Science of the Total Environment 541 (2016) 1232–1242

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Science of the Total Environment

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Concentrations and patterns of organochlorines (OCs) in various fish

species from the Indus River, Pakistan: A human health risk assessment
Timmer Robinson a, Usman Ali a, Adeel Mahmood b, Muhammad Jamshed Iqbal Chaudhry c, Jun Li d,
Gan Zhang d, Kevin C. Jones e, Riffat Naseem Malik a,⁎
a
Environmental Biology and Ecotoxicology Laboratory, Department of Environmental Sciences, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad 45320, Pakistan
b
Department of Biosciences, COMSATS Institute of Information Technology, Islamabad 45550, Pakistan
c
WWF-Pakistan, Ferozpur Road, PO Box 5180, Lahore 54600, Pakistan
d
State Key Laboratory of Organic Geochemistry, Guangzhou Institute of Geochemistry, Chinese Academy of Sciences, Guangzhou 510640, China
e
Centre for Chemicals Management, Lancaster Environment Centre, Lancaster University, Bailrigg, Lancaster LA1 4YQ, UK

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• OCPs composition profile in fish muscle

tissues showed highest contribution of
DDTs, while PCBs patterns showed
maximum contribution of tri−CBs.
• Diagnostic ratios of HCH and DDT indi-
cated both recent and past use of these
chemicals in the area.
• Risk assessment suggests that the daily
exposure to OCPs and PCBs yields a life-
time cancer risk of 1 in a million

a r t i c l e i n f o a b s t r a c t

Article history: The present study was conducted to reveal the concentrations and patterns of organochlorines [i.e., organochlo-
Received 1 August 2015 rine pesticides (OCPs) and polychlorinated biphenyls (PCBs)] in freshwater fish species collected from four eco-
Received in revised form 1 October 2015 logically important sites of the Indus River i.e., Taunsa (TAU), Rahim Yar Khan (RYK), Guddu (GUD) and Sukkur
Accepted 1 October 2015
(SUK). In the fish muscle tissues, concentrations of 15 OCPs (∑15OCPs) and 29 PCBs (∑29PCBs) varied between
Available online xxxx
1.93–61.9 and 0.81–44.2 ng/g wet weight (ww), respectively. Overall, the rank order of OCs was DDTs N PCBs N
Editor: D. Barcelo hexachlorocyclohexanes (HCHs) N chlordanes (CHLs). The patterns of PCBs showed maximum contribution of
tri-CBs (59%). Ratios of individual HCH and DDT analytes contributing to the summed values indicated both re-
Keywords: cent and past use of these chemicals in the region, depending upon fish species. To assess the associated health
Organochlorines risks, carcinogenic and non-carcinogenic risks were calculated through hazard ratios (HRs). For carcinogenic risk,
Organochlorine pesticides HR was N1 at both 50th and 95th percentile concentrations, suggesting that the daily exposure to OCPs and PCBs
Polychlorinated biphenyls
Fish

⁎ Corresponding author.
E-mail address: [email protected] (R.N. Malik).

http://dx.doi.org/10.1016/j.scitotenv.2015.10.002
0048-9697/© 2015 Elsevier B.V. All rights reserved.
 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242 1233

Indus River yields a lifetime cancer risk of 1 in a million. HR for non-cancerous risk was b1 at both the percentiles, signifying
Pakistan no adverse effect by OCs exposure in native population.
Risk assessment © 2015 Elsevier B.V. All rights reserved.

1. Introduction 2. Materials and methods

During the last century, reckless production and use of persistent or- 2.1. Study area and sampling
ganic pollutants (POPs) i.e., organochlorine pesticides (OCPs) and
polychlorinated biphenyls (PCBs) at agricultural and industrial level Four ecologically important sites were selected including Taunsa
has altered the global biodiversity (Köhler and Triebskorn, 2013; Teng Barrage (TAU), Rahim Yar Khan (RYK), Guddu Barrage (GUD) and
et al., 2012). This is due to their bioaccumulative character, persistent Sukkur Barrage (SUK) across the Indus River (Fig. 1). A total of 35 fish
nature and toxic effects on wildlife and humans (Haynes and Johnson, samples were collected from the selected sites of the Indus River be-
2000). Although the application of these chemicals has been banned tween February and April, 2014. All the selected fish species were dis-
under the Stockholm Convention (2001), many developing countries tributed throughout the study sites and extensively consumed by local
continue to use these chemicals owing to their low cost and versatility residents. Fish samples were immediately stored in ice and transported
in industrial, agricultural and health sectors (Guruge and Tanabe, to the Environmental Biology and Ecotoxicology Laboratory for mea-
2001). Though, Pakistan also signed the Stockholm Convention in surements of biological parameters (length and weight) and frozen
2001 but still there exists no systematic monitoring and control of until further analysis. Using the morphological characteristics, they
POPs in different environmental media across the country (Malik were identified by a fish taxonomist following Fishbase (2014). Twelve
et al., 2011). Recent studies (Ali et al., 2015a; Ali et al., 2015b; Sultana fish species were identified as carnivorous species (Chitala chitala,
et al., 2014) conducted in the Indus River Basin of Pakistan showed rel- Channa striata, Rita rita, Clupisoma gaura, Sperata seenghala, Wallago
atively higher or comparable levels of OCs in different environmental attu) and herbivorous species (Cirrhinus mrigala, Catla catla, Cyprinus
samples in comparison with global levels owing to the increasing indus- carpio, Labeo rohita, Labeo dyocheilus and Cirrhinus reba). The details re-
trial and agricultural activities being presently developed in the region. garding sampling sites, description and collected fish species are pre-
Indus River is one of the major rivers of Asia, acting as a source of water sented in Supporting information, SI Table 1 and SI Fig. 1.
and haven for endangered species and riverine ecosystem. It plays a crit-
ical role in the agricultural sector of the country and has a unique eco- 2.2. Extraction, lipid (%) determination and purification
logical importance in the region. At present, agricultural run-off,
industrial waste and municipal discharge have led to immense pollution The scales of the fish were removed after defrosting, thawing and
loads in the Indus River (Mughal, 2008). Surrounding ecosystem of the washing each sample with clean water. Dissection was done between
Indus River is contaminating due to extensive use of agrochemicals and the vent and pectoral fin of the fish in order to obtain the muscle tissues
pesticides for profitable farming. The escalating anthropogenic activities (without skin). Fish muscle samples were minced into small pieces.
along the Indus River may seriously pollute the region with OCs and About 10 g of muscle tissue was weighed and homogenized with anhy-
may cause high accumulations of OCs in the riverine biota. drous sodium sulfate (Na2SO4·H2O) and packed in filter paper using the
In aquatic systems, OCs are distributed in the environmental and bi- method of Eqani et al. (2013). Each individual of collected species was
ological compartments where they are influenced by their octanol– prepared separately, with varying size. Prior to extraction, decachlorobi-
water partition coefficients, organic matter in the sediments, and the phenyl (PCB209) and 2,4,5,6-tetrachloro-m-xylene (TCmX) were added
lipid contents in biota (Thomas et al., 2012). Compared to terrestrial as surrogate standards and Soxhlet extracted for 48 h with 150 ml of di-
mammals, fish have been shown to have an increased ability to chloromethane (DCM) and acetone (2:1 v/v). The extracts were concen-
bioaccumulate organic pollutants due to their lower mono-oxygenase trated to 10 ml and solvent exchanged to n-hexane. A 1 ml aliquot of
activity (detoxification enzymes) and hence, are a valuable bioindicator sample extract was used for gravimetric lipid determination. Then puri-
of pollution in aquatic habitats (Davodi et al., 2011). The accumulation fication was done with concentrated sulfuric acid to remove lipids and
of hydrophobic compounds in fish tissues has also been shown to ex- then cleaned up on 8 mm i.d. alumina/silica column packed, from the
hibit variation among different fish species, as well as within a species bottom to top, with neutral alumina (6 cm, 3% deactivated), neutral sil-
(Sharma et al., 2009). Global Monitoring Plan has categorized fish as a ica gel (10 cm, 3% deactivated), 50% (on a weight basis) sulfuric acid sil-
supplementary media to promote the evaluation of the Stockholm Con- ica (10 cm), and anhydrous sodium sulfate. The OCP and PCB fractions
vention regarding organic contaminants (Adu-Kumi et al., 2010). were solvent-exchanged to n-hexane and concentrated to 0.5 ml
Records on distribution and occurrence of OCs in commercially and under a gentle steam of pure nitrogen. 20 μl of PCB54 was used as an in-
recreationally important fish species are considered a vital aspect in ternal standard.
human health apart from ecological perspective (Erdogrul et al., 2005;
Thomas et al., 2012). In human diet, fish and its products contributes 2.3. GC-MS analysis of OCs and QC/QA
only 10% but still it is one of the most important source, responsible
for 90% exposure to the POPs (Djien Liem et al., 2000). Around the Analysis of OCPs and PCBs was done using Gas Chromatography
globe, various surveys have been conducted to evaluate the health Mass Spectrometry (GC–MS) with 50 m capillary column (Varian, CP-
risks associated with consumption of POP-contaminated fish (Binelli Sil 8 CB, 50 m, 0.25 mm, 0.25 μm). Helium was used as a carrier gas at
and Provini, 2004; Jiang et al., 2005; Yang et al., 2006) including studies 1.1 ml/min under constant flow mode. Injector temperature was 250
conducted in Pakistan (i.e., Eqani et al., 2013; Munshi et al., 2004; Saqib °C. The initial oven temperature was set at 150 °C for 3 min and raised
et al., 2005). But these studies are insufficient for providing the more re- to 290 °C at a rate of 4 °C/m. PCBs were determined in selected ion
alistic scenario of OCs contamination in the fish matrix of the country mode. Concentrations of organochlorines were expressed in ng/g ww.
along with associated health risks. Therefore, this study was conducted The following OCPs and PCBs were analyzed: DDTs (o,p′, p,p′-DDD,
with the objectives of to investigate the occurrence, pattern, compari- -DDE, -DDT), HCHs (α-HCH, β-HCH, γ-HCH, δ-HCH), trans-chlordane
son of OCs trend in two trophic levels (herbivore and carnivore) and (TC), cis-chlordane (CC), heptachlor, β-endosulfan, hexachlorobenzene
human health risk assessment of OCs in different types of edible fresh- (HCB) and PCBs (8, 28, 30, 37, 44, 49, 52, 60, 66, 70, 74, 77, 82, 87, 99,
water fish species, collected across the Indus River. 101, 105, 114, 118, 126, 138, 153, 156, 158, 169, 170, 179, 180, 189).
1234 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242

Fig. 1. Study area map and sites for fish sampling.

Strict quality control procedures were implemented to inspect all concentration. The ratios were estimated based on 50th and 95th per-
the samples. Standardization of instruments was done with calibration centiles exposure (fish tissue) concentrations (Jiang et al., 2005).
standards on daily basis. Field, procedural and solvent blanks were ana-
lyzed with the same method as used for actual samples. After every 10 Average daily exposure
Hazard ratio ðHRÞ ¼
samples, a procedural blank and a spiked blank was run to prevent con- Benchmark concentration
tamination. There was no significant contamination found in blank sam-
ples. Average surrogate recoveries were 72 ± 13% and 74 ± 15% for Risk  Body weight
TCmX and PCB209 respectively. The final values were corrected using Benchmark concentration ¼
Fish consumption  Slope factor
the recovery percentages. All the glass ware used were baked at 450
°C prior to use during the whole analytical procedure.
where ‘risk’ is the probability of lifetime cancer risk and the benchmark
concentration is derived by setting the cancer risk to one in one million
2.4. Toxic equivalent dioxin like PCBs
due to lifetime exposure. The benchmark concentration for carcinogenic
effect was derived using cancer slope factor (CSF) and for non-carcino-
For calculation of toxic equivalent dioxin like PCBs, WHO-TEQ (Toxic
genic effect Oral Reference Dose (RfD) was used, obtained from the US
Equivalents) values for dioxin like-PCBs (dl-PCBs) were calculated for
Environmental Protection Agency (USEPA) Integrated Risk Information
each species by multiplying the mean value of each species with the
System (IRIS) for each contaminant (SI Table 3).
toxic equivalency factor (TEF). WHO-TEF values for each mono-ortho
dl-PCBs and non-ortho dl-PCBs (Van den Berg et al., 2006) were utilized
for this purpose (SI Table 2). Total TEQs were calculated but summing Average daily exposure ¼ Fish consumption
 Contaminant concentration
up each congener-TEQ values calculated for each fish species.

2.5. Health risk assessment Fish consumption was expressed as daily consumption divided by
body weight (set to an average of 55 kg for an adult). Daily consumption
To assess cancer and non-cancerous risks associated with fish con- is used as 15 g/kg body weight/day. This estimation was done with
sumption in humans, hazard ratios (HR) were computed. Calculation questionnaire based survey conducted from the 120 local residents of
of HRs was done by dividing average daily exposure by benchmark the study area.
 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242 1235

2.6. Statistical analysis contribute b5% (Hitch and Day, 1992). Overall patterns of DDTs showed
highest contribution of p,p′-DDE (30.5%) and p,p′-DDT (30.1%) followed
Basic descriptive statistics were performed on IBM Statistics 20 and by o,p′-DDT (15.8%), p,p′-DDD (12.7%), o,p′-DDE (5.58%) and o,p′-DDD
for graphical representation of percentage compositions, Microsoft (5.25%). p,p′-DDE (51.7%) was the major contributor in M. armatus
Excel 2010 was used. Principal Component Analyses (PCA) was carried while it showed minor contribution in C. carpio (13.8%). Zhou et al.
out on Multivariate Analysis Statistical Package (MVSP Version 3.22) to (2007) reported p,p′-DDE as a major contributor in fish species of
explore the relationship between contaminants and species. To identify Qiantang River. Metabolic functions through oxygenase (enzyme) in
the classification of species that indicates their similarity based on or- different organisms especially fish has a central role in converting p,p
ganochlorines, Agglomerative Hierarchical Clustering (using un- ′-DDT into p,p′-DDE (Muralidharan et al., 2009) which might be the rea-
weighted pair-group average) was performed using XlStat. Study area son for more contribution of p,p′-DDE. The ratios of (DDE + DDD) /
representing the sampling points was created on Arcview GIS Version ∑ DDTs was high (SI Table 5) in most of the species and few had a
9.3. ratio b 0.5 that indicated aged DDT pollution and recent input of techni-
cal DDT (Ameur et al., 2013).
3. Results and discussion ∑HCHs showed comparatively lower concentrations than ∑DDTs
with a range of 0.17–22.7 ng/g ww. R. rita had the maximum mean
The measured biological parameters of all the fish samples are pre- value of ∑ HCHs (5.70 ± 4.54 ng/g ww) among all fish species. The
sented in SI Table 4. Body length of collected fish samples ranged be- compositional profile of HCHs in fish muscle showed dominance of α-
tween 22 and 47 cm with minimum length recorded for Channa HCH (46.6%) followed by γ-HCH (27.4%), β-HCH (24.7%) and δ-HCH
striatus while maximum for S. seenghala. Maximum body weight was re- (1.18%). Hence indicating the usage of technical grade HCH in the area
corded for C. mrigala (882 g) and minimum for Eutropiichthys vacha that typically consist of 55–80% α-HCH, 5–14% β-HCH, 8–15%, γ-HCH
(80 g). In case of lipid content, R. rita exhibited highest lipid content and 2–16% δ-HCH in agricultural division and sanitation
with a mean of 5.08% followed by Mastacembelus armatus 3.98%. Both (Muralidharan et al., 2009). α-HCH has higher vapor pressure and
species are carnivorous as they feed on zooplankton and fish with pref- Henry's Law Constant as compared to β-HCH and γ-HCH, hence it has
erence of benthic zone as a habitat (Fig. 2 for details). greater efficiency for atmospheric transport (Chen et al., 2002) and de-
position in riverine systems. Predominance of α-HCH were in accor-
3.1. Occurrence and patterns of OCs in fish species dance with the results reported in fish samples from Iran, Sri Lanka
and India (Davodi et al., 2011; Guruge and Tanabe, 2001; Pandit et al.,
Average concentrations of OCPs and PCBs (ng/g, wet weight) in the 2001). Most of the fish samples showed high ratios of α/γ (0.55–5.95;
fish samples are reported in Table 1. All the results and comparison SI Table 5) which indicated the application of technical HCH in the re-
are based upon wet weight basis. ∑OCPs ranged from 1.93 in C. reba gion (Yang et al., 2010).
to 61.9 ng/g ww in C. chitala while ∑PCBs varied between 0.62 ng/g Concentrations of ∑ CHLs ranged between 0.12–5.35 ng/g ww
ww in C. catla to 27.1 ng/g ww in C. striatus. while maximum mean value was recorded in C. chitala (2.68 ±
0.23 ng/g ww). The compositional profile of CHLs showed dominance
3.1.1. OCPs of TC (73.2%) as compared to CC (26.7%). Detection of TC in fish samples
∑OCPs were ranged between 1.93–61.9 ng/g ww in all the fish spe- indicated its usage in industrial and agricultural sector while it may
cies. The major metabolites of technical grade DDT are p,p′-DDT (75%), have transported to the river via atmospheric deposition, surface run-
o,p′-DDT (15%) and p,p′-DDE (5%), with the other metabolites off and erosion from the adjoining soils (Bidleman et al., 2002). Other

Fig. 2. Lipid content (%) profile of fish samples from the Indus River.
1236 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242

Table 1
Descriptive summary of OCPs and PCBs in freshwater fish species of the Indus River.

Site Species ∑HCHs ∑DDTs ∑CHLs ∑Other OCPs ∑OCPs ∑PCBs

TAU Chitala chitala 4.27 ± 3.43 6.93 ± 4.05 0.75 ± 0.52 0.06 ± 0.43 4.13 ± 4.15 0.88 ± 1.91
Cirrhinus mrigala 0.52 ± 0.52 0.41 ± 0.30 0.09 ± 0.08 0.09 ± 0.05 0.33 ± 0.36 0.33 ± 0.97
Catla catla 2.90 ± 2.47 1.90 ± 1.39 0.51 ± 0.50 0.33 ± 0.16 1.66 ± 1.79 0.03 ± 0.04
Rita rita 5.70 ± 4.54 3.91 ± 2.51 0.59 ± 0.48 0.58 ± 0.36 3.28 ± 3.41 0.70 ± 1.46
Ctenopharyngodon idella 0.50 ± 0.43 2.27 ± 1.58 0.44 ± 0.33 0.06 ± 0.01 1.11 ± 1.45 0.32 ± 0.62
RYK Cirrhinus mrigala 1.03 ± 0.67 0.51 ± 0.38 0.46 ± 0.36 0.07 ± 0.05 0.56 ± 0.53 0.28 ± 0.92
Chitala chitala 2.70 ± 2.35 4.21 ± 2.35 2.68 ± 0.23 0.23 ± 0.20 2.81 ± 2.12 0.88 ± 3.48
Chitala chitala 1.29 ± 1.26 2.20 ± 1.49 1.17 ± 0.17 0.14 ± 0.07 1.41 ± 1.38 0.61 ± 1.92
Rita rita 1.60 ± 1.49 3.46 ± 2.80 0.65 ± 0.60 0.14 ± 0.07 1.93 ± 2.41 0.80 ± 2.78
Rita rita 2.66 ± 2.21 1.40 ± 1.09 0.19 ± 0.14 0.08 ± 0.03 1.31 ± 1.61 0.21 ± 0.59
Clupisoma gaura 1.41 ± 1.22 0.41 ± 0.36 0.25 ± 0.41 0.05 ± 0.02 0.58 ± 0.82 0.83 ± 3.22
Clupisoma gaura 2.20 ± 1.93 0.60 ± 0.48 0.31 ± 0.23 0.06 ± 0.00 0.88 ± 1.27 0.76 ± 2.91
Sperata seenghala 0.75 ± 0.68 0.16 ± 0.12 0.20 ± 0.13 0.09 ± 0.07 0.31 ± 0.43 0.97 ± 2.51
Wallago attu 0.78 ± 0.66 0.07 ± 0.72 0.16 ± 0.09 0.05 ± 0.04 0.52 ± 0.64 0.71 ± 0.56
GUD Catla catla 0.90 ± 0.62 2.42 ± 1.09 0.39 ± 0.13 0.15 ± 0.15 1.29 ± 1.26 0.02 ± 0.03
Wallago attu 0.54 ± 0.39 0.89 ± 0.70 0.94 ± 0.07 0.10 ± 0.08 0.65 ± 0.59 0.62 ± 2.04
Cyprinus carpio 0.43 ± 0.28 1.67 ± 1.20 0.15 ± 0.08 0.11 ± 0.05 0.82 ± 1.08 0.48 ± 1.73
Labeo pangusia 0.78 ± 0.52 2.08 ± 0.72 0.19 ± 0.24 0.10 ± 0.03 1.09 ± 1.03 0.54 ± 1.76
Sperata seenghala 0.77 ± 0.68 5.69 ± 3.87 0.45 ± 0.37 0.29 ± 0.36 2.60 ± 3.66 0.66 ± 2.20
Eutropiichthys vacha 1.89 ± 1.40 3.88 ± 2.60 1.10 ± 0.09 0.49 ± 0.44 2.30 ± 2.32 0.94 ± 2.15
Mastacembelus armatus 1.71 ± 1.23 2.98 ± 2.92 0.24 ± 0.15 0.65 ± 0.91 1.81 ± 2.31 0.49 ± 1.76
Cirrhinus reba 0.04 ± 0.03 0.20 ± 0.16 0.06 ± 0.08 0.51 ± 0.25 0.13 ± 0.16 0.95 ± 1.84
Channa striatus 1.95 ± 1.36 0.59 ± 0.49 0.20 ± 0.14 0.04 ± 0.02 0.79 ± 1.03 0.93 ± 2.31
Channa striatus 2.06 ± 2.18 0.23 ± 0.32 0.18 ± 0.10 0.05 ± 0.05 0.68 ± 1.35 0.77 ± 2.72
SUK Ompok pabda 2.77 ± 2.57 2.19 ± 1.75 0.31 ± 0.17 0.17 ± 0.22 1.69 ± 1.99 0.51 ± 1.90
Wallago attu 3.01 ± 1.74 7.14 ± 2.63 1.20 ± 0.01 1.38 ± 1.06 4.10 ± 3.29 0.61 ± 2.12
Cyprinus carpio 0.43 ± 0.35 4.33 ± 2.83 0.26 ± 0.17 0.09 ± 0.06 1.90 ± 2.77 0.27 ± 1.00
Chitala chitala 0.50 ± 0.40 0.90 ± 0.66 0.52 ± 0.46 0.08 ± 0.04 0.58 ± 0.58 0.74 ± 2.40
Labeo rohita 0.98 ± 0.74 2.86 ± 2.70 0.58 ± 0.42 0.31 ± 0.31 1.55 ± 2.14 0.48 ± 1.37
Sperata seenghala 0.24 ± 0.26 0.28 ± 0.24 0.16 ± 0.07 0.04 ± 0.03 0.21 ± 0.22 0.55 ± 2.15
Labeo dyocheilus 0.67 ± 0.78 0.23 ± 0.17 0.22 ± 0.09 0.04 ± 0.04 0.31 ± 0.45 0.35 ± 1.70
Labeo calbasu 0.51 ± 0.52 0.21 ± 0.16 0.20 ± 0.09 0.05 ± 0.05 0.26 ± 0.31 0.43 ± 1.36
Channa striata 0.83 ± 0.62 3.94 ± 2.95 0.57 ± 0.41 0.26 ± 0.30 1.92 ± 2.60 0.91 ± 2.42
Barbus sarana 0.65 ± 0.79 1.04 ± 0.79 0.46 ± 0.42 0.05 ± 0.04 0.66 ± 0.75 0.22 ± 0.76
Notopterus notopterus 0.59–0.51 2.21 ± 1.84 0.63 ± 0.48 0.38 ± 0.50 1.20 ± 1.51 0.26 ± 0.46

OCPs showed low concentrations in all fish samples. HCB contributed 2012), hence direct disposal of waste from these industries may have
57% as compared to heptachlor (27%) and β-endosulfan (16%) to the transported tri-CBs into the river.
total composition of other OCPs. Low concentrations of HCB in fish mus- The concentration of ∑10dl-PCBs varied between 0.14 and 6.92 ng/g
cles may be attributed to its past application as a fungicide and its emis- ww (SI Fig. 2). Among all the fish species non-ortho dl-PCBs (PCB77,
sion during manufacturing and usage of various industrial and 126, 169) ranged from 0.05 in C. catla to 5.15 ng/g ww in C. chitala.
agrochemicals as a by-product (Adu-Kumi et al., 2010; Ameur et al., The maximum concentrations of mono-ortho congeners (PCB105, 114,
2013). Moreover HCB has a volatile nature (Kannan et al., 1995) that 118, 156, 189) were recorded in C. striata (3.53 ng/g ww), while
is also responsible for its transport in the environment. Ompok pabda showed minimum concentration (0.04 ng/g ww) for
these congeners. Di-ortho PCBs (PCB70, 80) varied between 0.01 and
0.28 ng/g ww. The probable source for the dl-PCBs could be the im-
3.1.2. PCBs proper incineration of electronic waste in the surrounding region.
∑PCBs ranged between 0.81–44.20 ng/g ww in fish muscles while WHO has established TEFs values to evaluate the toxicity associated
the trend for homologue groups was tri → hexa → tetra → di → with different contaminants including dl-PCBs, this is known as the
penta-CBs. Tri-CBs were highest in S. seenghala (9.66 ± 5.70 ng/g ww) WHO-TEF approach. By using the WHO-PCBs TEFs, a number of investi-
while lowest in C. catla (0.1 ± 0.07 ng/g ww). Hexa-CBs were highest gations (Adu-Kumi et al., 2010; McHugh et al., 2010; Szlinder-Richert
in Ctenopharyngodon idella (0.91 ± 0.47 ng/g ww) and lowest in et al., 2010) have reported dominance of non-ortho dl-PCBs that are
C. catla (0.01 ± 0.01 ng/g ww). In aquatic ecosystems, individual classes consistent with the present study. WHO-TEQ for ∑10dl-PCBs varied be-
of PCBs have varying distribution patterns among fish that generally de- tween 0.00 and 0.16 pg/g TEQ in all the fish species where PCB169
pends on contamination source, feeding preferences and type of fish showed the maximum contribution. The calculated TEFs were far
species (Yang et al., 2010; Zhou and Wong, 2004). Profiles of PCB conge- below the limit provided by European Commission Regulation, 2006
ners, according to the degree of chlorination in fish muscle are pre- in fish muscle (8 pg TEQ/g fresh weight).
sented in Fig. 3. Patterns of different PCB classes showed highest
contribution of tri-CBs (59%) in fish muscle followed by hexa-CBs 3.2. Spatial distribution of organochlorines
(23%), tetra-CB (11%), penta-CBs (4%) and di-CB (4%). Highest contribu-
tion of tri-CBs was observed in C. gaura (73%) while C. catla (33%) had Fish samples showed highest mean concentration for DDT (18.5 ng/
the lowest. Overall the low concentrations of PCBs and dominance of g ww) and HCH (11.1 ng/g ww) at Taunsa Barrage (Fig. 4) that was pos-
tri-CB congeners detected in fish propose a diffuse contamination via sibly attributed to the agricultural activities in the catchment area of the
water column where there is high solubility of low chlorinated conge- Indus River. Although the RYK region is known for massive cotton pro-
ners (Erdogrul et al., 2005). For aquatic biota, low CBs are more available duction, we found low concentrations of DDTs in fish collected from this
due to increased mobility of these compounds from substrate to water site. It could be due to the use of other classes of pesticides including
(Voorspoels et al., 2004). Low chlorinated PCBs such as tri-CB are typi- carbamates and organophosphates in the area (Hellar-Kihampa et al.,
cally used in additives of paints and electrical appliances (Eqani et al., 2013). Sultana et al. (2014) also reported reduced loads of OCPs in soil
 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242 1237

Fig. 3. Composition profile (%) of DDTs (a), HCHs (b), chlordane (c) and PCBs (d) in fish samples from the Indus River.

Fig. 4. Spatial distribution of OCPs (a) and PCBs (b) in fish samples from the Indus River.
1238 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242

and air samples of RYK. The overall spatial pattern of PCBs were Romania (Covaci et al., 2006). Range of CHLs were comparable with
followed as: RYK b GUD b SUK b TAU (Fig. 4). A confluence point is sport and market fish from Korean coast (Yim et al., 2005). Residual
formed at RYK and Kot Mithan where the Indus main stream and Panj- concentrations of PCBs are comparable with those reported in fish of
nad River joins. Industrialized cities of Punjab dispose the electric waste River Turia, Spain (Bordajandi et al., 2003). Davodi et al. (2011) reported
containing PCBs into the Panjnad River (Eqani et al., 2012) that are ulti- the dominance of tri-CBs in edible fish of Shadegan Marshes, Iran that
mately transported to confluence point. Hence RYK has higher loads of coincides our results as well.
PCBs as compared to other sites. The open burning of waste, dumping
and residential waste are common practices in all these areas. More- 3.4. Multivariate statistical analysis (PCA and cluster analysis)
over, the Indus River basin is very close to industrial and urban areas
that contain the paint industry, carbonless copy paper, cable insulation On the basis of correlation matrix, a Euclidean biplot was obtained
companies and workshops for burning electric cable for metal reclama- using the first two axis of PCA (Fig. 5). The first axis explained 60.5% of
tion that might be the sources of PCBs in Indus basin. The industrial ac- total variance and second axis accounted for 24.6% of variance. HCB
tivities including chemicals, printing, electronics, leathers, cement, and all metabolites of DDTs were strongly correlated with the first
textiles, pharmaceuticals and mining can be responsible for PCBs con- axis, suggested agricultural run-off as an important source of pollution
tamination (Ali et al., 2015b). On the other hand incineration of waste in the study area. In OCPs, HCB exists as an impurity and may be brought
containing PCBs, oil leakage from capacitors/transformers and inappro- to the riverine ecosystem via atmospheric transport (Jaward et al., 2004).
priate disposal also release PCBs in the environment (Syed et al., 2013). Isomers of HCHs and TC showed a weak correlation with both first and
All the four sites showed dominance of tri-CBs that might have origi- second axis but α- and γ-HCHs were clustered together suggested its
nated from electric waste disposal points and electric power generation wide use in both public health and agricultural activities (Rajendran
at TAU and GUD barrage (Eqani et al., 2012). Moreover, PCBs are used as et al., 2005). PCBs was inclined towards the second axis and separated
a technical mixture comprising of 70% tri-, tetra- and penta-CBs with from other organochlorines, presented industrial activities as a source of
dominance of tri-CBs in technical mixtures (Eqani et al., 2012). PCBs contamination. Vectors that were too short are not displayed in
the biplot as the concentration of those organic contaminants (β-HCH,
3.3. Global comparison CC, β-endosulfan and heptachlor) were comparatively low. Two distinct
groups are formed on the basis of trophic levels of fish species.
Table 2 shows the global comparison of fish concentrations of OCs Group-1 was comprised of the ‘Cyprinidae’ herbivorous species in-
with current study. Our DDT concentrations were comparable with cluding C. mrigala, C. catla, C. idella, C. reba, C. carpio, L. dyocheilus,
levels reported from 8 Western US National Parks (Ackerman et al., Labeo calbasu and Barbus sarana. In addition, four individuals of the car-
2008) and higher than Cambodia, South-East Asia (Monirith et al., nivorous species S. seenghala, W. attu, O. pabda and Notopterus
1999). Although DDT has been banned in Pakistan in 1994 (Ali et al., notopterus also clustered into this group. Group-2 consisted of the re-
2014) but easy accessibility and illegal use has promoted its practice maining fish from the following carnivorous species: C. chitala, R. rita,
in industrial, agriculture and health division across the country (Malik C. gaura, S. seenghala, W. attu, E. vacha, M. armatus and C. striatus.
et al., 2011). Around the world, Pakistan holds one of the largest stocks Among herbivores fish species, ∑ OCPs and ∑PCBs ranged between
of organochlorine pesticides while granaries consist of thousand kilo- 1.39–28.5 and 0.78–15.6 ng/g ww respectively. Maximum concentra-
grams of DDTs (Jan et al., 2009) that have ended up in contaminating tions of organochlorines were recorded in Group-2 where ∑ OCPs
biota including fish and environmental medias of the country. HCHs and ∑ PCBs ranged between 3.12–61.9 and 4.88–28.1 ng/g ww that
concentrations were lower as compared to that of Shadegan Marshes, was relatively higher than herbivore. Trophic position and lipid content
Iran (Davodi et al., 2011) and higher than Pearl River Estuary & Day of aquatic organisms are reliable predictors of OC concentrations in
Bay, China (Guo et al., 2008). Analysis of OCPs in fish from river Chenab aquatic ecosystem (Kidd et al., 2001). OCs can biomagnify and
(Eqani et al., 2013) showed maximum concentration of ∑ HCHs in bioaccumulate in carnivore fish as they are generally positioned at the
R. rita that was consistent with our results which displayed highest con- top of trophic level and contain relatively high lipid content as com-
centrations of ∑HCHs in R. rita. Moreover, dominance of DDTs over pared to herbivore and omnivore species (Deribe et al., 2011; Zhou
HCHs are in consistent with trend reported in fish from Danube Delta, et al., 2007). Other factors such as size, age and type of species can

Table 2
Worldwide comparison of OCs (range) in fish with current study.

Study area HCHs DDTs CHLs PCBs Unit Reference

Ebro Delta (Spain) 2.6–16.8 1.8–20.3 ng/g ww Pastor et al. (1996)

Cambodia (South East Asia) 0.01–0.22 0.3–25 0.01–0.35 b0.05–1.2 ng/g ww Monirith et al. (1999)
West Coast (Sri Lanka) 0.09–0.72 1.3–120 0.06–8.6 2.7–210 ng/g ww Guruge and Tanabe (2001)
River Turia (Spain) 4.28–45.3 6.86–43.6 ng/g ww Bordajandi et al. (2003)
Korea (Asia) 0.38–5.60 0.84–27.0 0.17–4.24 2.96–95.6 ng/g ww Yim et al. (2005)
River Ray (UK) 1.83–9.84 μg/kg ww Yamaguchi et al. (2003)
Danube River Delta (UK) 92.5–250 179–4829 47–1416 ng/g lw Covaci et al. (2006)
Rocky mountains (Canada) 0.023–1.2 0.17–52 0.5–59 ng/g ww Demers et al. (2007)
Alpine lakes (Switzerland) 6.6–22 7.5–40 ng/g ww Schmid et al. (2007)
River Elbe & Vltava (Czech) 43.6–69.6 μg/kg ww Hajšlová et al. (2007)
River Qiantang (East China) 1.86–5.85 2.65–133.5 ng/g ww Zhou et al. (2007)
Pearl River Estuary & Day Bay (China) 0.07–1.85 1.7–462 0.26–119 ng/g ww Guo et al. (2008)
Western Parks (US) 0.001–0.52 0.16–34 0.1–4.6 ng/g ww Ackerman et al. (2008)
Beijing (China) 0.58–8.48 7.54–88.3 n.d.–22.7 ng/g ww Li et al. (2008)
Mid-continental great rivers (US) 8.06–9.51 6.3–6.55 25.73–29.11 ng/g ww Blocksom et al. (2010)
Volta, Bosumtwi, Weija Lake (Ghana) 141.13–1126.51 4.09–10.61 ng/g lw Adu-Kumi et al. (2010)
New York City (United States) 1.0–98 ng/g ww McKelvey et al. (2010)
Tibetan plateau (Central Asia) 0.27–0.98 0.84–10.1 0.06–0.97 ng/g ww Yang et al. (2010)
Shadegan Marshes (Iran) 32–410 105–645 ng/g lw Davodi et al. (2011)
River Chenab (Pakistan) 2.5–8.6 8.83–190 14.3–45 ng/g ww Eqani et al. (2013)
River Indus (Pakistan) 0.17–22.78 0.94–42.85 0.12–5.35 0.81–44.20 ng/g ww This study
 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242 1239

Fig. 5. (a) PCA on the basis of feeding habit of fish species and (b) dendrogram for Agglomerative Hierarchical Clustering (using unweighted pair-group average).

also influence the levels of OCs in fish (Adu-Kumi et al., 2010). A signif- (C. catla). Among the two clusters, species in Cluster 1 included bottom
icantly high concentrations of DDTs in muscle of carnivore fish species feeders and showed highest concentration of ∑DDTs which may be
has been reported in contrast to other freshwater fish species with var- due to the fact that DDT biomagnified in different tissues of fish when
ious feeding habits by Kong et al. (2005). Therefore it has been sug- it accumulates in sediments and other biota. On the other hand, Cluster
gested that bioaccumulation of OCs is species-specific in fish due to 2 included the column feeder species with maximum concentrations of
their ecological features e.g. habitat and feeding modes. tri-CB that is probably due to increased mobility of low chlorinated bi-
By using unweighted pair group averages (UPGMA) as a linkage phenyls from substrate to water column (Voorspoels et al., 2004) there-
method and Euclidean distance as distance matrix, hierarchical clusters fore more uptake via gills.
were obtained. UPGMA was used in order to uncover the dissimilarities/
similarities between species and organic contaminants. Cluster analysis 3.5. Risk assessment of OCSs associated with fish consumption
grouped the 20 species into two clusters (Cluster 1: C. striatus,
C. mrigala, S. seenghala, M. armatus, R. rita, C. reba, L. calbasu. Cluster 2: In humans diet, total intake of OCs is mainly contributed by the lipid
Labeo pangusia, B. sarana, C. chitala, E. vacha, L. rohita, W. attu, C. carpio, content of the fish (Smith and Gangolli, 2002). In United States, dietary
L. dyocheilus, C. gaura, N. notopterus, C. idella, O. pabda) and one outlier exposure of contaminants through fish consumption accounts for a huge
1240 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242

fraction as compared to other foodstuff (Dougherty et al., 2000). Tsutsumi carnivore species indicating a lifetime cancer risk of 1 in a million due
et al. (2001) reported that consumption of shellfish and fish is a major di- to daily exposure of these contaminants through fish consumption.
etary source of dioxin-like compounds in Japanese population. High die- For CHLs, cancer risk was less than unity in herbivore while more than
tary intake of HCH via fish consumption in contrast to other food 1 for carnivore. Concentration of PCBs and DDTs were also greater
commodities has also been reported from India (Kumari et al., 2001). than unity even at the 50th percentile. This indicates that in humans, in-
gestion of DDTs and PCBs via contaminated fish can cause carcinogenic
3.5.1. Maximum admissible concentration (MAC) effects. Similar findings were reported for both cancer (HR ≥ 1) and
For fish consumption, USEPA (2000) has set a strict limit of 14.4 ng/g non-cancer risk (HR ≤ 1) from River Chenab (Eqani et al., 2013), coastal
ww for DDTs and 40% of our fish exceeded this ration. On the other region of China (Jiang et al., 2005) and South Korea (Moon et al., 2009).
hand, the European Union (Binelli and Provini, 2004) has established
a maximum admissible limit of 50 ng/g ww for DDTs, but none of our 4. Conclusions
sample exceeded this limit. Comparison of data with stringent value of
DDT (10 ng/g ww) set by Chinese Government (GB 18421-2001) for In the present study, OCs were detected in edible fish species from
fish consumption, 57% of the samples were overloaded. For HCHs, 22% the Indus River. DDTs were relatively more prevalent in the muscle tis-
of the fish samples exceeded the maximum admissible limit (10 ng/g sues. A significant variation in OCPs and PCBs contamination was ob-
ww) established by the European Union. For 7 congeners of PCBs (28, served between herbivorous and carnivorous species with
52, 101, 138, 153, 180), European Union Directive 1999/788 has considerably highest concentrations recorded in carnivores. This differ-
established a limit of 200 ng/g (lw) for food commodities (not particu- ence may be related to different trophic positions and feeding modes of
larly for fish). While our samples did not exceeded this value and ranged species. OCP residues in the Indus River are likely to originate from non-
between 0.08 and 4.36 ng/g ww. point sources via runoff, atmospheric deposition, and leaching due to
agricultural applications and vector control practices. Extensive indus-
3.5.2. Potential risk (risk characterization) trial activities and improper disposal of electronic waste are primarily
Calculation of hazard ratios is one of a suitable approach to assess the responsible for PCB contamination. Risk estimation indicated that
cancer and non-cancer risk associated with consumption of OCs con- DDTs and PCBs may pose a health risk to fish consumers. The results re-
taminated fish. HRs for both cancer and non-cancerous risks using vealed that reported concentrations of OCPs and PCBs in fish are low to
50th and 95th percentiles in herbivore and carnivore species are pre- moderately contaminated, when compared to other studies of the
sented in Fig. 6. For non-cancerous risk, all HRs of OCs in both the herbi- world on fish fauna. Since this study tested a limited number of fish
vore and carnivore species were b 1 at 50th and 95th percentiles, which samples, further investigation on freshwater ichthyo-fauna should be
is relatively due to small concentrations of OCs in samples hence signi- considered by the appropriate bodies at the national level in Pakistan.
fying no adverse effect by OCs exposure. Other factors may include low
rates of fish consumption (15 g/person/day) in the area as compared to Acknowledgments
India (47 g/person/day) (Muralidharan et al., 2009) and China (30 g/
person/day) (Yang et al., 2006). The authors of this manuscript are highly thankful to the World
On the other hand, cancer risk assessment based on 95th percentile Wide Fund for Nature, Pakistan (WWF, Pakistan) in providing facilities
for PCBs, DDTs, and HCB were all greater than unity in herbivore and for fish sampling.

Fig. 6. Hazard ratios for cancer (a) and non-cancer (b) risk assessment in general population.
 T. Robinson et al. / Science of the Total Environment 541 (2016) 1232–1242 1241

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