in Taiwan, Japan,
the different sources of arsenic in the environment, water- Bangladesh, West Bengal-India, Chile and Argentina have
borne arsenic probably poses the greatest threat to human higher cancer risks for skin and other organs, including
health. Naturally high dissolved-As concentrations are pri- lung, bladder, kidney and liver.[1011] A significant exposure-
marily associated with groundwater.[23] Large populations response between arsenic concentration and the mortality
around the world are at risk for toxic As-exposure from from cancers has also been reported.[78]
drinking water[4] and through the consumption of As-rich In southwestern Taiwan, As has been well documented as
seafood.[5] It has been well recognized that consumption of one of the major risk factors for blackfoot disease (BFD),
a peripheral vascular disease that causes severe gangrene in
the extremities and cancer. This disease is considered to be
Address correspondence to Jiin-Shuh Jean, Department of Earth correlated with the consumption of arsenic-contaminated
Science, National Cheng Kung University, Tainan 70101, Taiwan; groundwater by local inhabitants of this region.[7,12]
E-mail: jiinshuh@mail.ncku.edu.tw Though groundwater is no longer used these days for
Health risks for human intake of As-contaminated fish 1267
drinking or cooking, the groundwater in the region After dissection, the samples were dried in a hot air oven
is still used in commercial fish-ponds for large-scale at 70 C for about 72 h. Dry samples were converted to fine
aquaculture.[12] Since arsenic can be bio-accumulated in powder by grinding with pestle and mortar, then sieved and
aquatic organisms[13], use of high arsenic concentration stored in polyethylene bags at room temperature prior to
of groundwater for aquaculture has resulted in an accu- microwave digestion.
mulation of arsenic in cultured animals, such as fish and About 0.5 g of dry, powdered tilapia or shrimp samples
shrimp. Previous studies have noted high concentrations were placed in a Teflon bomb and 20 mL of concentrated
(>329 g g1) of total arsenic in cultured fish from the HNO3 (67%) was added drop by drop, mixed thoroughly,
arsenic-contaminated area.[12,14] and allowed to stand for a few minutes at room tempera-
Tilapia and shrimp are the most commonly consumed ture with agitation to avoid bubbling. The sample was then
fish in Taiwan and are high in nutritional protein values. microwave digested in the Teflon bomb at specific condi-
Most of the commercially important tilapia and shrimp tions (at 200220 C at 40 psi for 20 min). After complete
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

aquacultural centers in the country are located in the digestion, the acid-mixed sample was allowed to cool and
coastal region of southwestern Taiwan. Several studies have the volume made up to 50 mL after repeated washing with
reported that the use of arsenic-contaminated groundwa- de-ionized water. The liquid was then filtered through a
ter for aquaculture that may cause an accumulation of Millipore acetate cellulose membrane (0.45 m pore size)
arsenic in fish.[1213,1516] Arsenic-contaminated fish con- filtering apparatus. Extracted sample was kept in a refrig-
sumption could result in arsenic exposure to humans and erator at 4 C prior to total final arsenic quantification.
lead to adverse health effects.[17] Ling et al. have esti-
mated the risk of the intake of aquacultural milkfish from
Analytical
the ponds that use arsenic-contaminated groundwater.[13]
However, there is limited research on the cancer risk and Total arsenic content was analyzed using the Millenium Ex-
non-cancer health risk associated with consuming arsenic- callibur Fluorecence Atomic Analyzer (PS Analytical Ltd,
contaminated tilapia and shrimp. Kent, UK). Analytical accuracy was checked with reference
In the present investigation, we assess the cancer and material with precision ensured through repeated measure-
non-cancer risk of consuming aquacultural tilapia and ments. For total arsenic, standard reference solution SRM
shrimp contaminated with arsenic in southwestern Taiwan. 3103a (NIST, USA) was used. The standard solutions for
Also, the study quantifies the bioaccumulation of arsenic arsenic speciation of arsenite [As(III)], arsenate [As(V)] and
within different parts of the fish along with the distribu- dimethyl arsenic (DMA) were prepared by dissolving in wa-
tion of organic and inorganic arsenic species. These results ter from the commercially available salts: arsenite (sodium
will be valuable to physiologically based pharmacokinetic arsenite), arsenate (sodium arsenate), DMA (dimethyl ar-
(PBPK) model in assessing various internal cancers caused senic acid sodium salt, trihydrate). Chemicals including
by ingestion of arsenic-affected tilapia. As(V) and As(III) and DMA salts were purchased from
Sigma Aldrich (USA). De-ionized water used for all so-
lutions was prepared with an Auto Pure WQ500 system
(Millipore, Bedford, MA).
Nitric acid (containing 67% HNO3 ) and hydrochloric
Materials and methods
acid (containing 36% HCl) used for wet-digestion were of
super special grade. All other chemicals were of analytical
Sample collection and preparation
grade. The detection limit of arsenic species was 1 g L1
We investigated several aquaculture ponds from three dif- for all three species and was 0.1 g L1 for total arsenic.
ferent areas including Budai (B-1, B-2, B-3, B-4 and B- The coefficient of variation (CV) was calculated to test the
5), Yichu (Y-6 and Y-7) and Beimen (Be-8 and Be-9) of reliability and was found <5% in all the replicates. Quality
Southwest Taiwan (Fig. 1a). Tilapia (Oreochromis mossam- assurance was confirmed with standard reference material
bicus L.) and shrimp (Penaeus monodon L.) samples were (DORM-2, dogfish tissues) with same digestion method
collected along with pond water from selected cultivation and analytical procedure. Recovery rates ranged from 97%
ponds where arsenic-contaminated groundwater has been to 102% (Certified mean value: 18.0 1.1 g g1; Measured
used. The fish samples (kept frozen during transportation) mean value: 17.6 0.68 g g1 to 18.3 0.82 g g1).
were washed thoroughly with tap water to remove soil and For speciation of arsenic (As(III), As(V) and DMA),
other particles and finally washed with de-ionized water a coupled high performance liquid chromatography
with continuous shaking. The samples were then stored at hydride generation atomic fluorescence spectrometry
20 C until further analysis. Length and weight of each (HPLC-HG-AFS) system was used with a PSA analyzer
fish were recorded before dissection. Part of the fish tissues (Kent, UK). A P.S. Analytical model Excalibur atomic flu-
were minced and blended to get a homogenous sample and orescence spectrometer (AFS) equipped with an As hollow
prepared for analysis of arsenic speciation. Fish bone and cathode lamp (current intensities primary = 27.5; boost
head also separated for digestion to estimate total arsenic. = 35.0) and a Perma pure drying membrane for drying
1268 Kar et al.
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

Fig. 1. (a) Map showing locations of sampling sites in the southwestern part of Taiwan. (b) Schematic diagram of investigation process
to assess potential risk (CR: Cancer Risk; HQ: Hazard Quotient).

the generated hydride were utilized. Speciation of arsenic stand overnight for the separation of chloroform and wa-
was measured at 193.7 nm wavelength. Data acquisition ter/methanol layers. The water/methanol layer was evapo-
was performed with computer software (SISC). Peak sig- rated to dryness and dissolved in 5 mL of de-ionized water.
nals were recorded using a computer linked to PSA that is After filtering the filtrate was made up to 10 mL with de-
capable of both peak height and peak area measurement. ionized water and used as a water-soluble arsenic fraction.
The peak height signals were measured and the concentra-
tions of arsenic of the samples were measured against the
standard curve. Calculation of bioaccumulation factor (BAF)
Separation of the species was performed using the GBC The bioaccumulation factor (BAF), relating the concentra-
LC 1120 HPLC system which includes an autosampler, tion of arsenic in water to its level in fish[12], was used to
column oven and mobile phase degasser in addition to the estimate the propensity of arsenic accumulation in tilapia
chromatography pump. A 200 L aliquot of the sample so- and shrimp: BAF = Cf /Cw , where Cf (g g1) is the arsenic
lution was injected into the LC system (Injector: Rheodyne level in fish and Cw (g L1) is the arsenic concentration in
7725i, USA), equipped with a Hamilton PRP X100 anionic water.
column. Phosphate buffer solution at pH 6.0 was pumped
at 1 mL min1. The eluent from the chromatographic col-
umn reached the hydride generation system, where HCl Estimation of potential health risks
(2 mol L1 at 8 mL min1) and 1.5% (m/v) NaBH4 in
The human health risk associated with the ingestion of
0.4% NaOH at 3 mL min1 were introduced. The elute
inorganic arsenic in aquacultural tilapia and shrimp was
reached the gas-liquid separator and was then transferred
estimated following U.S. EPA guidelines.[1920] A schematic
to an Atomic Fluorescence Spectrometer (AFS) detector
diagram has been shown to understand the accumulation
with the help of argon flow of 300 mL min1 through an
process which raises the potential risk (Fig. 1b). Cancer
air-based Perma pure drying membrane (air flow: 2.5 L
risk (CR) and hazard quotients (HQ) were used to indicate
min1).
the magnitude of carcinogenic and non-carcinogenic hu-
man health risks, respectively. The method to estimate CR
and HQ is provided in the USEPA Guidance for Assessing
Extraction of arsenic for speciation Chemical Contaminant Data for Use in Fish Advisories,
Each sample was extracted by using mortar and pestle. A Volume 2, Risk Assessment and Fish Consumption Lim-
3 g-portion of the sample was extracted with 30 mL of its, Third edition.[1920] The equations for estimating CR
chloroform and methanol (2:1). Because the use of only and HQ are shown as follows:
organic solvents is suggested to be insufficient to extract  
CR = Cb IRF 103 CPSo EFr ED tot
water-soluble arsenic compounds, especially inorganic ar-
/ (BWa ATc) and
senicals, the residue was further extracted with 30 mL of  
de-ionized water.[18] Both chloroform-methanol and water HQ = Cb IRF 103 EFr EDtot
extracts were combined, shaken vigorously and allowed to / (RfD BWa ATn)
Health risks for human intake of As-contaminated fish 1269
where CR is the calculated cancer risk; Cb is the inorganic in feedstuffs used to feed the fish at a detection limit of 0.1
arsenic level in fish (mg kg1); IRF is the fish ingestion rate g L1. Earlier studies of Huang et al. also supported this
(g d1); CPSo is the oral carcinogenic potency slope (kg d finding of arsenic contamination in farmed fish and pond
mg1); EFr is the exposure frequency (350 d yr1); EDtot water from the arsenic-contaminated region.[14]
is the total exposure duration (30 yr); BWa is the body
weight of an adult (70 kg); ATc is the averaging time for
carcinogens (25,550 d); HQ is the hazard quotient; RfD is Bioaccumulation of arsenic in fish
the reference dose (mg kg1d1); and ATn is the averaging The bioaccumulation of arsenic in freshwater-cultured fish
time for non-carcinogens (EDtot 365 d yr1). The calcu- (tilapia and shrimp) was measured to assess the risks to
lated cancer risk and hazard quotient were compared to a human health (see section Potential health risk). Table 1
de Minimus lifetime cancer risk of 1 106 and a target represents the bioaccumulation factor (BAF) of total ar-
hazard quotient of 1.0, respectively. Values of CPSo and senic in tilapia from pond water. BAF for total arsenic was
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

RfD for arsenic (1.5 kg1 d mg1 and 3 104 mg kg1 found in the range from 10.3 to 22 in tilapia from the Budai
d1, respectively) were taken from USEPAs Integrated Risk aquacultural pond, whereas 15.1 to18.4 and 12.5 to 15.7 in
Information System (IRIS) database (www.epa.gov/IRIS). Yichu and Beimen, respectively. Estimated BAF for inor-
We evaluated potential human health risks on the basis of ganic arsenic (assuming total arsenic as inorganic arsenic
inorganic arsenic in fish since the CPSo and RfD for arsenic in pond water) was found in the range of 1.33 to 2.82.
apply to inorganic arsenic, not total arsenic. The bioaccumulation of total arsenic in fish is highly
correlated with total arsenic level of pond water (n = 10;
Statistical analysis R2 = 0.80; p < 0.05) (Fig. 2a). This relationship was found
to be in good agreement with Lin.[21] Therefore fish can
Data were presented as minimum-maximum values and be used as a bioassay indicator for surface water pollution
mean standard deviation (SD), correlation statistics, level by high concentrations of arsenic. Arsenic contents were
of significance were analyzed using the SPSS statistical soft- also analyzed in three major consumable parts of fish
ware version 13.0 (SPSS Inc.). A p-value less than 0.05 was body, namely the head, tissue and bone. Fish tissue was
considered to indicate statistical significance. Linear regres- characterized by a higher content of arsenic than fish bone
sion was used to find correlation between the arsenic level and head (Table 2).
in pond water and that in the fish body. The mean arsenic levels in fish tissue were found in the
range from 0.43 0.01 to 1.91 0.05 g g1. The mean
Results and discussion arsenic contents in fish bone and head were found in the
range from 0.33 0.01 to 1.42 0.04 g g1 and 0.21
Arsenic levels in fish, pond water and sediment 0.01 to 1.31 0.04 g g1, respectively. Arsenic content
in total fish is highly correlated with the arsenic content of
The study investigated the relationship between As levels in bone (n = 10; R2 = 0.98) compared to head (n = 10; R2 =
aquaculture pond water, sediment and cultured fish. Mean 0.97) and tissue (n = 10; R2 = 0.96) of tilapia (Fig. 2b). The
concentrations of total arsenic in the aquacultural pond variation of arsenic concentrations in different parts of the
water (n = 10) in Budai were found in the range from 29.5 tilapia body was shown in Figure 2c. Table 3 indicates that
1.10 to 75.7 1.90 g L1 in contrast to 52.3 1.60 to
58.6 1.70 g L1 and 64.6 1.80 to 71.3 1.90 g L1
for Yichu (n = 10) and Beimen (n = 10), respectively (per- Table 1. Bioaccumulation Factor (BAF) of total arsenic in tilapia
missible limit 50 g L1 for aquacultural water in Taiwan) (Units of BAF in L g1).
(Table 1). Average total arsenic in pond water was higher Total arsenic content (n = 10)
in Budai, followed by Beimen and Yichu, indicating not
much variation among the ponds. Total arsenic contents Sampling Tilapia Pond water BAF =
of 0.791.12 mg g1 were observed in pond sediments (not pond (g g1) (Cf ) (Cw )(g L1) Cf /Cw
shown in table). B-1 0.70 0.04 56.9 1.6 12.3
These findings reveal that As in pond water and sediment B-2 1.34 0.09 68.3 1.8 19.6
are important exposure media for the bioaccumulation of B-3 1.58 0.09 75.7 1.9 20.9
As in fish. The mean length of sampled tilapia (n = 10) was B-4 0.33 0.02 32.2 1.2 10.3
16.6 2.14 cm, and the mean weight was 204 25.5 g (fresh B-5 0.65 0.02 29.5 1.1 22
weight). The arsenic contents in tilapia in Budai were found Y-6 0.79 0.04 52.3 1.6 15.1
to be at an alarming level (n = 10) in the range from 0.33 to Y-7 1.07 0.08 58.6 1.7 18.3
1.58 g g1 (mean 0.92 0.52 g g1), whereas 0.79 to 1.7 Be-8 0.78 0.04 71.3 1.9 10.9
g g1 (mean 0.93 0.19 g g1) and 0.73 to 0.78 g g1 Be-9 0.73 0.02 64.6 1.8 11.3
(mean 0.76 0.03 g g1) were the concentration ranges in
BAF = Bioaccumulation Factor; Cf = Concentration in fish; Cw =
Yichu and Beimen, respectively. Arsenic was not detected Concentration in water.
1270 Kar et al.
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

Fig. 2. (a) Relation between total arsenic levels in fish and pond water samples in Budai, Yichu and Beimen in Taiwan. (b) Relation
between total arsenic levels in head, tissue and bone of aquacultural tilapia fish. (c) Box and Whisker plot representing the variation
of total arsenic levels in head, tissue and bone of tilapia.

large tilapia fish contains more total arsenic than smaller our results with these published data. Arsenic in different
ones. fish tissues were analyzed by Shah et al.[22] and showed
Arsenic content in different parts of the fish body has significant higher level in fish muscle (2.1215.2 g g1)
been studied by various researchers and we can compare compared to gills (1.0110.4 g g1), mouth pieces
(1.0118.6 g g1), intestine (1.0111.2 g g1), and liver
(3.5110.9 g g1). Jankong et al. reported that the As level
Table 2. Total arsenic content in head, muscle and bone of tilapia in contaminated areas of Thailand as high as 0.050.81 g
cultured using contaminated groundwater (n = 10).

Arsenic in tilapia (g g1) Table 3. Total arsenic content in different parts of large and small
tilapia and shrimp cultured using contaminated groundwater (n
Sampling pond Head Muscle Bone
= 10).
B-1 0.54 0.02 0.92 0.03 0.65 0.02
Arsenic in different parts of fish (g g1)
B-2 1.13 0.03 1.72 0.05 1.21 0.04
B-3 1.31 0.04 1.91 0.05 1.42 0.04 Fish Head Tissue Bone
B-4 0.21 0.01 0.43 0.01 0.33 0.01
B-5 0.48 0.01 0.78 0.02 0.69 0.02 Tilapia(large): Body 0.63 0.01 1.03 0.01 0.76 0.01
Y-6 0.59 0.02 1.12 0.03 0.66 0.02 weight > 200 g
Y-7 0.81 0.02 1.31 0.04 1.05 0.03 Tilapia (small): Body 0.58 0.01
Be-8 0.69 0.02 0.84 0.02 0.72 0.02 weight < 100 g
Be-9 0.57 0.02 0.93 0.03 0.68 0.02 Shrimp 0.36 0.01
Health risks for human intake of As-contaminated fish 1271

g1 in edible fish muscle.[23] In comparison to our results, compounds being more toxic than their organic counter-
it was observed that the arsenic level in fish tissues were parts[5,28].
significantly lower in contaminated areas of Taiwan. An
arsenic level in fish muscle was higher than other parts
like bone and head, which is in agreement with Chan and Potential human health risk
Huff.[24] The accumulation and distribution of As in the Our data show that tilapia and shrimp bioaccumulate ar-
fish body are probably controlled by methylation capacity senic while being cultured in ponds in southwestern Taiwan.
(which likely changes with exposure), period of metabolism Local inhabitants are known to consume these species and
and As-excretion.[22] hence are exposed to arsenic through ingestion. This expo-
sure, in turn, represents a health risk to these inhabitants
based upon the toxicity of arsenic. A conceptual diagram
Arsenic species in fish shows the mechanism of arsenic contamination and accu-
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

mulation in aquacultural fish and the associated risk to


Table 4 shows concentrations of the three major arsenic people who then consume the fish (Fig. 3). Cancer risk and
species in tilapia tissue, As(III), As(V), and DMA. Results non-cancer risk (expressed as a hazard quotient HQ) were
showed that DMA was present in a higher amount than calculated following the approach described in the meth-
both the inorganic species As(III) and As(V). DMA rages ods section, where local consumption rates of tilapia were
from 0.134 0.009 to 0.663 0.024 mg kg1, whereas considered.
As(III) and As(V) ranged from 0.012 0.001 to 0.053 Based on a field survey, the consumption of tilapia (fish
0.002 mg kg1 and 0.031 0.001 to 0.142 0.006 mg ingestion rate: IRF) of 56 local residences of the three stud-
kg1, respectively. The fish from Budai showed higher lev- ied areas was estimated to range between 182 26.3 and
els (mean 0.5 0.03 g g1) of all As species compared 315 52.1 g d1. The mean value, which was used for the
to Yichu (mean 0.48 0.02 g g1) and Beimen samples risk calculations, was 242 11.6 g d1. The CR for con-
(mean 0.41 0.02 g g1). DMA was found the major suming tilapia from the different ponds ranges from 0.92
species (4045%) among the three species, whereas inor- 105 to 4.16 104 (Table 5), with a mean of 2.36
ganic As(III) and As(V) were found in the range of 11.7 to 104 0.99 104. This average increase in cancer risk is
14.2%, which is higher than reported in the previous study over 200 times greater than a de Minimus lifetime risk of
of Huang et al.[14] 1 106. In a similar way, the non-cancer health risk for
The inorganic arsenic level (44.1 10.2%) in milkfish intake of the tilapia (expressed as HQ) ranged from 0.48 to
is much higher than that in the seafood and tilapia.[25] It 2.15, with a mean of 1.22 0.52 (Table 5). The CR values
demonstrates that tilapia might have a higher ability to in Budai were found to range between 0.92 105 to 4.16
covert the inorganic arsenic into organic forms, and arsenic 104 (mean 2.47 104 1.34 104); 2.09 104 to
in ambient water is often in an inorganic form. The previ- 2.83 104 (mean 2.46 104 0.52 104) for Yichu;
ous studies also reported that among the arsenic species in and 1.89 104 to 2.07 104 (mean 1.98 104 0.13
fish, organic species like arsenobetaine and DMA predom-
inate [2627], though they were supposed to be less harmful
as they are quickly excreted from human body. Normally,
the toxicity of arsenic species varies according to their
oxidation state and organic form, with inorganic arsenic

Table 4. Major arsenic species in tissue of tilapia (Oreochromis


mossambicus L.) where n = 10.

Arsenic species in tissue (g g1)


Sampling pond As(III) As(V) DMA

B-1 0.025 0.001 0.063 0.003 0.298 0.013


B-2 0.046 0.002 0.121 0.008 0.563 0.021
B-3 0.053 0.002 0.142 0.006 0.663 0.024
B-4 0.012 0.001 0.031 0.001 0.134 0.009
B-5 0.023 0.001 0.062 0.002 0.274 0.012
Y-6 0.027 0.002 0.071 0.003 0.332 0.015
Y-7 0.037 0.002 0.096 0.005 0.447 0.019 Fig. 3. Conceptual diagram of arsenic contamination and ac-
Be-8 0.027 0.001 0.070 0.003 0.325 0.013 cumulation in aquacultural fish and associated health risk to
Be-9 0.024 0.002 0.065 0.003 0.302 0.011 humans who ingest the fish (color figure available online).
1272 Kar et al.
Table 5. CR (Cancer Risk) and HQ (Hazard Quotient) associ- the full extent and magnitude of arsenic contamination in
ated with the ingestion of inorganic arsenic in tilapia raised in aquacultural fishes in areas where contaminated ground-
aquaculture ponds feed with contaminated groundwater. water is used in the aquaculture ponds. In addition, ways
Inorganic arsenic in of eliminating or at least reducing the exposure and risk
Pond tilapia (g g1) CR HQ should be considered.

B-1 0.088 1.88 104 0.97


B-2 0.167 3.56 104 1.86 Conclusion
B-3 0.195 4.16 104 2.15
B-4 0.043 0.92 105 0.48 Aquacultural fish (tilapia and shrimp) from groundwater-
B-5 0.085 1.81 104 0.94 cultured ponds in southwestern Taiwan (Budai, Yichu and
Y-6 0.098 2.09 104 1.08 Beimen) represents a potential health risk for human As ex-
2.83 104
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

Y-7 0.133 1.47


posure. Water samples from all of the aquacultural ponds
Be-8 0.097 2.07 104 1.07
had arsenic concentrations greater than 10 g L1, which is
Be-9 0.089 1.89 104 0.98
the USEPA mandated safe drinking-water limit. The can-
cer and non-cancer health risks associated with consuming
aquacultural fish were moderate to high compared to de
104) for Beimen. HQ values in Budai were found in the Minimus risks. The inhabitants in the arsenic-contaminated
range from 0.48 to 2.15 (mean 1.28 0.69); 1.08 to 1.47 area, who consume arsenic-contaminated tilapia, are ex-
(mean 1.28 0.27) for Yichu; and 0.98 to 1.07 (mean 1.03 posed chronically to arsenic pollution with carcinogenic
0.063) for Beimen. and non-carcinogenic risks. It is of concern that As-rich
The CR and HQ values indicate that consumption of groundwater is commonly used for aquaculture in the As-
arsenic contaminated tilapia grown in groundwater fed contaminated area in Taiwan. Many other cultured fish
aquacultural ponds increases both cancer and non-cancer from this area may also be contaminated by arsenic; how-
risks to people who consume these fish. In case of shrimp ever few potential risk assessments have been done. A
the health risk was not assessed due to lack of informa- greater understanding of the extent and magnitude of this
tion on regular consumption. We suggest that government problem is warranted.
regulatory agencies consider limitations on the use of As-
contaminated groundwater in the aquaculture of fish, or
alternatively, to require a high level of treatment of the Acknowledgments
groundwater prior to its use in aquaculture.
Taiwanese population exposed to arsenic show an in- The authors wish to thank the National Science Council
crease in fatal internal organ cancers as well as an increase of Taiwan for partial financial support. The authors also
in skin cancer.[7] These cancers, as well as the BFD epidemic thank Prof. Subhas Chandra Santra (Department of En-
of the 1950s and 1960s, were correlated with high levels of vironmental Science, University of Kalyani, West Bengal,
arsenic in drinking water. Several studies have been carried India) and Prof. Arabinda Das (Former Vice-Chancellor
out on the doseresponse relationship between the arsenic of University of Kalyani, West Bengal, India) for their
level in drinking water[6], and most of these studies involve valuable suggestions. Finally, the authors thank Dr. Tomas
the relations between arsenic in water and human health. Kulp at the U.S. Geological Survey (USGS), Menlo Park,
However, there has been relatively little attention given to CA 94025, USA for language editing and his scientific com-
As exposure from a food safety perspective. Some recently ments.
published reports on farmed fish have involved analyses
of total arsenic accumulation in cultured fish,[16,29] but few References
of them have examined the risk based on arsenic expo-
sure. Liao and Ling carried out a risk analysis to quantify [1] Tsai, S.Y.; Chou, H.Y.; The, H.W.; Chen, C.M.; Chen, C.J. The
the inorganic arsenic bioaccumulation in cultured tilapia effects of chronic arsenic exposure from drinking water on the neu-
and mullet from the arsenic-contaminated area in Taiwan, robehavioral development in adolescence. Neurotoxicol. 2003, 24,
747753.
as well as the risk associated with consumption of these [2] Smedley, P.L.; Kinniburgh, D.G. A review of the source, behavior
fish.[14] and distribution of arsenic in natural waters. Appl. Geochem. 2002,
They reported that the ninety-fifth percentile of poten- 17, 517568.
tial health risk associated with consuming these fish ranged [3] Kar, S.; Maity, J.P.; Jean, J.-S.; Liu, C.-C.; Nath, B.; Yang, H.-J.;
from 1.92 104 5.25 104 for Taipei city residents eat- Bundschuh, J. Arsenic-enriched aquifers: Occurrences and mobi-
lization of arsenic in groundwater of Ganges Delta Plain, Barasat,
ing tilapia harvested from Hsuehchia fish farms, whereas West Bengal, India. Appl. Geochem. 2010, 25, 18051814.
for subsistence fishers the risk was 7.36 1041.12 [4] Liu, C.W.; Jang, C.S.; Liao, C.M. Evaluation of arsenic contam-
103. That study, incorporating our study, suggests that an ination potential using indicator kriging in the Yun-Lin aquifer
environmental monitoring program is needed to estimate (Taiwan). Sci. Tot. Environ. 2004, 321, 173188.
Health risks for human intake of As-contaminated fish 1273
[5] Donohue, J.M.; Abernathy, C.O. Exposure to inorganic arsenic [17] Falco, G.; Llobet, J.M.; Bocio, A.; Domingo, J.L. Daily intake of ar-
from fish and shellfish. In Arsenic exposure and health effects; Chap- senic, cadmium, mercury, and lead by consumption of edible marine
pell, W.R.; Abernathy, C.O.; Calderon, R.L.; Eds.; Elsevier, BV, species. J. Agric. Food. Chem. 2006, 54, 61066112.
1999; 8998. [18] Francesconi, K.A.; Kuehnelt, D. Determination of arsenic species:
[6] Yu, W.H.; Harvey, C.M.; Harvey, C.F. Arsenic in groundwater in A critical review of methods and applications, 20002003. Analyst
Bangladesh: A geostatistical and epidemiological framework for 2004, 129, 373395.
evaluating health effects and potential remedies. Water Resour. Res. [19] USEPA. Guidance for assessing chemical contaminant data for use
2003, 39, 1146. in fish advisories. Vol. 2-Risk assessment and fish consumption limits.
[7] Chen, C.L.; Hsu, L.I.; Chiou, H.Y.; Hsueh, Y.M.; Chen, S.Y.; Wu, 3rd ed. Washington DC: USEPA. EPA 823-B-00-008, 2000.
M.M. Ingested arsenic, cigarette smoking, and lung cancer risk: a [20] Greene, R; Crecelius, E. Total and inorganic arsenic in Mid-Atlantic
follow-up study in arseniasis-endemic areas in Taiwan. JAMA 2004, marine fish and shellfish and implications for fish Advisories. Integ.
292, 29842990. Environ. Asses. Manage. 2006, 2, 344354.
[8] Chiou, H.Y.; Hsueh, Y.M.; Liaw, K.F.; Horng, S.F.; Chiang, M.H.; [21] Lin, M.C. Risk assessment on mixture toxicity of arsenic, zinc
Pu, Y.S.; Lin, J.S.N.; Huang, C.H.; Chen, C.J. Incidence of internal and copper intake from consumption of milkfish, Chanos chanos
Downloaded by [IIT Indian Institute of Technology - Mumbai] at 09:59 07 September 2017

cancers and ingested inorganic As: a seven-year follow-up study in (Forsskal), cultured using contaminated groundwater in southwest
Taiwan. Cancer Res. 1995, 55, 12961300. Taiwan. Bull. Environ. Cont. Toxicol. 2009, 83, 125129.
[9] IPCS. Environmental health criteria on arsenic and arsenic com- [22] Shah, A.Q.; Kazi, T.G.; Arain, M.B.; Jamali, M.K.; Afridi, H.I.;
pounds. In Environmental Health Criteria Series, No. 224: Arsenic Jalbani, N.; Baig, J.A.; Kandhro, A. Accumulation of arsenic in
and arsenic compounds, WHO, Geneva, 2001; 521. different fresh water fish species potential contribution to high
[10] Mandal, B.K.; Suzuki, K.T. Arsenic round the world: A review. arsenic intakes. Food Chem. 2009, 112, 520524.
Talanta 2002, 58, 201235. [23] Jankong, P.; Chalhoub, C.; Kienzl, N.B.; Goessler, W.; Francescon,
[11] Lee, J.J.; Jang, C.S.; Wang, S.W.; Liu, C.W. Evaluation of poten- K.A.; Visoottiviseth, P. Arsenic accumulation and speciation in
tial health risk of arsenicaffected groundwater using indicator freshwater fish living in arsenic-contaminated waters. Environ.
kriging and dose-response model. Sci. Tot. Environ. 2007, 384, Chem. 2007, 4, 1117.
151162. [24] Chan, P.C.; Huff, J. Arsenic carcinogenesis in animals and in hu-
[12] Lin, M.C.; Cheng, H.H.; Lin, H.Y.; Chen, Y.C.; Chen, Y.P.; Liao, mans: mechanistic, experimental, and epidemiological evidence. J.
C.M.; Chang-Chien, G.P.; Dai, C.F.; Han, B.C.; Liu, C.W. Arsenic Environ. Sci. Health 1997, 15, 83122.
accumulation and acute toxicity in milkfish (Chanos chanos) from [25] Lin, M.C.; Liao, C.M. Assessing the risks on human health as-
blackfoot disease area in Taiwan. Bull Environ. Contam. Toxicol. sociated with inorganic arsenic intake from groundwater-cultured
2004, 72, 248254. milkfish in southwestern Taiwan. Food Chem. Toxicol. 2008, 46,
[13] Ling, M.P.; Liao, C.M.; Tsai, J.W.; Chen, B.C. A PBPK/PD 701709.
modeling-based approach can assess arsenic bioaccumulation in [26] Liu, C.W.; Liang, C.P.; Lin, K.H.; Jang, C.S., Wang, S.W.; Huang,
farmed tilapia (Oreochromis mossambicus) and human health risks. Y.K.; Hsueh, Y.M. Bioaccumulation of arsenic compounds in aqua-
Integr. Env. Assess. Manag. 2005, 1, 4054. cultural clams (Meretrix lusoria) and assessment of potential car-
[14] Huang, Y.K.; Lin, K.H.; Chen, H.W.; Chang, C.C.; Liu, C.W.; Yang, cinogenic risks to human health by ingestion. Chemosphere 2007,
M.H.; Hsueh, Y.M. Arsenic species contents at aquaculture farm 69, 128134.
and in farmed mouthbreeder (Oreochromis mossambicus) in black- [27] Maher, W.; Goesler, W.; Kirby, J.; Raber, G. Arsenic concentrations
foot disease hyperendemic areas. Food Chem. Toxicol. 2003, 41, and speciation in the tissues and blood of sea mullet (Mugil cephalus)
14911500. from Lake Maxquarie NSW, Australia. Marine Chem. 1999, 68,
[15] Liao, C.M.; Ling, M.P. Assessment of human health risks for 169182.
arsenic bioaccumulation in tilapia (Oreochromis mossambicus) [28] Phillips, D.J.H. Arsenic in aquatic organisms: A review, emphasizing
and large-scale mullet (Liza macrolepis) from blackfoot disease chemical speciation. Aquat. Toxicol. 1990, 16, 151186.
area in Taiwan. Arch. Environ. Contam. Toxicol. 2003, 45, [29] Jang, C.S.; Liu, C.W.; Lin, K.H.; Huang, F.M.; Wang, S.W. Spatial
264272. analysis of potential carcinogenic risks associated with ingesting
[16] Ling, M.P.; Liao, C.M. Risk characterization and exposure assess- arsenic in aquacultural tilapia (Oreochromis mossambicus) in black-
ment in arseniasis-endemic areas of Taiwan. Environ. Int. 2007, 33, food disease hyperendemic areas. Environ. Sci. Technol. 2006, 40,
98107. 17071713.

You might also like