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REGRESSION ANALYSIS FOR PREDICTING THE DURATION DEPENDENT RESPONSE OF OXIDATIVE STRESS DYNAMICS AND NUCLEAR ANOMALIES IN CATLA CATLA EXPOSED TO CHLORPYRIFOS AND ENDOSULFAN.

Byline: H. Naz, S. Abdullah, T. Ahmed, K. Abbas and M. U. Ijaz

Keywords: Fish, Antioxidant enzymes, genotoxicity, tissues, insecticides

INTRODUCTION

The application of pesticides in forestry, agriculture, veterinary and public health practices are gaining attention because of their potential to control pests such as weeds, insects and unwanted aquatic fauna and flora (Abu-Darwish et al., 2011). The exponential use of pesticides resulted in a serious contamination of brackish and freshwater bodies which are the ultimate sink of these chemicals and their residues (Lal, 2012; Deka and Mahanta, 2016; Nugegoda and Kibria, 2017). The synthetic compounds can cause the changes in behavior and physiology of aquatic animals especially fish due to their persistent and bio-accumulation properties (Liess et al., 2005). Even at very low quantity, pesticides can affect the basal metabolism.

Sometimes these effects expressed as sudden mortality or by other changes like reduced growth, development and reproduction, depending on the pesticide's formulation, dose, degradation capability and also on ability of fish to metabolize them (Lal et al., 2013; Sabra and Mehana, 2015). According to Chakraborty and Roy (2017) pesticides also cause alterations at biochemical and genomic level by targeting the metabolic proteins and nucleic acids, respectively.

Most commonly used pesticides in the fields includes organochlorine, organophosphate, pyrethroids, carbamates, necotenoides and trizole (Srivastava and Singh, 2014; Sarba and Mehana, 2015). Organochlorine insecticide such as endosulfan is widely used in horticultural and agricultural crops (Tuduri et al., 2006; Sutherland et al., 2004) to minimize the insect pest's population (Rehman et al., 2016). Endosulfan has direct effect on fish's central nervous system resulted in hyperactivity, convulsions and sometimes cause sudden mortality. Among organophosphorus pesticides, chlorpyrifos is commonly used in agriculture and is highly toxic to fish by inhibiting the acetylcholinesterase activity in nerve cells (Yen et al., 2011) and also induced gut microbiota dysbiosis, oxidative stress, neurotoxicity, disruption of endocrine and immune system (Zhang et al., 2017; Wang et al., 2019).

Pesticides are well known inducer of oxidative stress by forming the reactive oxygen species (ROS) leading to blockage of antioxidant enzymes activities which are scavenger of free radicals. The oxidative stress in the cell can be minimized by antioxidant enzymes like superoxide dismutase (SOD), glutathione peroxidase (GPx), catalase (CAT) (Agarwal et al., 2010) and glutathion S-transferase (GST) one of the phase II enzymes protect against free radicals by conjugation (Rahaman et al., 1999).

Currently, micronuclei (MN) assay and other nuclear abnormalities (NAs) of erythrocytes are extensively used as bio-marker of genotoxicity and mutagen in fish exposed to contaminants (Bolognesi and Hayashi, 2011; Obiakor et al., 2012). This assay also identifies the single cell for NAs includes lobed, blebbed, notched and bi-nucleated cells but exact pathway of their formation is not understood (Barsiene et al., 2006; Da-Rocha et al., 2011). Ample of research was conducted on single effect of pesticides but combined impact of these chemicals is scarce. Due to above mentioned toxicity of pesticides and their increased use, this research was planned to assess the toxic effect of pesticides mixture on oxidative stress dynamics and nuclear anomalies of Catla catla.

MATERIALS AND METHODS

The freshwater fish, Catla catla were acquired from a Fish Seed Hatchery Faisalabad and shifted to wet laboratory of fisheries research Farm UAF to acclimatized the laboratory conditions for approximately a couple of weeks. For experimental trail, acclimatized fish (n=20) were placed into glass aquaria of 100 L water capacity. The physical (pH=7.25; temperature= 28AdegC) and chemical properties (dissolve oxygen= 5.00ppm; water hardness= 225 mgL-1) of water were maintained during the experimental period. A stock-I solutions of chlorpyrifos(C) and endosulfan (E) were prepared separately by dissolving 1 g in 100ml methanol (95%). The final stock-II solutions (10 ppm) were made in deionized water while required C+E mixture (1:1) was made for treating the fish. Fish were kept under acute exposure of C+E mixture for 4-days and sampling was done at 1-day interval. The tolerance limits (LC50) of C. catla against C+E was computed as 1.35+-0.01ugL-1 (Naz et al., 2019b).

Oxidative stress dynamics: A number (n=5) of fish were sacrificed at each sampling and organs viz. gills, liver, kidney, brain, heart and muscle were separated to assess the superoxide dismutase (SOD) by Giannopolitis and Ries (1977), peroxidase (POx) and catalase (CAT) by Chance and Mehaly (1977), and glutathione S-transferase (GST) by Mannervik (1985). Organ homogenates were prepared according to the method explained by Naz et al. (2019a).

Micronuclei test: For each sampling, fish blood was taken from caudal vein and smeared were made on slide and also fixed immediately with methanol for 10 minutes and stained with 10% Giemsa solution for 8 minutes (Barsiene et al., 2004). Micronuclei (MN) and nuclear abnormalities (NAs) including bi-nucleated cells, dumbbell shaped nuclei, blebbed, notched and de-shaped nuclei were scored according to the criterion mentioned by Fenech et al. (2003). The MN frequency was calculated by applying following formula:

MN%= Number of cells containing micronucleus/Total number of cells counted x 100

Statistical Analyses: The statistically significant (pa$?0.05) difference between stressed and unstressed fish antioxidant enzymes were calculated by applying ANOVA followed by Tukey test. For MN and NAs non-parametric criteria, Mann-Whitney U test was used. Relationship among various parameters and duration of exposure were found out by applying linear regression analysis. The analyses were performed in statistix 8.1 version and graphs were drawn in MS Excel.

RESULTS AND DISCUSSION

Oxidative stress dynamics: In the present research, statistical modeling called linear regression analysis was applied to find out the casual relation a dependent variable (enzymes/DNA damage) and one independent variable (duration of exposure). Table 1 shows the relationship between enzymes activities with exposure time of C+E mixture. The SOD activity in organs of fish showed the significant and positive dependence with duration of exposure. The CAT activity in gills, liver and kidney showed significantly positive relation while brain, heart and muscle had significantly negative dependence with duration which showed that it decreased with increasing exposure time. The activity of POx in gills, brain and heart showed a significant dependence on exposure duration while liver, kidney and muscle had non-significant dependence with exposure. The GST activity had highly significant positive relation with exposure time.

Figure1 shows that SOD, POx and GST activities augmented in all organs of fish due to mixture exposure. However, CAT activity induced in liver, kidney and gills of fish while it was declined in heart, brain and muscles of fish. Same were reported by Unal et al. (2019) who noted the decrease CAT activity in brain and intestines in rotenone exposed zebra fish. Naz et al. (2019a) also observed augmentation in CAT activity in liver, kidney and gills of L. rohita after C+E exposure while it was lowered in muscle, brain and heart. Time-dependent increase in gill, kidney and liver CAT level of L. rohita under lethal and sub-lethal exposure of malathion was studied by Patil and David (2013). Lihocin exposure caused gradual increase in GPx and SOD of C. catla in gills, liver, kidney and muscle tissues exposed for 3, 7, 14, 30 and 45 days where as CAT activity is gradually decreased throughout the study period (Vineela and Reddy, 2014).

Exposure to endosulfan+deltamethrin increased the GST level in muscle, liver, kidney and gills of Channa striata (Abdullah et al., 2018). Naz et al. (2017) noted the time reliant increased in liver SOD level in three Indian major carps exposed to tertiary insecticides mixture of bifenthrin, chlorpyrifos and endosulfan. Naz et al. (2019a) also studied the increased SOD, POx and GST activities in bronchial, muscle, hepatic, neural, and cardiac tissues of L. rohita due to C+E exposure. Endosulfan exposure induce time-dependent raise in CAT, POD, SOD and GST activities in brain, gills, muscle and liver of L. rohita (Ullah et al., 2016). Ullah et al. (2014) observed the raise in CAT and POx levels in liver, brain, gills and muscle tissues of Masherr exposed to cypermethrine as exposure time increased. Activity of GST and CAT shows a significant increase afterday 1 than decreased upto 5 day in liver and brain of fish exposed to Quinalphos as compared to the control (Greeshma et al., 2019).

Exposures of endosulfan and imidacloprid mixture on zebrafish caused time-dependent decrease in gill, liver and muscle SOD and CAT activities (Muazzam et al., 2019). Delthametrin triggers the CAT, GPx and SOD activities in zebra fish under acute exposure (Strungaru et al., 2019). Vijayakumar et al. (2016) studied the accelerated SOD and CAT level in cypermethrin exposed L. rohita. A time-reliant significant increase in liver CAT, SOD, POx, and GST levels in rohu due to malathion exposure noted by Ullah et al. (2018). Pandey et al. (2001) documented the increased GST and GPx level of fish exposed to endosulfan while CAT activity was decreased significantly in liver, kidney and gills. Thenmozhi et al. (2011) assessed the higher level of gills, muscle and liver GST and CAT due to malathion in L. rohita. Acute (96 h) exposure of methyl parathion caused significant raised in liver, muscle, and gills SOD, CAT and GST activities of fish (Monteiro et al., 2006).

Nuclear Anomalies: The results of geno-toxicity showed that MN and NN had significantly positive relation with duration while other NAs had non-significant relation with time exposure (Table 2). Figure 2 showed that C+E mixture exposure increased the formation of MN and NAs in RBCs of fish in relation to control. Moreover, the high value of R2 for fish predicts significantly high reliability of this regression model. Similarly, Ansoar-Rodriguez et al. (2015) documented the production of MN and NAs in blood of Oreochromis niloticus due to imidacloprid concentration. Labeo rohita showed higher frequency of MN and NAs (notched, blebbed, bi-nucleated and lobed nuclei) in blood when exposed to triazophos for 2-, 3-and 4-day of post-treatment (Ghaffar et al., 2015). Significant induction of MN and NAs in Channa punctata erythrocytes due to deltamethrin was observed by Ansari et al. (2009).

Anbumani and Mohankumar (2015) observed the duration-dependent induction of MN and NAs in Catla catla exposed to butachlor and monocrotophos mixture. Muranli and Guner (2011) noted the MN and NAs formation in erythrocytes of mosquito fish treated with lambda-cyhalothrin for 6-,12-, 24-, and 48-h. Islam et al. (2019) reported the increased frequency of MN in RBCs of sumithion exposed striped catfish. Wu and Ding (2016) noted the formation of MN in erythrocytes of top mouth gudgeon (Pseudorasbora parva) by endosulfan exposure for 48-and 96-h. Dichlorvos exposure increased the rate of MN formation in Misgurnus anguillicaudatus (Nan et al., 2015). After exposure to dimethoate, the induction of MN was increased in Channa punctatus as the concentration and exposure time increased (Ali et al., 2014). C. chanos showed significant increase in MN when exposed to chlorpyrifos and carbendazim (Palanikumar et al., 2014).

Oreochromis mossambicus showed the high frequency of MN in erythrocytes after exposure to different pesticides viz. chlorpyrifos, cypermethrin, buctril, malathion and lambda-cyhalothrin (Naqvi et al., 2016). Nwani et al. (2010) documented time specific MN generation in blood of carbosulfan treated Channa punctatus for 94-h.

Table 1: Relationships between antioxidant enzymes activities and duration of C+E mixture exposure.

Enzymes###Organs###Regression Equation###SE###r###R2

###Gills###46.4 + 0.665**Time###0.01925###0.998###0.997

###Liver###80.6 + 0.590 **Time###0.01732###0.998###0.997

###Kidney###50.5 + 0.746**Time###0.05142###0.991###0.986

SOD###Brain###70.5 + 0.533 **Time###0.02938###0.994###0.991

###Heart###23.8 + 0.723 *Time###0.04894###0.991###0.986

###Muscle###22.0 + 0.378 *Time###0.02163###0.993###0.990

###Gills###210 + 0.478 **Time###0.08546###0.940###0.910

###Liver###249 + 0.510 **Time###0.04522###0.985###0.977

CAT###Kidney###162 + 0.412 ** Time###0.01288###0.998###0.997

###Brain###115 - 0.459** Time###0.02852###0.992###0.988

###Heart###97.4 - 0.506 ** Time###0.06152###0.971###0.957

###Muscle###178 - 0.486 ** Time###0.05321###0.977###0.965

###Gills###1.97 + 0.0371** Time###0.0006038###0.999###0.999

###Liver###2.74 + 0.0470 Ns Time###0.01237###0.879###0.818

###Kidney###2.11 + 0.0275 NS Time###0.007607###0.867###0.800

POx###Brain###2.32 + 0.0406** Time###0.001622###0.997###0.995

###Heart###1.14 + 0.0365** Time###0.0003997###0.999###0.999

###Muscle###1.13 + 0.0269NS Time###0.008510###0.833###0.749

###Gills###203 + 1.94**Time###0.05402###0.998###0.998

###Liver###235 + 2.46**Time###0.2285###0.983###0.975

###Kidney###232 + 2.06 **Time###0.1645###0.987###0.981

GST###Brain###331 + 2.26**Time###0.1635###0.990###0.985

###Heart###156 + 1.75**Time###0.2037###0.974###0.961

###Muscle###281 + 2.56**Time###0.03139###0.990###0.990

Table 2: Relationships between nuclear anomalies in fish and duration of C+E mixture exposure.

Nuclear###Regression Equation###SE###r###R2

Abnormalities

MN###1.05 + 0.0282 *time###0.003691###0.967###0.95

BN###0.570 + 0.0299Nstime###0.003251###0.977###0.965

DN###- 0.0200 +0.00983Ns time###0.0008457###0.985###0.978

BEN###0.105 + 0.0153Nstime###0.001808###0.973###0.959

NN###0.205 + 0.0115*time###0.0006495###0.994###0.991

DES###0.280 + 0.0495 Nstime###0.002919###0.993###0.990

Conclusion: This study indicates a positive dependence of antioxidant enzymes activities of Catla catla on exposure duration of insecticides mixture. Moreover, this study also suggested that induction of MN and NAs can be used as a non-specific biomarker and can also successfully apply to evaluate geno-toxic potential of agrochemical pollutants in aquatic animals like fish.

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Author:H. Naz, S. Abdullah, T. Ahmed, K. Abbas and M. U. Ijaz
Publication:Journal of Animal and Plant Sciences
Date:Jun 22, 2021
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