Carcinogenic and Non-carcinogenic Risks of Heavy Metals in Clarias gariepinus (African Catfish) Obtained from Bariga Section of Lagos Lagoon, Nigeria

The Bariga section of Lagos lagoon is famous in Lagos for fishing activities. However, the safety of edible fishes sold in the place has not been evaluated for a long time. This study determined the safety of Clarias gariepinus (African catfish), which is the most frequently patronized fish species in the area. Samples of the fish and soil sediments obtained during rainy and dry seasons were subjected to atomic absorption spectroscopy to determine the levels of cadmium (Cd), lead (Pb), zinc (Zn), copper (Cu), and manganese (Mn). Afterward, the daily intake (DI), target hazard quotient (THQ), hazard index (HI), and carcinogenic risks (CR) of the heavy metals were calculated. The results showed that the levels of Cd and Pb in the fish and soil sediments were above the world health organization (WHO) permissible limits, while Zn, Cu, and Mn were normal. The DI of the heavy metals, as well as the THQ and HI, were normal. However, the CR of Cd and Pb were above the recommended limits. The heads of the fishes contained the highest concentrations of the heavy metals, DI, THQ, HI, and CR. Among the heavy metals, Cd had the highest CR. There was no significant (p > 0.05) seasonal variation in the accumulations of the heavy metals in the soil sediments. Overall, the results showed that the fish may predispose consumers to health hazards. Consequently, there is a need for heavy metal pollution control in the lagoon, to safeguard the health of fish consumers. doi: 10.5829/ijee.2021.12.01.08


INTRODUCTION 1
Heavy metal pollution of the aquatic ecosystem is increasingly linked to health and environmental hazards due to increasing applications of the metals in societies. Heavy metals are loosely described as toxic metals with a specific density of 5 g/cm 3 and above [1]. Among heavy metals, lead (Pb), chromium (Cr), nickel (Ni), zinc (Zn), cadmium (Cd), cobalt (Co), titanium (Ti), and iron (Fe) cause more damage to aquatic organisms due to their high bioaccumulative property in water [2]. Heavy metals in an aquatic ecosystem can build up in the food chain and predispose humans to various diseases. Heavy metals can also compromise the nutritional quality of fish, particularly its healthy protein, fats, and cholesterol [2][3][4].
*Corresponding Author Email: yahayatajudeen@gmail.com (T . O. Yahaya) However, at minute quantities, some of these heavy metals functionally maintain biochemical and physiological processes in living organisms. Sources of heavy metals in aquatic ecosystems are mining operations as well as waste discharges from homes, industries, and farms [5].
In aquatic habitats, fish are more affected by pollution than any organism. This is because fish occupy the top trophic level and so can accumulate enormous quantities of pollutants in their bodies. Thus, most of the times, fish are the causes of health hazards in aquatic habitats and so fish are often used to assess the health status of aquatic environments [6,7]. Bioaccumulation of heavy metals in fish depends on several factors such as age, size, feeding habits, and body physiology. Other factors include the level and bioavailability of metals, physicochemical properties of water, among others. The accumulation of heavy metals in various tissues of fish depends on the structure and function of the tissues [5]. Generally , metabolically active tissues such as gills, liver, and kidneys accumulate more heavy metals than other tissues such as skin and muscles [5]. All these put together show that fish are sensitive to xenobiotics and that evaluation of heavy metal levels in fishes is important for the health of humans and aquatic environments.
Lagos lagoon in Nigeria contains several species of fish which were classified into three main ecological groups, namely the marine fishes, freshwater fishes, and euryhaline fishes [8]. The marine fishes use the lagoon for breeding and comprise thirty-one species, while the freshwater fishes dominate the lagoon during the low salinity periods and consist of seventeen species. The euryhaline fishes include twenty-four species and are found in the lagoon all-year-round. These fishes are consumed by the inhabitants and also provide income to fishermen. Unfortunately, studies conducted by Oguguah et al. [9] showed that, over the years, the Lagos lagoon has been contaminated by industrial and domestic pollutants. These pollutants might have caused serious health hazards in the fish and other aquatic organisms in the lagoon, which may pose public health hazards through the consumption of such fishes. Hence, there is a need for periodic evaluation of heavy metals in edible fish species inhabiting the Lagos lagoon. From literature, there is a dearth of such studies on the fishes inhabiting the Barig a section of the lagoon, wherein intense fishing activities and sales take place daily. Among several fish species, African catfish (Clarias gariepinus) is the most frequently consumed and sold fish in the area, possibly due to its taste and fleshy body. Therefore, this study evaluated the carcinogenic and non-carcinogenic risks of heavy metals in Clarias gariepinus inhabiting the Barig a section of Lagos lagoon.

Description of the study site
This study was carried out at the Bariga section of Lagos lagoon in Lagos, Southwest Nigeria. Lagos is the capital of Lagos State, on latitude 6°37ʹN and 6°70ʹN and longitude 2°70ʹE and 4°35ʹE. The state is bordered by the Republic of Benin on the west, Ogun State on the east and north, and the Atlantic Ocean on the south [10]. The city is one of the fastest-growing urban settlements in the world and is the economic hub of Africa. Lagos is the most industrialized city in Nigeria, which, coupled with its high population density, is responsible for high waste generation and environmental pollution in the city. The vegetation of the state is mainly tropic with several water bodies including the lagoon, rivers, and creeks. The climate of the state consists of a long rainy season and a short dry season.
The Lagos lagoon is a continuation of lagoons and creeks that stretches for about 257 km from Cotonou in the Republic of Benin to Niger-Delta in Nigeria. The lagoon borders the forest belt and receives water fro m numerous big rivers [11]. It also receives wastes fro m homes, industries, and farms as well as automobile exhausts and leftovers of other anthropogenic activities. It empties into the Atlantic Ocean at Lagos and Cotonou. The Bariga section of Lagos lagoon (the study site) has GPS coordinates of 6° 31ʹ29"E and 3° 23ʹ58"N in Shomolu Local Government Area. It is a highly commercialized environment known for its fishing activities and sales. The residents of Bariga and many other places in Lagos and environs patronize the site for fish for consumption and sales. This necessitates periodic monitoring of heavy metals in the fish, to prevent or reduce unintended health hazards.

Sample collection and preparation
Sixty (60) samples of adult Clarias gariepinus with a mean weight of 163.17±3.01 g and a mean length of 27.56±2.01 cm were purchased from Bariga section of Lagos lagoon between January and June 2020 (spanning dry and rainy seasons). The fish were transported to the laboratory in a well-ventilated container, containing the same water obtained from the site where the fishes were caught.
During the period mentioned above, sixty soil samples were also obtained randomly within the top 30 cm of the lagoon sediments into clean and pre-sterilized polyethylene bags. The samples were air-dried at room temperature (28 °C) for 8 days, and later oven-dried until constant weights were attained. The samples were then ground with a mortar and pestle, sieved with a 2-mm mesh sieve, and homogenized [12]. The products obtained were stored in a desiccator before further analyses.

Heavy metal analysis
The levels of Pb, Cd, Zn, Mn, and Cu in the fish and soil sediments were determined using atomic absorption spectroscopy (AAS) as described by Yahaya et al. [13]. The samples were digested by adding 10 ml of HNO3 to 1 g of each fish and soil sample and the mixture was heated on a heat block. The heating was done gradually, starting from 100 °C to between 250 and 300 °C. The digestion was completed in about 72-83 minutes, indicated by the appearance of white fumes. The mixt u re was left to cool and then transferred to 50 ml volumetric flasks and distilled water was added to increase the mixture to the 50 ml mark. The solution was transferred to plastic bottles, labeled accurately, and subjected to atomic absorption spectroscopy using a spectrophotometer (UNIAM model 969).

Quality assurance and control
The glassware and plastic materials used for the heavy metal analysis were washed with a detergent solution and rinsed with deionized water. About 10% HNO3 was then poured into the materials to sterilize them, after which they were rinsed with deionized water again.
Background contamination of the fish and soil samples was checked to ensure the accuracy of the data. Blank samples were analyzed after five samples and all analyses were replicated three times. The reproducibility of the values was found to be at the 95% confidence level. Therefore, the mean value of each heavy metal was used for further analysis. All the chemicals used for the analysis were of high analytical grade.

Health risk assessment
The carcinogenic and non-carcinogenic risks of the heavy metals in the fish samples were used to assess the health risks of daily consumption of the fish. The noncarcinogenic risks were calculated from the daily intake (DI), target hazard quotient (THQ), and hazard index (HI) of the heavy metals as given in equations 1, 2, and 3, respectively [14,15]. The carcinogenic risks (CR) were calculated using Equation 4 [16].
HI=∑ of all heavy metals In equations 1, 2, and 3, according to Miri [17], ED (exposure duration) is 54.5 years, which is equivalent to the average life span of Nigerians. EF (exposure frequency) is 365 days/year. CF (conversion factor) is 0.208, to convert the dry weight of fish to wet. ABW (average body weight) is 60.7 kg, which is equivalent to the average body weight of adult Nigerians. FIR (fish ingestion rate) is 0.02 g/day. C (concentration) is the concentrations of the heavy metals in the fish tissues. AT (average time) is 365 x ED. RFD (reference dose) of the heavy metals in fish are 0.0035 for Pb, 0.04 for Cd, 0.07 for Cu, 0.14 for Mn, and 0.3 for Zn [17]. THQ and HI values below 1 were considered normal [17].
CSF is the cancer slope factor, which is 0.38 and 0.0085 for Cd and Pb, respectively [16]. CR values greater than 10 -6 were considered abnormal [18].

Data analysis
The data obtained from the fish and soil samples were subjected to mean and standard deviation (SD). The Student's t-test was used to compare the differences between the heavy metals accumulated in the soil sediments in the rainy and dry seasons. The histogram was drawn using the Minitab software version 7.0.

Levels of heavy metals in the fish samples
Lead and Cd were detected in the heads, trunks, and tails of the fish above the world health organization (WHO) permissible limits, while Zn, Cu, and Mn were normal (  [18]. This could be due to the natural abundance of Zn in Nigerian environments, of which the aquatic environment is a major depository [18]. In a study by Ogundele et al. [24], the concentrations of Zn in tested soil samples ranged from 30.8-219.23 mg/kg. Abnormal concentrations of Pb and Cd detected in this study could have resulted from domestic and industrial sewage and acid batteries [5]. It could have also emanated from fertilizers used on the farms around the lagoon as well as oil leaks from ferries and boats. The high concentrations of the heavy metals in the head of the fish compared to the trunk and tail were also reported by Olowu et al. [18] and Olubunmi et al. [26]. Fish heads contain gills, a biologically active organ that requires constant water, which may be laden with heavy metals, hence increased concentrations of heavy metals in the head [5]. Additionally, water, which could be laden with heavy metals, is often egested through the mouth and gills [18]. The detection of the heavy metals in the fish samples suggests that Clarias gariepinus inhabiting the Barig a section of Lagos lagoon may predispose consumers to health risks. Cadmium and Pb, which were detected above the permissible limits, are particularly worrisome. Furthermore, the heads, which contained the highest concentrations of the heavy metals, were at an increased risk for heavy metal toxicities. Cadmium has been implicated in the kidney, respiratory and skeletal diseases [27]. Lead exposure may cause kidney and brain problems, as well as anemia, weakness, infertilit y , pregnancy loss, stillbirths, and fetal developmental errors [28]. Though Zn, Cu, and Mn were detected within the permissible limits, in strict terms, there are no safe levels for heavy metals. Prolonged exposure to high concentrations of Zn, in particular, may induce apoptosis, especially in the brain [29].

Non-carcinogenic risks of the heavy metals
The DI of Cd, Pb, Zn, Mn, and Cu through the consumption of the fish was within the recommended dietary daily intakes (RDI) ( Table 2). Zinc was the most ingested, while Cu was the least ingested. The highest ingestion of Cd was from the trunk, while the highest ingestion of Pb, Zn and Cu were from the head. The ingestion of Cu was jointly highest in the head and trunk. Collectively, these showed that the DI of the heavy metals by the consumers came mostly from the head. The THQ and HI of the heavy metals were less than 1, the upper limit within which a substance could be considered safe for consumption. In the head, Cu had the highest THQ, while in the trunk and tail, Zn had the highest, indicating that Zn had the highest THQ of all the heavy metals and thus posed more non-carcinogenic risks. The HI of the heavy metals was the highest in the head, followed by trunk and tail, suggesting that the heads posed more noncarcinogenic risks.
The normality of the DI, THQ, and HI of the heavy metals suggest that the fish may not pose any serious noncarcinogenic risk. However, since the estimation was based on the average life span of Nigerians, people that live above this age may be at an increased risk. Furthermore, the heavy metals that were not investigated in this study may add to the non-carcinogenic risks and become significant. The results of the current study agree with Oguguah et al. [9], Bawa-Allah et al. [30] and Bassey and Chukwu [31], all of them who reported no non-carcinogenic health risk of heavy metals in fishes collected from different sections of the Lagoon. From the literature survey, no study reported dissenting findings.

Carcinogenic risks of the heavy metals
The CR of Cd in the head, trunk, and tail, as well as Pb in the head and trunk of the fishes, was greater than the permissible limit of 10 -6 (Table 4). Zinc, Mn and Cu have no cancer slope factor (CSF) and thus have no CR (Table  4). In other words, Zn, Mn, and Cu are non-carcinogenic. On average, the CR of the heavy metals is the highest in the head, followed by the trunk and tail. These imply that the head of the fish posed more cancer risk than the trunk and tail, respectively. Moreover, Cd posed the highest cancer risk, followed by Pb. Both Cd and Pb may induce    [34]. Cadmium may also damage the DNA by generating free radicals, inducing oxidative stress [35]. Additionally, Cd may induce cell proliferation as well as inhibit apoptosis and DNA repair [36]. Regarding Pb, it can replace Zn in many proteins that modulate transcription. It may also produce free radicals and damage the DNA through  Figure 1 shows the seasonal variations in the levels of Cd, Pb, Zn, Mn, and Cu in the soil sediments of the Barig a section of Lagos lagoon. Except Pb, the levels of the heavy metals were higher during the rainy season than the dry season (p > 0.05). The levels of Pb and Cd in the soil sediments were above the WHO permissible limits, while Zn, Cu, and Mn were normal. These findings are consistent with the results obtained by Okoye et al. [38] who detected higher levels of some heavy metals during the rainy season than the dry season in a certain section of Lagos lagoon. The mentioned findings are also in line with Adeyemo et al. [39] who reported higher concentrations of heavy metals during the rainy season than the dry season in the soil sediments of the Lekki-Epe section of the Lagos lagoon. Moreover, Bassey et al. [40] reported abnormal concentrations of Cd, Pb, and Zn in Ologe and Badagary sections of the Lagos lagoon. However, the findings of the current study contradict Akinjogunla and Lawal-Are [41] who reported higher concentrations of heavy metals during the dry season than the rainy season in the soil sediments of Ebute-Oko , Tomaro, and Agala sections of the Lagos lagoon. The higher concentrations of heavy metals in the soil sediments during the rainy season could be due to increased urban runoff. It could also be attributed to the influx of freshwater during the rainy seasons.

CONCLUSION
The results established that the fishes bioaccumulated non-permissible concentrations of Cd and Pb as well as permissible levels of Zn, Cu, and Mn. Thus, the fishes may pose some health threats to consumers, particularly Cd and Pb toxicity-related diseases. However, the DI, THQ, and HI of these metals were within the permissible limits, suggesting that daily consumption of the fishes may not pose any serious non-carcinogenic health hazards. The heads of the fishes had the highest concentrations of heavy metals as well as the highest DI, THQ, and HI, which indicate that the head may pose more health risk than the trunk and tail, respectively. The CR of Pb and Cd in the fishes were above the allowable limits, indicating that daily consumption of the fishes may predispose consumers to cancers. Among the heavy metals, Cd had the highest CR, thus it may pose the highest cancer risk. Also, the heads of the fishes had the highest CR, which suggests that it poses more cancer risk than trunk and tail, respectively. Collectively, these findings call for close monitoring of heavy metals in Clarias gariepinus inhabiting the Bariga section of Lagos lagoon, to safeguard the health of consumers. While we call for more studies to ascertain our claims, agencies in charge of the environment and public health in Lagos State are advised to work towards reducing pollution of Lagos lagoon.