Environ Monit Assess DOI 10.1007/s10661-014-3660-6

Hazard assessment of metals in invasive fish species of the Yamuna River, India in relation to bioaccumulation factor and exposure concentration for human health implications Atul K. Singh & Sharad C. Srivastava & Pankaj Verma & Abubakar Ansari & Ambrish Verma Received: 18 July 2013 / Accepted: 21 January 2014 # Springer International Publishing Switzerland 2014

Abstract Monitoring of heavy metals was conducted in the Yamuna River considering bioaccumulation factor, exposure concentration, and human health implications which showed contamination levels of copper (Cu), lead (Pb), nickel (Ni), and chromium (Cr) and their dispersion patterns along the river. Largest concentration of Pb in river water was 392 μg L−1; Cu was 392 μg L−1 at the extreme downstream, Allahabad and Ni was 146 μg L−1 at midstream, Agra. Largest concentration of Cu was 617 μg kg−1, Ni 1,621 μg kg−1 at midstream while Pb was 1,214 μg kg−1 at Allahabad in surface sediment. The bioconcentration of Cu, Pb, Ni, and Cr was observed where the largest accumulation of Pb was 2.29 μg kg−1 in Oreochromis niloticus and 1.55 μg kg−1 in Cyprinus carpio invaded at Allahabad while largest concentration of Ni was 174 μg kg−1 in O. niloticus and 124 μg kg−1 in C. carpio in the midstream of the river. The calculated values of hazard index (HI) for Pb was found more than one which indicated human health concern. Carcinogenic risk value for Ni was again high i.e., 17.02×10−4 which was larger than all other metals studied. The results of this study indicated bioconcentration in fish due to their exposures to heavy metals from different routes which A. K. Singh (*) : S. C. Srivastava : P. Verma : A. Ansari Exotic Fish Germplasm Section of Fish Health Management, National Bureau of fish Genetic Resources, Canal Ring Road, P.O. Dilkusha, Lucknow 226002 Uttar Pradesh, India e-mail: [email protected] A. Verma Uttar Pradesh Pollution Control Board, Lucknow 226016, India

had human health risk implications. Thus, regular environmental monitoring of heavy metal contamination in fish is advocated for assessing food safety since health risk may be associated with the consumption of fish contaminated through exposure to a degraded environment. Keywords Heavy metals . Invasive fish . Health index . Risk assessment . Yamuna River

Introduction The environment is continuously loaded with heavy metals released by urban communities and industries. Environmental pollution containing hazards of metal contamination represents a major problem both in developed and under developed countries (Kazi et al. 2009; Ozden 2010). Heavy metal in aquatic environments is hazardous because once the metals enter the aquatic environment they cannot be destroyed rather they change from one form to another persisting in the aquatic environment (WHO 2011). The presence of metals in a segment of an aquatic ecosystem does not, by itself, indicate injurious effects rather elevated concentrations of heavy metals with industrial activities and household waste may have human health hazards in addition to environmental problem. Study on the relative contribution of ingestions to the bioaccumulation of metals in invasive fish has been reported that concentrations of the metals in fish muscle had a significant adverse effect in human health (Singh et al. 2012).

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Recent attention has been paid in developed and developing countries on the subject of anomalous distribution of metals in the waters, sediments, and fishes which are fundamentally important for understanding the behavior of the metals and, also, the swapping between the sediments and the water column (Kazi et al. 2009; Ozden 2010). However, in India, only a few references are available on the speciation of metals in rivers and its effect on health risk (Nayaka et al. 2009; Bhattacharyya et al. 2010; Rejomon et al. 2010; Kumar and Mukherjee 2011; Singare et al. 2012). In recent years, there has been a growing concern of increased pollution of the Yamuna River in India (Mishra 2010; Upadhya et al. 2011) where hardy fishes such as Oreochromis niloticus and Cyprinus carpio have invaded and now contributing substantially to the fishery (Singh and Lakara 2011; Singh et al. 2013). The Yamuna River receives treated and untreated effluents from various towns and cities located on its banks (Bhargawa 2006; Namdev and Singh 2012). As a result, some pockets of the river are believed to be intensely polluted and serve as reservoirs of a variety of organic and inorganic pollutants. Some of the tributaries, which meet Yamuna River at different points also, transfer their pollution load to it (CPCB 2007). The Yamuna River is sustaining a large population of the northern region of India; however, there is hardly any systematic study on the metal fractionation in sediments of river. The presence of metal pollutant in fresh water is known to disturb the delicate balance of the aquatic ecosystem. Fish are notorious for their ability to concentrate heavy metals in their muscles (Singh et al. 2012) and they also play important role in human nutrition. Therefore, it is important to carefully screen the bioconcentration factor and exposure concentration of heavy metals to ensure that unnecessary elevated level of some toxic metals is not being transferred to human through fish consumption i.e., health risk (Singh et al. 2012). It is important to mention that degraded aquatic environment is becoming a source of fetching fish as food to human. Contaminated aquatic ecosystems have yet to be identified for their risk to aquatic life and, ultimately, to humankind. The presence of metal in aquatic environment may lead to accumulation of metals in aquatic organisms through different mechanisms: via the direct uptake from water through gills or skin (bioconcentration), via the uptake of suspended particles (ingestion), and via the consumption of contaminated food (biomagnification) (Oost et al. 2003). In the light of the above facts, it was considered worthwhile to study the bioaccumulation factor of heavy metals in hardy

O. niloticus and C. carpio that invaded into the Yamuna River. Keeping in view of different exposure routes which included the sediment and water, the ecotoxic potential of the present metals was determined in relation to human health. In this paper, hazard assessment of heavy metals has been carried out in the Yamuna River in relation to bioaccumulation factor and exposure concentration to determine the human health risk.

Materials and methods Sampling sites The study was carried out in the River Yamuna of Uttar Pradesh, India which is a potential resource for capture fisheries and forms the lifeline for rural economy and environment of the area. The Yamuna River originates from hilly glaciers of Yamunotri but the stretch covered in this study exists in the plains starting from Saharanpur to Allahabad forming a length of about 900 km. The sampling was done from the following six sites, details of which are the following: S1 Agra city situated at N 27°13.718′ latitude E 077°58.358′ longitude. Nineteen drains collect high portion of wastewater and discharge effluents from leather tanneries as well as dying industries in the Yamuna River water at the Agra city (Mishra 2010; Upadhyay et al. 2011). S2 Etawah where the site was located before the confluence of River Chambal, situated at N 26°51.095′ latitude E 078°48.951′ longitude. The industrial effluents discharging industries include paper, sugar as well as sewage water from the city. Substantial quantity of river water is lifted by the farmers for irrigating their fields (CPCB 2007; Mishra 2010; Upadhya et al. 2011). S3 Kalpi where the site was located after the confluence of Sind River and situated at N 26°07.657′ latitude E 079°45.535′ longitude. There are so many small and big drains that bring the sewage to Yamuna River. Approximately 100 conventional industrial units are present and their effluent is discharged into the river without any treatment (Mishra 2010; Upadhya et al. 2011). S4 Hamirpur situated at N 25°57.657′ latitude and E 080°09.057′ longitude from the river where city’s water supply is drawn from the river. It is also

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polluted, showing black color because of the decomposition of organic waste discharged by the industries and domestic sewage (Mishra 2010; Upadhya et al. 2011). S5 Allahabad site was located before the confluence of Yamuna River with River Ganga, and situated at N 25°25.134′ latitude E 081°49.539′ longitude. Sewage waste is the main discharge. S6 Confluence of the Ganga and the Yamuna at Allahabad located after the confluence of the Yamuna River with the Ganga River at Sangam. This station gave an idea of the cumulative effect of pollution of the Yamuna River and the Ganga at Allahabad, situated at N 25°25.696′ latitude E 081°52.674′ longitude. Industrial influence and untreated sewage are being discharged in the Yamuna River in Allahabad.

Sampling procedure and analysis The present study was carried out in the Yamuna River between May 2011 and April 2012 where six samples each consisting of fish, water, and sediment were randomly collected every two months throughout the year from each site. The metal contaminants in water, soil, and fish tissues collected from each sampling site were analyzed following the Standers method (APHA 2005). Each fish species O. niloticus and C. carpio were captured at selected sampling sites using drag net. The netted fish specimens were put in a picnic box with some quantity of river water and brought to the laboratory for examination. Fish muscle of each fish was properly cleaned by rinsing with distilled water to remove debris planktons and other external adherent. It was then drained under folds of filter, weighed, wrapped in aluminum foil, and then frozen at −10 °C prior to analysis. We examined four metals namely Cu, Pb, Ni, and Cr in the water of the Yamuna River and also in 216 tissue samples of fish to perform health-based risk analysis, and sediment from each study site was collected into pre-cleaned polythene bag using a stainless van-ven grab, air dried, and then sieved with 200 mm mesh screen. 5 g of the sediment was taken into 150-mL conical flasks. 50 mL of 0.1-M HCl was added and the flask was agitated on an orbital shaker for 30 min at 200 rpm. The water samples of each site was collected in sterilized polyethylene bottles, brought to the laboratory, and kept in refrigerator until analysis. 200 mL of

this stored water sample was taken in conical flask and evaporated to 20 mL on a hot plate at controlled temperature of 80 °C. Thereafter, 3-mL concentrated HCl (35 %) and 1-mL concentrated HNO3 (65 %) were added and allowed to continue boiling till the volume reduced to 5 mL. In the case of any sedimentation, concentrated HCl was added and boiled for 1 min. Samples were then extrapolated to 25 mL using deionized water and stored in a plastic reagent bottle for further analysis. Similarly, muscle tissues of fishes were collected and washed with double-distilled water and put in petri dishes to dry at 120 °C until reaching a constant weight. One gram of dried tissue (in three replicates) was then digested with di-acid (HNO3 and HClO4 in 2:1 ratio; Canli and Atli 2003) on a hot plate set at 80 °C (gradually increased) until all materials were dissolved. Digested samples were diluted with doubledistilled water appropriately in the range of the standards, which were prepared from the stock standard solution of the metals (Sd-Fine). Metal concentrations in the samples were measured using a UNICAM-flame atomic absorption spectrophotometer (AAS, Model 2380, PerkinElmer, Inc. Norwalk, CT, USA). The results were expressed as microgram per kilogram dry weight of fish tissue and microgram per liter for water, respectively. The detection limit for Cu, Pb, Ni, and Cr was 0.02, 0.1, 0.025, and 0.02 μg, respectively. Human health risk assessment was carried out in three stages: (1) hazard identification, (2) exposure assessment, and (3) risk characterization (Yongli et al. 2010; Singh et al. 2012). The hazard identification was done by monitoring of heavy metals in river water as well as fish muscle as described above. For quantification of exposure in relation to consumption of heavy metals, a multiple pathway exposure model (SEDISOIL) was used (Harma et al. 1999). The equation in the next section was used to calculate exposure. Calculation of bioaccumulation factor (BAF) The bioaccumulation factor (BAF), relating the concentration of metal in water and surface sediment to its level in fish (Lin et al. 2004), was used to estimate the propensity of metal accumulation in O. niloticus and C. carpio. It was calculated using the formulae: (i) BAF=Cf/Cw, where Cf (microgram per gram) was the metal level in fish and Cw (microgram per liter) was the metal concentration in water.

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(ii) BAF=Cf/CS, where Cs (microgram per gram) was the metal concentration in surface sediment. Risk assessment was performed using the formula (Harma et al. 1999)
Ingestion of contaminated sediment mg kg−1 day−1 ¼

CS  IRs  EF  AF BW

ð1Þ

where CS=concentration of the contaminant in sediment (milligram per kilogram per dry weight), IRs= ingestion rate of sediment (kilogram per dry weight exposure day), AF=absorption factor (unitless), and BW=body weight (kilogram).
Ingestion of surface water mg kg−1 day−1 ð2Þ ¼

CW  IRw  EF  AF BW

where CW=concentration of the contaminant in surface water (milligrams per liter) and IRw=ingestion rate of surface water (liter per exposure day).
Ingestion of suspended material mg kg−1 day−1 ð3Þ ¼

CM  CMW  IRw  EF  AF BW

where CM = concentration of the contaminant in suspended matter (milligram per kilogram per dry weight) and CMW=suspended matter content of surface water (kilogram per liter). Dermal contact with contaminated sediment mg kg−1 day−1




CS  SAs  AD  ASs  Mf  EDs  EF  AF ð4Þ BW

where SAs=dermal surface area for sediment exposure (square meter), AD=dermal adherence rate for sediment (milligram per square centimeter), ASs=dermal absorption rate for sediment (litter per hour), Mf=matrix factor (unitless), and EDs=exposure duration from dermal exposure to sediment (hour per day ). −1

Dermal contact with contaminated surface water mg kg day

CW  SAw  ASw  EF  EDw  AF BW

ASw ¼ 5000  ð0:038 þ 0:153  Kow Þ 5000 þ ð0:038 þ 0:153  Kow Þ

−1




ð5Þ

exp ð−0:016  MÞ 1:5

ð6Þ

where SAw=dermal surface area for exposure in surface water (square meter), ASw=dermal absorption rate for exposure in surface water [(mg m−2)/(mg L−1) h−1], EDw=exposure duration from dermal exposure to surface water (hour per day), Kow =octanol/water partition coefficient, and M=molecular weight (grams per mole). Ingestion of fish mg kg−1 day−1




¼ CF  IRf  FI  AF BW

ð7Þ where CF=concentration of the contaminant in fish [milligram per kilogram fresh weight (fw)], IRf=ingestion rate of fish (kilogram per fresh weight per day), and FI=fraction contaminated (unitless). Calculated heavy metal exposure levels were compared with the tolerable daily intake (TDI). The TDI refers to the reference dose of a substance that can be taken in daily without identifiable risk of lifetime exposure. Additionally, the hazard index was calculated, which referred to the ratio of the calculated lifetime daily exposure divided by the reference dose (TDI). Daily exposure (milligram per kilogram per day) averaged over a lifetime (e.g., 70 years) was calculated as TDI ¼

þ 64  daily exposure : 7

Risk characterization was considered separately for carcinogenic and non-carcinogenic effects of metals and included discussion of factors that may result in either an over estimation or an underestimation of the risks for the Yamuna River (Fig. 1). Potential non-carcinogenic risks of exposure to contaminants in fish muscle were of potential concern and were evaluated by comparison of the estimated contaminant intakes from each exposure route with the reference dose (RfD) to produce the hazard index (HI), defined as follows (USEPA 1998): HI ¼ CDI=RfD; where HI was the hazard index (unitless) and RfD was the reference dose (milligram per kilogram per day). The HI assumed that there was a level of exposure (i.e., RfD) below which it was unlikely for even sensitive populations to experience adverse health effects. There may be a concern arising for the potential no carcinogenic effects if the HI exceeds one (unity).

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Fig. 1 Sampling locations in the Yamuna River h

mg kg−1 day−1


−1 i

Carcinogenic risk

Carcinogenic risk ðCRÞ ¼ TDI  Slope factor

Risk-specific doses were derived from the slope factor or unit risk to estimate the dose associated with a specific risk level (USEPA 2004). Carcinogenic risks were estimated as the incremental probability of an individual developing cancer over a lifetime as a result of exposure to a potential carcinogen; the following linear low dose carcinogenic risk equation was used for each exposure route (Li Yongli et al. 2010):

If a site has multiple carcinogenic contaminants, cancer risks for each carcinogen and each exposure route are added (assuming additive effects) and compared with the accepted risk. The reference dose (RfD) and carcinogenic potency slope factor (CPS) were used for health risks evaluation as provided by USEPA (2011). The cancer slope factors for ingested metals are likely to be without appreciable

:

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risk of deleterious effects during a lifetime (averaging time of 365 days year−1 for 70 years).

Results Water In the Yamuna River, the observed concentrations of Cu, Pb, Ni, and Cr in water showed that the level of Cu was highest at S1 and minimum at S6 site indicating a decreasing trend downstream of the river (Fig. 2). The level of Pb was more or less similar from Agra to Etawah but it was highly elevated at Allahabad, the extreme end of the downstream. However, the level of Cr declined from S1 to S6 sites. Site S2 showed the largest level of Ni as compared to all other sites. The level of Ni was elevated mainly at Etawah while its concentration remained nearly comparable at other places. Cr was found absent at Allahabad, the tail end downstream (Fig. 2).

Acceptable risk distribution The lower end of the range of acceptable risk distribution is defined by a single constraint on the 95th percentile of risk distribution that must be equal or lower than 10−6 for carcinogens and may be up to 10−4 in some circumstance. The health protection standard of lifetime risk for HI is one (USEPA 2011).

Statistical analysis Data are expressed as mean depending on the sampling and statistics of parameters used in the exposure model in the health risk estimations (Table. 1). The carcinogenic risk was calculated with the help of risk calculator (www.ajdesigner.com).

Surface sediment When the concentration of four metals Cu, Pb, Ni, and Cr was calculated in the surface sediment, it was found

Table 1 Statistics of input parameter in the health risk estimations Parameters

Unit

Value

References

Ingestion rate of sediment (IRs)

kg dw exposure day−1 (dw=dry weight) kg f day−1 (fw=flesh weight)

0.35×10−3

Harma et al. (1999)

0.055

Heijna and Hof (1993)

Ingestion rate of fish (IRf)

−1

−3

Ingestion rate of surface water (IRw)

Liter exposure day

50×10

Absorption factor (AF)

Unit less

1

Harma et al. (1999)

Dermal absorption rate (Ass)

L h−1

0.005

Hawley (1985)

Dermal surface area for sediment exposure (SAs) Dermal surface area for exposure in surface water (Saw) Dermal adherence rate for sediment (AD)

m2

0.28

Hawley (1985)

m2

1.80

Veerkamp and Ten Berge (1990)

mg−1 cm2

3.75

Veerkamp and Ten Berge (1990)

Matrix factor (Mf)

Unit less

0.15

Hawley (1985)

30

Harma et al. (1999)

−1

Van wijnen (1982)

Exposure frequency (EF)

Days

Body weight (BW)

kg

56

Veerkamp and Ten Berge (1990)

Suspended matter content of surface water (CMW) Exposure duration to sediment (EDs)

kg L−1

30×10−6

Riza (1989)

h day−1

8

Hawley (1985)

Exposure duration in surface water (EDw)

h day−1

1

Harma et al. (1999)

Fraction contaminated (Fl)

Unit less

0.5

Fiore et al. (1989)

1

Allison (2005)

Octonal/water partition coefficient (Kow)

−1

L kg

365 days

Environ Monit Assess Fig. 2 Concentration of metals in the Yamuna River Water

that the concentration of Cu was largest at S1 while it was absent in extreme downstream. Maximum concentration of Pb was present at Allahabad while it was minimum at Etawah. Calculated amount of Ni was found maximum at S2 (Etawah) and minimum at S5 site. Maximum concentration of Cr was present at S3 while it was absent at S5 and S6 sites in extreme downstream (Fig. 3). Fish Bioconcentrations of all the four metals i.e., Cu, Pb, Ni, and Cr in the muscle of O. niloticus were detected at all sampling sites (Fig. 4). Among the metals detected, the largest concentration of Cu was present at Hamirpur in O. niloticus and it reduced considerably in extreme downstream at Allahabad. However, concentration of Pb was maximum in O. niloticus captured from Allahabad, while it was minimum at the confluence of

Fig. 3 Concentration of metals in surface sediment of the Yamuna River

the Ganga at Allahabad. Maximum amount of Ni was present in O. niloticus at Etawah followed by Hamirpur. Largest concentration of Cr in O. niloticus was observed in midstream at Agra, and it was absent in extreme downstream at Allahabad. The concentration of all the four metals was also detected in C. carpio from Agra to downstream at Hamirpur (Fig. 5). Maximum concentration of Cu was present in C. carpio, collected from S3 (Kalpi) while it was absent at Allahabad. Maximum amount of Pb was found in C. carpio, collected at Etawah (S2) and minimum concentration of Pb was present in Allahabad (S6). Concentration of Ni was also highest in C. carpio, collected from Etawah (S2) and minimum in Allahabad (S5). Observed label of Cr was maximum in C. carpio, collected from Kalpi (S3) while it was absent in specimens collected from Allahabad. Bioaccumulation factor with respect to water was when calculated in O. niloticus and C. carpio, we found that accumulated amount of Cu was maximum

Environ Monit Assess Fig. 4 Concentration of metals in O. niloticus captured from the Yamuna River

in O. niloticus collected from Hamirpur (S4) and C. carpio collected from Kalpi (S 3 ) (Fig. 6). However, minimum concentration of Cu for O. niloticus and C. carpio was observed at Allahabad (S5). Accumulated amount of Pb was maximum for both O. niloticus and C. carpio in Allahabad (S 5 ). Minimum amount of Pb was observed in Hamirpur (S4) for O. niloticus as well as C. carpio. Accumulation factor for Ni was maximum in O. niloticus collected from S2 and minimum in S5. It was maximum in C. carpio, collected from S2 and it was absent downstream at Allahabad (S5). Largest amount of Cr was present in O. niloticus captured from Hamirpur (S4) and it was absent in O. niloticus captured from Allahabad (S5 and S6). Bioaccumulation factor for surface sediment showed that maximum amount of accumulated Cu through surface sediment was present in O. niloticus collected from extreme downstream at S 5 site and it was absent at S 6 (Fig. 7). Cu was found maximum in C. carpio

Fig. 5 Concentration of metals in C. carpio captured from the Yamuna River

collected from Etawah (S2) and minimum from Agra (S1) but it was totally absent in Allahabad (S6). Accumulated amount of Pb was maximum for O. niloticus collected from Etawah (S2) and minimum from Allahabad (S6). Pb was maximum in C. carpio, collected from S2 and minimum amount of Pb for C. carpio was present in S6. Equal amount of Ni accumulated in O. niloticus collected from S1 and S6, minimum amount of Ni was present in O. niloticus collected from S5. Maximum amount of Ni accumulated in C. carpio collected from (S6) and minimum from S5. Bioaccumulation of Cr in O. niloticus was maximum in Hamirpur (S4) and absent in Allahabad (S5 and S6). Accumulated amount of Cr was also maximum for C. carpio, collected from S4 and absent in S5 and S6. Ingestion of heavy metals was calculated by different exposure routes from each site S1 to S6 (Table 2). Ingested concentration of Cu was calculated from S1 to S6. Total ingested value for Cu

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Fig. 6 Bioaccumulation factor of metals in O. niloticus and C. carpio captured from the Yamuna River through water

was maximum in Agra (S1) and it was equal in downstream from S4 to S6. Total ingested amount of Pb was maximum in Allahabad (S5) and minimum in Kalpi (S3). Ingested amount of Ni was maximum in Agra (S1) and it was equal in S4 and S5. Total ingested amount of Cr was largest at S1 and minimum at S6. The calculated hazard

index (HI) showed that it was maximum at S1 and it was more than one showing carcinogenic risks (Table 2). HI for Pb present at S1, S2, S4, S5, and S6 sites was more than one and it also indicated carcinogenic risk. In S1, S2, and S6 sites, calculated HI for Ni was also more than one while it was below one at S3, S4, and S5. HI calculated for

Fig. 7 Bioaccumulation factor of metals in O. niloticus and C. carpio captured from the Yamuna River through surface sediment

Environ Monit Assess Table 2 Exposure level to heavy metals and hazard index with carcinogenic risk in the Yamuna River Sampling sites

S1

S2

S3

S4

S5

S6

Cu (μg kg−1day−1) Ingestion of sediment Ingestion of surface water

0.09×10−3 −3

6.73×10

−3

1.8×10

−3

1.88×10

−3

1.35×10

−3

0.85×10−3

−4

1.39×10

1.74×10

1.86×10

1.43×10

1.29×10−4

Dermal contact with sediment

1.6×10−3

0.7×10−4

3.0×10−4

2.8×10−4

0.3×10−4

0.1×10−4

−3

−3

−3

−3

−3

0.3×10−3

0.8×10

−6

0.9×10

−4

0.002×10−3

ND

1.62×10

−5

−4

0.016×10−3

1.68×10 3.1×10

−4

0.016×10−3

Ingestion of suspended matter Dermal contact with surface water

−4

0.004×10−3

0.6×10

−6

−5

0.7×10

−4

Ingestion of fish

1.3×10

1.5×10

7.2×10

1.9×10

0.3×10

ND

Total

0.0417

0.0119

0.0128

0.0098

0.0098

0.0062

Hazard indices

1.0417

0.2977

Carcinogenic risk

16.8×10−4

4.76×10

5.12×10

3.92×10

3.92×10

2.48×10−4

0.03×10−3

0.006×10−3

0.014×10−3

0.005×10−3

0.047×10−3

0.018×10−3

−1

0.3202 −4

0.2452 −4

0.2462 −4

0.1539 −4

−1

Pb (μg kg day ) Ingestion of sediment Ingestion of surface water

−3

3.57×10

−4

−3

2.51×10

−4

−3

2.31×10

−4

Ingestion of suspended matter

1.68×10

1.62×10

1.74×10

Dermal contact with sediment

1.2×10−4

1.1×10−4

2.5×10−4

Dermal contact with surface water Ingestion of fish

−2

5.43×10

−5

5.73×10

3.80×10−2 −5

2.47×10

2

3.51×10−

−5

1.76×10

−3

−3

4.1×10−3

1.88×10

−4

1.43×10

1.29×10−4

0.09×10−4

0.32×10−4

0.08×10−4

−2

−2

1.23×10−2

−4

2.96×10

1.96×10−6 0.1332

2.79×10

−4

4.16×10

−6

5.30×10

4.80×10

1.27×10

Total

0.0599

0.0424

0.0395

0.0464

0.1378

Hazard indices

1.4963

1.0592

0.9877

1.1602

1.4462

Carcinogenic risk −1

−4

−4

−4

−4

1.3320 −4

5.99×10

4.24×10

3.95×10

4.64×10

13.75×10

13.74×10−4

0.06×10−4

0.24×10−3

0.09×10−3

0.015×10−3

0.025×10−3

0.021×10−3

−3

−3

−3

−1

Ni (μg kg day ) Ingestion of sediment Ingestion of surface water

1.86×10

5.19×10

3.13×10

4.05×10−3

−4

1.74×10

1.88×10

1.43×10

1.29×10−4

Dermal contact with sediment

1.2×10−3

4.3×10−4

1.6×10−4

0.27×10−4

0.03×10−4

0.01×10−4

−2

1.74×10−2

Ingestion of fish

8.02×10

−5

4.37×10

2.23×10

−5

5.85×10

−2

1.34×10

−5

3.20×10

−4

2.46×10

1.62×10

−2

−4

2.33×10

1.64×10

−2

−4

−3

Ingestion of suspended matter Dermal contact with surface water

−4

−3

−2

1.0×10

−5

1.17×10

1.06×10

−5

0.5×10

1.17×10−5 0.0227

Total

0.0851

0.0298

0.0186

0.0146

0.0146

Hazard indices

1.5293

1.4936

0.9316

0.7285

0.7290

Carcinogenic risk −1

−4

−4

−4

−4

1.1376 −4

0.45×10−4

17.02×10

5.96×10

3.72×10

2.92×10

2.92×10

0.06×10−3

0.01×10−3

0.22×10−3

0.01×10−3

0.028×10−3

ND

−3

−3

−3

−3

−1

Cr (μg kg day ) Ingestion of sediment Ingestion of surface water

3.27×10

1.92×10

1.92×10

0.68×10

ND

ND

Ingestion of suspended matter

1.68×10−4

1.62×10−4

1.74×10−4

1.88×10−4

1.43×10−4

1.29×10−4

Dermal contact with sediment

1.1×10−3

1.4×10−4

3.8×10−4

0.28×10−4

0.01×10−4

0.001×10−4

−3

−5

Dermal contact with surface water

−2

1.24×10

−4

−3

2.53×10

−6

−3

4.08×10

−5

2.61×10

−5

8.16×10

−7

8.16×10−5

Ingestion of fish

2.2×10

7.26×10

1.29×10

1.1×10

3.92×10

ND

Total

0.0188

0.0062

0.0118

0.0080

0.00155

0.0014

Hazard indices

0.1251

0.0103

0.0091

7.75E−05

7.0E−05

Carcinogenic risk

0.0415 −4

9.4×10

0.0789 −4

3.1×10

Cr showed a value of below one in all sites indicating that there was no health risk concern for Cr and it was ingestible for humans.

0.0539 −4

5.9×10

−4

4.0×10

The calculated carcinogenic risk value for Cu was maximum in midstream at Agra (S1) and lowest value in extreme downstream at Allahabad S6 (Table 2). Largest

Environ Monit Assess

carcinogenic risk value for Pb was found at the S1 site. The carcinogenic risk value for Ni was at the maximum value which was higher than the values of all other metals and this maximum value for Ni was detected from Agra (S1). Maximum carcinogenic risk value for Cr was present in S 1 site and minimum in S 6 . Comparing the carcinogenic risk vales with guideline values, indicated that S1 site had highest carcinogenic risk compared with other sites but consumption may have the probability of contracting cancer due to mild carcinogenic effect of Ni, Cu, Pb, and Cr over a long life time of 70 years or more in future.

Discussion In this study, we have examined possible bioaccumulation of heavy metals in selected hardy exotic fishes O. niloticus and C. carpio which are now commonly available in the Yamuna River (Singh and Lakra 2011). The consumption of these commercially captured fishes increased since riverine production of O. niloticus and C. carpio has increased over the last few years (Singh et al. 2013). It is to mention that there are so many drains bringing sewage and effluents of several factories and industries such as dyeing, electroplating, fabric printing, bangle cutter, battery, and paints into the Yamuna River water (CPCB 2007; Bhargawa 2006; Namdeve and Singh 2012). The results of this study on the monitoring of the heavy metals and their bioconcentration revealed that concentration (microgram per liter) of heavy metals in the water of the Yamuna River was highest for Pb followed by Cu, Ni, and Cr. The assessment of the health risks and hazards of environmental pollutants in relation to bioaccumulation factor and exposure concentration suggested possible carcinogenic and noncarcinogenic risks particularly for Pb through consumption of contaminant fish (USEPA 2004; Michael et al. 2011; Imar and Carlos 2011). Risk assessment was performed in four steps: hazard identification, exposure assessment, dose response assessment, and risk characterization (Ma et al. 2007; Emmanuel et al. 2009). The risk value was regarded as the evaluation index and quantitatively described the risk of pollution and contaminants to human health. Risk assessment for metal contaminants was calculated as the processes and the probability of occurrence of an event and the probable magnitude of adverse health effects over a specified time period (Kolluru et al. 1996). Much of the earlier

risk assessment literature focuses on assessing potential impacts of chemical stressors on animals and humans (Allen et al. 2006). However, risk assessment in this study was obtained through the process of quantitative or qualitative measures of risk levels (USEPA 1998). Many reports are available relating the heavy metals in the aquatic environment, their bioconcentration factor and exposure concentration concerning health hazards (Sin et al. 2001; Canli and Atli 2003; Gale et al. 2004). Recently, Batayneh (2010) has reported heavy metals in water springs of the Yarmouk Basin, North Jordan and their potentiality in health risk while DeForest et al. (2007) have reported metal bioaccumulation in aquatic environments where inverse relationship between bioaccumulation factors, trophic transfer factors, and exposure concentration has been suggested. Further, McGeer et al. (2003) suggested inverse relationship between bioconcentration factor and exposure concentration of metals, while implicating hazard assessment of metals in the aquatic environment. Results of this study revealed that bioaccumulation of metals through water in O. niloticus and C. carpio was highest for Cr and Ni in midstream at Agra region. In Etawah, the maximum concentration of Ni was present in water and surface sediment, and, consequently, maximum concentration of Ni was present in O. niloticus and C. carpio captured from the river. Maximum accumulated amount of Pb was present in both O. niloticus and C. carpio through surface sediment downstream at Allahabad. Exposure to all other metals through the ingestion of fish was at the border line of acceptable limit whereas HI for Pb and Ni was more than one showing that carcinogenic effect of these metals was high. Further, high level of Pb and Ni at Firozabad and Mathura areas might have been due to surface run-off coming from bangle and pot making industries. The results indicated that Kalpi region had highest concentration of Ni and Cr, respectively, while in fish captured from the same site had high concentration of Ni and Cu. When HI for other metals was although below one, the detected concentration of all the metals had latent ability of creating carcinogenic risk of skin problem in human (Singh et al. 2012). In Hamirpur region, the observed value of metals in the Yamuna River water and surface sediment showed maximum level of Pb and Ni, respectively. The fish muscle of O. niloticus and C. carpio captured from the Hamirpur region also had maximum concentration of Cu and Ni as compared to other metals. Among the four metals, maximum amount of Pb was

Environ Monit Assess

exposure through dermal contact with surface water whereas maximum concentration of Cu was through ingestion of fish. Value of HI for Pb was more than one and for Cu, Ni, and Cr was less than one. The most probable cause of an increased amount of Pb was from effluents discharged from industrial areas and also from domestic sewage. Water sample collected from Allahabad region revealed that the concentration of Pb was highest in Yamuna as well as confluence region of Ganga and Yamuna. Cr was not detected in the Yamuna at Allahabad and at the confluence with the Ganga possibly because there is no tannery near it. However, highest concentration of Pb was observed in O. niloticus and C. carpio captured from Yamuna at Allahabad stream possibly due to sewage and other domestic effluents. HI for Pb was above one in the Yamuna River at Allahabad and carcinogenic risk value for Pb was more than all other metals. It is obvious that the Yamuna River water contaminants led to the accumulation of heavy metals in soil and consequently into the fish (McGeer et al. 2003). Bioaccumulation of metals can be caused by bioconcentration, mainly via respiratory membranes, or by biomagnification via dietary uptake since both O. niloticus and C. carpio are although omnivorous but chiefly feed on phytoplankton (Singh and Lakra 2011). Fish are located at the end of aquatic food chain and may accumulate metals even in water in which they are below the limit of detection in routine water sample (Mason 1987; Yehia & Sebaee 2012). As partitioning between water or food and outer membranes of organisms represents the most important process of bioaccumulation in aquatic systems, these substances tend to concentrate mainly in the lipid fraction of organisms and may lead to substantial physiological burdens (Kumar and Mukherjee 2011; Imar and Carlose 2011). The accumulation of such residues in the food chain can reach toxic levels to predators and represents a risk for human health (Kumar and Mukherjee 2011; Imar and Carlose 2011). Assessing the bioconcentration as well as the biomagnification potential is, therefore, an important issue for the environmental and human risk assessment, and, thus, it forms one of the main features in environmental monitoring (DeForest et al. 2007). Heavy metal concentrations varied between O. niloticus and C. carpio, which reflected the differences in their uptake capabilities (DeForest et al. 2007). In all sampling sites, Cu, Pb, Ni, and Cr concentrations were above the permissible limits as decided by the national and international standards. Hazard indices of heavy metals also

suggest that Cd, Pb, Ni, and Cr contamination in the invasive fish species had potential to pose risk for human health due to consumption of fish having long-term exposure to the contaminated water of the river. Percent contribution to daily intake rate of Cu, Ni, Pb, and Cr was higher by both fish muscles, whereas intake of Pb and Ni was principally higher by the ingestion of C. carpio. Consumption of these fish with elevated levels of heavy metals may lead to high level carcinogenic risk to human health. It is thus advocated that regular monitoring of heavy metal contamination in the fish species thriving at contaminated water must be carried out to ascertain the food safety issue (Canli and Atli 2003; Imar and Carlose 2011). Our findings address an important aspect of biomonitoring using proper tools and have greater implications for developing fish consumption advisories and public awareness about the consequences of eating contaminated fish. This initiative will be an important step to undertake measures to remove heavy metals from the river water as per need in view of the environmental and food safety. Acknowledgement The authors are grateful to Dr. J.K. Jena, Director NBFGR for his encouragements and consistent support. We thankfully acknowledge the financial support of the Uttar Pradesh Biodiversity Board, Lucknow.

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