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Bulletin of Environmental Contamination and Toxicology

https://doi.org/10.1007/s00128-020-02987-7

Hepatic Toxicity in Etroplus suratensis (Bloch 1790): An Economically


Important Edible Fish in Vembanad Fresh Water Lake, Kerala, India
Arathi Pettamanna1 · Divya Raghav1 · Raveendran Harikumaran Nair1

Received: 28 April 2020 / Accepted: 3 September 2020


© Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract
Fish consumption from contaminated water-bodies is a serious health issue. This study conducted to reveal the presence
of heavy metals and bisphenols in Vembanad lake, an exploiting tourist spot in Kerala, receiving untreated agricultural,
domestic, municipal, and industrial effluents. We evaluated aquatic contaminant impact on hepatic stress markers in Etroplus
suratensis from fragile Vembanad lake. The significant difference in water physiochemical parameters, the concentration of
heavy metals, and bisphenols (BPA and BPS) were studied. Hepatic tissue of E. suratensis inhabited in lake featured with
high iron (11.29 ± 0.39 ppm) and BPA (0.02412 ± 0.0031 µg/mL) content along with an increased hepatic stress marker and
distorted hepatic structure. The study highlights the presence of high iron and BPA in edible fish. The study recommends
monitoring of physiochemical characters of freshwater lakes is essential for better survival of freshwater flora and fauna.

Keyword Freshwater contamination · Heavy metal toxicity · Bisphenols · Hepatic damage

Vembanad backwater tourism with cruise houseboats et al. 2015; Brede et al. 2003). Persistent chemical impreg-
emerged as a backbone of the Kerala tourist sector, India, nated sources around the terrain of Vembanad lake is a seri-
which lead to a tremendous increase of anthropogenic activi- ous issue to address. So, the prime focus of our study is to
ties in the shore of Vembanad. Mismanagement of tourist evaluate the possibility of infiltrated chemicals like heavy
activities generates a huge quantity of solid waste deposits metals, BPA, and BPS in Vembanad lake water from waste
around the terrain of Vembanad lake. There are no effective disposal.
control mechanisms to maintain Vembanad resources from Vembanad lake is most prominent with more than 70
industrial, agricultural, municipal, and domestic drainages. edible species (Synudeen 2017). Among them, E. suratensis
As waste effluents enter the surface water, chemical contami- is an edible fish with high economic value than other fresh-
nants including heavy metals and xenoestrogens also enter water fishes. According to Abraham et al. (2019) in IUCN
the aquatic system. Song et al. (2010) revealed that industrial red data report, mature E. suratensis in Kerala facing a popu-
drainage serves as a point source for heavy metal pollution in lation decline and are in the least concerned conservation
the Changjiang river. Shyleshchandran et al. (2018) reported status. Fishes are the toppers of the aquatic food chain and
that sediments of Vembanad lake act as a major reservoir are extremely sensitive towards aquatic pollutants, served as
for heavy metal contamination. High levels of solid waste bio-indicators of environmental pollution. The enrichment
disposal like magazines, newspapers, paper rolls, food cans, of persistent aquatic pollutants from the uncontrolled waste
receipts, and plastic products have been noticed in certain disposal in freshwater resources may be one of the reasons
hotspots of the Vembanad lake. These solid waste contents for declining E. Suratensis. Hence, the discharge of heavy
are currently recognized as an exposure source for xenoes- metal and bisphenol impregnated sources in the Vembanad
trogens like bisphenol A (BPA) or bisphenol S (BPS) (Rocha terrain created a need for their monitoring in E. suraten-
sis. Since the fish liver is the center of metabolic activities
(James 1986) and lake contaminants likely to be metabolized
* Raveendran Harikumaran Nair
harinair@mgu.ac.in in this organ. The various hepatic activities are prone to the
toxic effects and can be used as indicators of freshwater pol-
1
Physiology Research Laboratory, School of Biosciences, lutant effect. Therefore, the study focused to evaluate the
Mahatma Gandhi University, Kottayam, Kerala 686560, cumulative effect of heavy metals and bisphenol analogs
India

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Vol.:(0123456789)
Bulletin of Environmental Contamination and Toxicology

in liver damage in E. suratensis inhabitant of Vembanad and collected in a heparinized tube. Fishes were ice packed
freshwater lake, Kerala. and brought to the laboratory and hepatic tissue excised
and subsequently used for biochemical analysis.
Identification and quantification of BPA and BPS were
Materials and Methods made by comparing HPLC retention time of sample peak
with those of the authentic standards. Water samples were
Vembanad lake, Kerala, India (9° 36′ 34.8″ N 76° 25′ 18.6″ prepared by the method Rezaee et al. (2009). In brief, a
E) was chosen as a study site because the coastal regions mixture of acetone (2 mL) and chloroform (600 µL) was
are noticed with solid waste deposition. Lake samples were injected rapidly into a 5 mL sample solution using a 5 mL
compared with farm samples, are noticed with effective solid glass syringe. The produced cloudy solution was centrifuged
waste management (Fig. 1). for 10 min at 8000 rpm (Eppendorf centrifuge 5804, Ham-
Water (6 L) and E. suratensis (Pearl spot or Karimeen) burg Germany). The sedimented phase was evaporated by
(9) were collected from the area of Vechoor (2 L water; placing in a water bath; the residue was dissolved in 1 mL
three fishes), Kumarakom (2 L water; three fishes) and methanol, filtered through a 0.22-micron filter, and sub-
Puthuchara (2 L water; three fishes) of Vembanad Lake. jected to HPLC analysis. Hepatic tissues were prepared by
For comparison, unpolluted farm samples (6 L water; six the method Aristiawan et al. (2015). For this, hepatic tissues
fishes) were considered as controls. Samples were col- were homogenized and mixed with dichloromethane shaken
lected from January 2018 to March 2018. Water samples for 10 min. Then 10 mL acetonitrile was added, and the mix-
were collected from the bottom of the water sources with ture was shaken for 5 min, centrifuged at 4500 rpm. Finally,
a clean glass bottle (Knapton 1985). Water quality param- the acetonitrile phase was transferred and filtered through
eters were measured using procedures described in the a 0.22-micron filter and a 20 µL sample injected to HPLC.
APHA method (1998). Heavy metals (arsenic, lead, mer- The LOD (Limit of Detection) value detected from the
cury, cadmium, and iron) were determined with the aid of equation 3 SB/m. The LOQ (Limit of Quantification) value
bulk scientific atomic absorption spectrophotometer (AES, was calculated from equation 10 SB/m. Where ‘SB’ is the
2000 series, Shimadzu, Japan). Quality assurance and standard deviation and ‘m’ is the slope. The regression coef-
quality control were assessed in duplicates, with method ficient (R2) value of the calibration curves was 0.999 for
blanks and standard reference materials. Three replicates BPA and BPS. The concentration was measured from the
were tested for the determinations of heavy metals. A regression equation Y = mx + c. The levels of lipid peroxi-
total of 15 E. suratensis species were collected from the dation (Buege and Aust 1978) and the activities of superox-
study sites using a net trap (mesh size 1.5 cm). Species ide dismutase (Kakkar et al. 1995), catalase (Aebi 1984),
were identified by using food and agricultural organiza- and glutathione (Ellman 1959) were estimated from liver
tion (FAO) species identification datasheet. Total length homogenates. Serum ALT and AST were analyzed following
(11–14.5 cm) and body weight (65.7–83.1 g) of collected the manufacturer’s instructions from the Agape diagnostic
fishes were recorded. The gender difference was not con- kit, India. Histology assessment of hepatic tissue was done
sidered. Blood samples were taken from the caudal vein with hematoxylin and eosin staining (Ke et al. 2010).

Fig. 1  Sampling stations ( Source: Google map). a Kumarakom, Vembanad Lake, Kottayam, Kerala, India. The sampling area covered a total
distance of 13.06 km from Vechoor to Puthuchara of Kumarakom. b J S farm, Neendoor, Kottayam, Kerala, India

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Bulletin of Environmental Contamination and Toxicology

Statistical analysis was done using Post Hoc Multiple water quality parameters. Current study obtained significant
comparison test in SPSS 16 software (Chicago, IL, USA). variations in the quality of Vembanad lake water compared
A significant difference (p < 0.05) was considered from the to farm water.
mean value of six samples from Vembanad (nine fishes were The level of Cu (essential micronutrient) in Vembanad
collected and three omitted due to higher range) and farm water was found to be 0.007 ± 0.0009 ppm and farm water
samples ± standard deviations (SD). is 0.010 ± 0. 0014 ppm; both values are within the range
(0.005–1.5 ppm) of the recommended IS limit. We obtained
a high concentration of Fe (0.432 ppm), Cl (> 15,300 ppm),
Results and Discussion and S (> 1540 ppm) in freshwater. Vembanad lake Fe con-
centration greatly varied (0.87–2.15 mg/L) during mon-
The quality of water was assessed by employing the analysis soon season (Verma et al. 2002). Sulfate and iron contents
of water chemistry parameters (Table 1). in aquatic bodies usually result from industrial sewage and
The optimum pH and alkalinity for pearl spot fishes are mine waste (Canario et al. 2003). Sulfate toxicity results in
6.5–9 and 50–400 ppm, respectively. High alkalinity coupled ionic stress (Heming and Blumhagen 1988) in fishes. Iron
with a rise in pH may cause the death of fishes (Saraswathy contamination in fishes causes gill degradation and growth
et al. 2015). Vidya et al. (2020) reported that Vembanad lake retardation (Elahee and Bhagwant 2007). S and Fe related
pH varied from 6.69 to 8.08, adjacent to the industrial area. studies are limited from the Vembanad region. Free Cl, As,
The present study obtained high pH (8.8 ± 0.12), high alka- Pb, Cd, and Hg were not detected in freshwater and farm
linity (115.33 ± 2.45) and high hardeness (3300.33 ± 103.27) water samples.
from lake water compared to farm water. Optimal hard- Heavy metal contamination has been reported from the
ness for fishes is 15–375 ppm. High hardness levels might Vembanad region (Ramasamy et al. 2017; Shyleshchan-
also cause a low fertilization rate in fishes. Ammonia is a dran et al. 2018). Our study reports that Vembanad lake is
nitrogenous waste product causes (> 1 ppm) gill irritation contaminated with heavy metals together with bisphenol
and respiratory problems in fishes (Saraswathy et al. 2015). analog A (BPA), a tracer for plastic burning (Darbre 2018).
Our study resulted in higher ammonia (1.81 ± 0.079 ppm) Sruthy and Ramasamy (2017) suggested that microplastics
content in Vembanad lake. The seasonal concentration of contamination higher in Vembanad lake. Until no data has
ammonia in Vembanad lake varied from 0 to 31.16 μg/L been reported regarding the presence of BPA in Vemba-
(Laxmilatha et al. 2005). High oxygen demand might be nad lake water and edible fishes. The results may reflect
critical to the survival of most aquatic animals. Thus, higher the contamination of freshwater shore with plastic waste,
BOD (8.1 ± 0.12 mg/L) in the Vembanad freshwater system and it might be higher than the studied artificial ecosystem
denotes less availability of oxygen to sustain their biota. (farm). Heavy metals and BPA are the widespread pollutants
Vincy et al (2012) studied high TDS value (3.3–5.9 mg/L) of great environmental concern. We found that Vembanad
and high hardness (371–417 mg/L) in Vembanad lake water lake contains a high level of Fe and BPA compared to the
during monsoon season. The current study obtained TDS farm (Tables 2 and 3).
value s 42638.2 ± 953.15 ppm from lake water compared The level of BPA in pearl spot liver inhabiting Vembanad
to farm water.iChanging salinity associated with high TDS was found to 0.00314 and 0.0241 µg/mL, respectively. BPA
might eliminate less tolerant species from the aquatic system was not detected in pearl spot liver inhabiting farm water.
(Saraswathy et al. 2015). Budhlani et al (2014) noticed that The occurrence of BPA (330 ng/L) has been reported in
the discharge of sewage and solid waste in to the river affects the Dutch water system, Netherlands (Belfroid et al. 2002)

Table 1  Physiochemical Parameters IS ­valuea Freshwater Farm water


analysis of freshwater and farm
water Appearance Clear Clear Clear
Color 0–15 HZ 2.16 ± 0.39 2.8 ± 0.40
pH 6.5–8.5 8.8 ± 0.12* 7.3 ± 0.14
Alkalinity 20–200 ppm 115.33 ± 2.45* 108.83 ± 2.20
Hardness 15–375 ppm 3300.33 ± 103.27* 332.16 ± 7.75
Ammonia (NH3) 0.06 ppm 1.816 ± 0.079* 0.052 ± 0.003
Biological oxygen demand (BOD) 3 mg/L 8.1 ± 0.12* 4.12 ± 0.06
Total dissolved solvents (TDS) 500–2000 ppm 42638.2 ± 953.15* 1271.5 ± 45.96

*p < 0.05: compared to farm water. Values are mean of six samples from each site ± SD
a
IS Indian standard (IS10500-2002) range/value of water chemistry parameters

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Bulletin of Environmental Contamination and Toxicology

Table 2  Concentration of heavy Heavy metals IS ­valuea Fresh water Farm water Fresh water fish Farm fish
metals in freshwater and farm
water and their bioaccumulation Copper (Cu) 0.005–1.5 ppm 0.007 ± 0.0009 0.010 ± 0. 0014 < LOD < LOD
in the liver of pearl spot fish
Iron (Fe) 0.3–0.4 ppm 0.432 ± 0.045* 0.234 ± 0.011 11.29 ± 0.39* 8.73 ± 0.63
inhabiting such water
Chloride (Cl) 240–300 ppm 15325 ± 902.57* 260 ± 14.47 < LOD < LOD
Sulphate(S) 240–300 ppm 1548.66 ± 79.97* 255.83 ± 5.74 < LOD < LOD
Free Cl 100 ppm ND ND NA NA
Arsenic (As) 0.01 mg/L BDL ND ND ND
Lead (Pb) 0.01 mg/L BDL ND ND ND
Cadmium (Cd) 0.003 mg/L ND ND ND ND
Mercury (Hg) 0.001 mg/L ND ND ND ND

Values are Mean ± SD


LOD limit of detection, NA not analyzed, BDL below detection level, ND not detected
*p < 0.05, compared to farm samples
a
IS value: Indian standard (IS10500-2002) range/value of heavy metals in water

Table 3  The level of BPA and BPS in waters of Vembanad lake and farm and their bioaccumulation in the liver of pearl spot fish inhabiting such
water
Bisphenols Vembanad water Vembanad fish liver Farm water Farm fish liver

BPA (µg/mL) 0.00314 ± 0.00014a 0.02412 ± 0.0031b < LOD ND


BPS (µg/mL) ND ND ND ND

BPA bisphenol-A, BPS bisphenol-S, ND not detected, LOD limit of detection


a,b
Values are expressed as mean ± SD

with high content BPA in the fish liver (75 ng/g) than fish pathogenesis can exert by the depleted status of antioxidants
muscle (1–11 ng/g). Water sources from southern India were like SOD, CAT, and GSH (Fig. 2).
also found to be polluted with BPA (2.8–136 ng/L) (Sel- The mean activities of antioxidant enzymes (SOD, CAT,
varaj et al. 2014). The occurrence of BPA analog (BPS) and GSH) were found to be significantly (p < 0.05) lower
in the river system has been noticed in several studies (Jin in freshwater fishes than farm fishes. Our study obtained
and Zhu 2016; Wan et al. 2018). In our study, BPS was not an augmented level of MDA (peroxidation marker) in pearl
detected in the Vembanad system. But the release of excess spot fish liver from freshwater. The analyzed hepatic tissue
heavy metals like iron, calcium, sulfur, and xenoestrogens of freshwater fishes shows higher activities of AST and ALT
like BPA into the freshwater bodies may affect the quality in lake fishes. Therefore, we assume that the cellular level
of food resources like E. suratensis. Fishes are the environ- peroxidation rate in the freshwater fish liver is augmented
mental sentinel for aquatic toxicants. Fishes can concentrate by the depletion antioxidant enzymes. The cytoplasmic
pollutants, preferentially in fatty tissue like liver from their vacuolation and tissue disintegration in freshwater fish liver
surroundings medium (Denton and Burdon 1986). The study indicate the extent of liver toxicity during their exposure to
of Xavier et al. (2019) revealed that E. suratensis survived environmental contaminants. These changes were observed
from the chronic exposure of Cu and Zn. Chandrasekar et al. in those fishes contaminated with Fe and BPA. In support
(2014) mentioned the adaptation of E. suratensis over chang- of our results, it has been suggested that the changes like
ing salinity. Our results have shown that the bioaccumula- hepatic vacuolation, elevated AST and ALT, reduced anti-
tion of iron and BPA were significantly higher in freshwater oxidants in fishes can arise from iron (Vasanthi et al. 2013)
fishes when compared to the farm. Iron and BPA contamina- or BPA (Faheem and Lone 2017) exposure. The obtained
tion has been reported from water bodies (Slaninova et al. histopathology of pearl spot liver reflects severe hepatic
2014; Wong et al. 2017). While BPA related studies in Vem- damage (Fig. 3).
banad regions are limited. Thus, Fe and BPA might have a role in degrading the
Faheem and Lone (2017) revealed that the exposure of quality of Vembanad lake water and fish resources. The
BPA to aquatic organisms can enhance reactive oxygen study warranted that proper monitoring and management
specious production with subsequent damage to the lipid of river ecosystems is the need of the hour for the protec-
bilayer membrane. The peroxidation reactions in the cellular tion and safety of species inhabiting there. The inefficiency

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Bulletin of Environmental Contamination and Toxicology

Fig. 2  Level of stress markers in pear spot fishes inhabiting freshwa- nm/mg tissue; CAT: U/min/mg tissue; SOD: U/mg tissue. Values are
ter lake and farm water a AST and ALT. b MDA, CAT, SOD, and expressed as mean ± SD (n = 6), *p < 0.05 when compared to values
GSH. ^Denotes units of stress markers; MDA: nm/mg tissue; GSH: of farm samples

Fig. 3  Hepatic histology of pearl spot fish liver inhabited in farm and freshwater a Freshwater fishes show hepatocytes (black arrow) with nor-
mal architecture b Farm fish liver possess lipid type vacuolation (black arrow) and distorted hepatic structure

will lead to the destruction and extinction of aquatic species by tourist invasion and monitoring the health of economi-
in the future. The research on community health effects of cally important pearl spot fishes. Regarding health risk, the
consumption of fishes from high content iron and BPA water current study high lightened the need for more research to
needs important attention. evaluate the role of aquatic contaminants on other species
The release of additive chemicals from plastics and of commercial interest as human food.
other commodities to a freshwater system and interfere
with the food web is challenging. The notable changes in Acknowledgements This work was financially supported by the
Department of Science and Technology, New Delhi. We thank the
freshwater quality parameters render the environmental Department of Biotechnology, Government of India for the excel-
contaminant like heavy metals and xenoestrogens bio- lent research facilities supported through the DBT-MSUB-IPLS
availability. It should be noted that most of the heavy (BUILDER) program. We also thank Mr. Dineep Vasudevan, Inter-
metals are essential for various physiological processes, University Instrumentation Centre, School of Environmental Sciences,
Mahatma Gandhi University for technical assistance on this work.
but the bioaccumulation produces a hazardous effect on
aquatic fauna. Therefore, it will be important in the future
to investigate the routes of exposure of aquatic contami-
Compliance with Ethical Standards
nants to fish fauna. The study is an effort to monitoring Conflict of interest The authors declare that they have no conflicts of
the ecological health of freshwater ecosystems surrounded interest.

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Bulletin of Environmental Contamination and Toxicology

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