Bioaccumulation of heavy metals and assessment of the human health risk of consumption of Clarias gariepinus and Parachanna obscura from the Owan River, Edo State, Nigeria

INTRODUCTION

In recent years, fish species have attracted considerable interest in studies assessing biological and biochemical responses to environmental contaminants (Parente, Hauser-Davis, 2013). Fish are dominant species in virtually every aquatic ecosystem and play a fundamental role in the aquatic food-webs because of their function as carriers of energy from lower to higher trophic levels. The understanding of toxicant uptake, behaviour, and responses in fish is therefore of high ecological relevance (van der Oost et al., 2016).

Heavy metals are naturally occurring elements that have a high atomic weight and a density at least five times greater than that of water. Their multiple industrial, domestic, agricultural, medical, and technological applications have led to their wide distribution in the environment raising global public health concerns over their potential effects on human health and the environment (Scientific India, 2017). The concentration of heavy metals in an organism is the product of equilibrium between the concentration of the metal in an organism’s environment and its rate of ingestion and excretion (Idodo-Umeh, 2002). Toxic effects occur when excretory, metabolic, storage, and detoxification mechanisms are no longer able to counter uptake (Kalay, Canli, 2000). Unlike organic contaminants that lose toxicity with time by biodegradation, heavy metals cannot be degraded and their concentration can be increased by bioaccumulation and biomagnification (Aksoy, 2008). Bioaccumulation is the net build-up of substances from water in an aquatic organism as a result of enhanced uptake and slow elimination of such substances (Bhattacharya et al., 2006). This is largely attributed to differences in the uptake and depuration period for various metals in different fish species (Tawari-Fufeyin, Ekaye, 2007). Studies have shown that accumulation of heavy metals in a tissue is mainly dependent on its concentration in water and its exposure period, although other environmental factors such as salinity, pH, hardness, and temperature play significant roles in their accumulation (Quan et al., 2007; Jeffree et al., 2006; Singh et al., 2007).

This study was aimed at investigating the bioaccumulation of five heavy metals (Ni, Zn, Pb, Fe and Cr) in organs (the liver and muscle) of Clarias gariepinus and Parachanna obscura from the Owan River and at identifying the health risks they pose to humans through consumption.

MATERIALS AND METHODS

Study area

The study was conducted along a stretch of the Owan River in Ovia North-East Local Government Area, Edo State (Longitude 5°45’E and 5°48’E and Latitudes 6°48’N and 6°49’N) (Fig. 1). The river takes its origin from Otuo in Owan East Local Government Area, runs through Okpokhumi, Sabongidda Ora, and empties into the River Osse, which transverses through Gelegele to Iziedema communities and finally empties into the Atlantic Ocean.

The Owan River is relatively calm and pristine with respect to the water quality, and supports a rich diversity of aquatic insects (Edegbene, Arimoro, 2012; Enuneku et al., 2013) and serves as a major source of water for domestic purpose within the communities along its banks (Omoigberale et al., 2014).

Collection of water samples

Eight (8) water samples were collected from two sampling points between the hours of 9:00 am and 12:00 noon from July to October 2017. Standard methods and procedures were followed during sample collection.

Analysis of water samples

In the laboratory, pH, Total Dissolved Solids (TDS), Total Suspended Solids (TSS), Electrical Conductivity (EC), Turbidity, Dissolved Oxygen (DO), Biochemical Oxygen Demand (BOD5), chloride, sodium, potassium, magnesium, sulphate, nitrate, phosphate, lead, iron, zinc, nickel, and chromium were identified according to the procedures outlined in the Standard Methods for the Examination of Water and Wastewater (APHA, 1998). The surface water temperature was taken in situ using a mercury-in-glass thermometer. Heavy metals – nickel (Ni), zinc (Zn²⁺), lead (Pb²⁺), iron (Fe²⁺), and chromium (Cr²⁺) were identified after digestion of samples using an atomic absorption spectrophotometer (AAS).

Digestion of fish samples

In the laboratory, routine body measurements such as the total length and the standard length in centimetres (cm) were taken to the nearest 0.1 cm using a measuring board. Fish weight in grams (g) were taken using a sensitive Mettler balance (Mettler P. E. 360) and the values recorded to the nearest 0.1 g. Fish samples were then placed on a clean surface and 1 g wet weight of the fish tissue (muscle) along the lateral line was taken. The fish was dissected, the gut removed, and the liver extracted while still very fresh. After dissection, all the samples were labelled by species. The extracted liver and muscle portions were wrapped in foil paper, labelled, and oven dried at a temperature of 105°C for 1 h. The dried samples were reduced to powder with a plastic mortar and pestle, sieved to obtain a uniform particle size, and preserved in well-labelled containers. The digestion procedure complied with the American Standard Methods for the Examination of Water and Waste (APHA, 1998).

Bioaccumulation factor (BAF)

The bioaccumulation factor (BAF) for heavy metals in fish is expressed below (Latif et al., 1982)

Assessment of the human health risk of fish consumption

The models provided by the United States Environmental Protection Agency (USEPA, 2012) were used in determining the human health risk and they are the Estimated Daily Intake (EDI), Target Hazard Quotient (THQ), and Hazard Index (HI).

where MIf = mass of fish ingested per day; CM_f = concentration of metal in fish, and BW = body weight (60 kg for adult). In Nigeria, the per capita consumption of fish and shellfish for human food is 9.0 kg, which is equivalent to 24.7 g per day. (USEPA, 2012; Duoye, Michael, 2015).

where THQ = Target Hazard Quotient, EF = Exposure Frequency (365 days/year); ED = Exposure Duration (52.62 years), which corresponded to average life expectancy of a Nigerian; (CIA, 2017); AT = average exposure time for non-carcinogens (365 days/year × ED). The Oral Reference Dose (ORD) is an estimate of daily exposure to human population (including the sensitive subgroup) that is likely to be without an appreciable risk of the deleterious effect during a lifetime. The Oral Reference Dose (ORD) (mg/kg/day) used are Ni – 2.0 × 10–2, Zn – 3.0 × 10–1, Pb – 3.5 × 10–3, Fe – 7.0 × 10– 1, and Cr – 1.5 × 10–3 (USEPA, 2012).

The hazard index (HI) from the consumption of Clarias gariepinus and Parachanna obscura obtained from Owan River, Edo state, was calculated as the sum of THQs of all the metals in the fish samples and was expressed as follows;

HI = THQPb + THQCr + THQZn + THQFe + THQNi

where HI = hazard index; THQPb = the Target Hazard Quotient for Pb intake; THQCu = the Target Hazard Quotient for Cu intake, THQZn = the Target Hazard Quotient for Zn intake; THQFe = the Target Hazard Quotient for Fe intake, and THQNi = the Target Hazard Quotient for Ni intake.

Data analysis

The data obtained was analysed using the computer software SPSS (statistical package for social sciences) v.22. Basic statistical measurement of the central tendency and the t-test were used in the comparison between the heavy metal levels in the fish.

RESULTS

Table 1 shows the mean of physical and chemical parameters of the Owan River between July and October 2017. The mean levels of Ni, Zn, Pb, Fe, and Cr in the liver and muscle of C. gariepinus were 0.25, 0.57, 0.02, 2.18, 0.48, and 0.15, 0.15, 0.07, 1.60 and 0.62, respectively, while P. obscura recorded mean concentrations of 0.34, 0.72, 0.28, 5.67, 0.66 for the liver and 0.27, 0.38, 0.18, 3.13, and 0.57 for the muscle (Table 2). Significant differences (p < 0.05) were observed between the levels of Zn in the liver and muscle of C. gariepinus and between the lead concentration in the liver and muscle of P. obscura (Tables 2 and 3). The order of heavy metal accumulation observed in the liver and muscle of C. gariepinus of the Owan River was Fe > Zn > Cr > Ni > Pb and Fe > Cr > Ni > Zn > Pb, respectively, while the same order of Fe > Cr > Zn > Ni > Pb was observed for both the liver and muscle of P. obscura in the Owan River. Iron consistently had a higher concentration in both fishes studied.

Table 1. Summary of physical and chemical parameters of the Owan River between July and October 2017

Bioaccumulation factor of fishes

Table 4 shows bioaccumulation factors of heavy metals in C. gariepinus and P. obscura. All heavy metals analysed in both C. gariepinus and P. obsura revealed bioaccumulation factors greater than one (1) except for chromium and lead in C. gariepinus, and Cr in P. obscura.

Health risk assessment of fishes

The Estimated Daily Intake for Clarias gariepinus was in the order Fe > Cr > Ni = Zn > Pb, while the THQ was Cr > Pb > Ni > Fe = Zn with risk values of 0.015, 0.004, 0.001, 0.000 and 0.000, respectively (Tables 5 and 6). The hazard index was 0.021. For Parachanna obscura, the EDI was in the order: Fe > Cr > Zn > Ni > Pb, while the Target Hazard Quotient in the descending order was Cr > Pb > Ni > Fe > Zn with risk values of 0.014, 0.010, 0.002, 0.001 and 0.000, respectively. The hazard index (HI) of heavy metals in this fish was 0.027. In both fishes, chromium had the highest percentage contribution to the HI.

Table 2. Comparison of heavy metal concentrations in the liver and muscle of Clarias gariepinus

Table 3. Comparison of heavy metal concentrations in the liver and muscle of Parachanna obscura

Table 4. Bioaccumulation factors of C. gariepinus and P. obscura from Owan River

Table 5. Assessment of the health risk of consumption of Clarias gariepinus from the Owan River

Table 6. Assessment of the health risk of consumption of Parachanna obscura from the Owan River

DISCUSSION

Bioaccumulation of metals in fish is considered an index of metal pollution in the aquatic bodies that can be a useful tool to study the biological role of metals present at higher concentrations in fish (Tawari-Fufeyin, Ekaye, 2007; Osman, Kloas, 2010).

Heavy metal concentrations were observed to be higher in fish than in water, which was indicative of bioaccumulation. Fish has the ability to concentrate heavy metals in their tissues to the concentration levels which comprise of several orders of magnitude higher than those in water (Oguzie, 2003). The difference in the levels of accumulation in different organs of a fish can be attributed to the differences in the physiological role of each organ. Other factors such as regulatory ability, behaviour and feeding habits may play a significant role in the differences of accumulation in these organs (Kehinde et al., 2016). Also, the chemical nature of the metals, the ionic strength, and pH tend to be a master variable in the accumulation process (Eneji et al., 2011).

C. gariepinus and P. obscura were revealed to have accumulated heavy metals in their liver and muscle. The ranges of Ni levels (0.12–0.61 mg/kg) in P. obscura are similar to the values recorded by Obasohan (2007) for P. obscura, however, this was lower than the 1.28 mg/kg reported for C. gariepinus (Adewumi et al., 2014). The mean concentration of zinc in the muscle of C. garipeinus (0.15 mg/kg) is similar to the mean recorded by Ayeloja et al. (2014) for C. gariepinus. In contrast, Adewumi et al. (2014) reported a higher mean concentration for C. gariepinus. Sublethal levels of zinc in C. gariepinus have been known to adversely affect hatchability, survival, and haematological parameters of the fish (Cardeihac et al., 1981; Kori-Siakpere, Ubogu, 2008).

Mean lead ranges of 0.02 mg/kg and 0.07 mg/kg were observed for the liver and muscle of C. gariepinus, while the levels in P. obscura were 0.28 mg/kg and 0.18 mg/kg for liver and muscle, respectively. Similar levels of accumulation were reported by Anim et al. (2011) for P. obscura and Ayeloja et al. (2014) for C. gariepinus; Obasohan (2007), on the contrary, reported higher values in P. obscura.

The total mean accumulation of iron (1.89 mg/kg and 4.40 mg/kg) in C. gariepinus and P. obscura were lower than values reported by Anim et al. (2011), but higher than the mean value for C. gariepinus by Edward et al. (2013). The dominance of iron over other metals observed in this study is consistent with findings of Oronsaye et al., 2010; Akan et al., 2012; Edward et al., 2013; Ekpo et al., 2013; Nsofor, Ikpeze, 2014, and Omoregie et al., 2016. This may be explained by the fact that iron being the most abundant metal in the environment could conceivably be bioaccumulated more than other trace metals (Oronsaye et al., 2010). It has been reported that iron occurs at high concentrations in Nigerian soils (Asaolu, Olaofe, 2004). Furthermore, iron is the major respiratory pigment in the blood and is thus present in abundance in the circulatory system (Oronsaye et al., 2010).

Chromium is an essential trace metal and the biologically usable form of Cr plays an essential role in glucose metabolism (Kehinde et al., 2016). Mean concentrations of 0.48 mg/kg (liver) and 0.62 mg/kg (muscle) for C. gariepinus, and 0.66 mg/kg (liver) and 0.57 mg/kg (muscle) for P. obscura have similarly been reported by Aghoghovwia et al. (2016) for the liver and muscle of P. obscura. Obasohan (2007) and Omoregie et al. (2016) reported higher Cr ranges for P. obscura and C. gariepinus.

The observed bioaccumulation factors in this study suggest that C. gariepinus and P. obscura are contaminated with these heavy metals. Bioaccumulation of metals in various organs of fish may cause structural lesions and functional disturbances (Jezierska, Witeska, 2006) thus affecting physiological functions in the fish and portending serious dangers to humans who consume these fishes.

The hazard index via the consumption of C. gariepinus and P. obscura were 0.021 and 0.027, respectively. Since the HI is less than one (1), it can be inferred that the consumption of these fishes is unlikely to pose any health risks to consumers hence allaying fears of heavy metal induced toxicities. Bearing in mind the tendency of bioaccumulation of heavy metals in fish and their non-degradability in human systems, it becomes imperative to continuously monitor heavy metal levels to ascertain the risks they pose to humans.

ACKNOWLEDGEMENTS

The authors are grateful to the Benin Owena River Basin Laboratory and Department of Chemistry laboratory for doctoral studies, University of Benin, for providing equipment and assistance in the analysis of the samples.

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* Corresponding author. Email: obohij@yahoo.com

Ijeoma Patience Oboh, Benjamin Chima Okpara

SUNKIŲJŲ METALŲ BIOAKUMULIACIJA IR CLARIAS GARIEPINUS BEI PARACHANNA OBSCURA IŠ OWANO UPĖS (EDO VALSTIJA, NIGERIJA) VARTOJIMO RIZIKOS SVEIKATAI ĮVERTINIMAS