Health risk assessment of organochlorine pesticide residues in freshwater fish in Ibadan, Nigeria
Article information
Abstract
This work was aimed at assessing the potential human health risk of organochlorine pesticides (OCPs) due to consumption of five different species of fish from Dandaru River and Eleyele Lake in Ibadan, Nigeria. Five OCPs (aldrin, beta-lindane, beta-endosulfan, endosulfan ether and heptachlor epoxide) were investigated. Extraction was carried out by a quick, easy, cheap, effective, rugged, and safe (QuEChERS) procedure; extract was cleaned-up using solid phase extraction while instrumental analysis was performed by gas chromatography-mass spectrometry. Health risk assessment (non-carcinogenic and carcinogenic) to adult, children and infants was carried out using standard models and indices. Target OCPs were measured up to 0.013 mg/kg for heptachlor epoxide in Oreochromis niloticus from Dandaru River. Lowest concentrations for most of the OCPs were determined in Clarias gariepinus from Eleyele River. Hazard indices (HI) indicate that non-carcinogenic risk to adult and children was not apparent by consuming all investigated fish species from Dandaru River and Eleyele Lake. However, a high non-carcinogenic risk to infants was expected by consuming Oreochromis niloticus and Oreochromis lidole from Eleyele Lake as well as all investigated fish species (except Oreochromis aureas) from Dandaru River, apparently due to the contribution of heptachlor epoxide. Although carcinogenic risk was not expected in adult due to consumption of all investigated fish species from both Eleyele Lake and Dandaru River, consumption of Oreochromis niloticus from Eleyele Lake by infants and children, Oreochromis lidole from Eleyele Lake by infants, as well as all investigated fish species (except Oreochromis aureas) from Dandaru River by infants poses possible carcinogenic effects. Regular health risk assessment of target OCPs for the investigated fish species from the two water bodies is necessary to safeguard the safety and health of consumers, especially infants.
Introduction
Pesticides are extensively used worldwide in agriculture to ensure high crop production [1]. Pesticides are also commonly employed prior to crop harvesting to guard against crop contamination before product is made available for sale in the market [2].Aquatic food resources, fisheries, and aquaculture have all been repeatedly threatened by the pollution of water systems worldwide due to the presence of pesticide residues. The dispersion of residues from agricultural chemicals, including pesticides, in the surrounding environment can significantly contaminate land-based ecosystems and taint human foods [3].
The issue of pesticide residues contamination in fish is a matter of serious concern [4]. Fish can be considered as one of the most significant bioindicators in fresh water systems for the estimation of pesticides pollution level [5, 6]. The gills of fish come into direct contact with water, making them particularly susceptible to the presence of pesticide residues in aquatic environments. As a result, the concentration of pesticides found in fish may reflect the concentration of these chemicals in the water where the fish reside [7]. In certain circumstances, chemicals that have accumulated in the silt and bottom sediments of water bodies can migrate back into the water, potentially leading to increased pesticide concentrations in the aquatic environment. This migration process can further contribute to the contamination of fish and other organisms in the ecosystems.
Organochlorine pesticides (OCPs) are a class of pesticides which have been used historically due to their high efficiency and cost-effectiveness [8]. The entry of the majority of OCPs into the ecosystem occurs through runoff from agricultural fields, improper disposal of waste, and the by-products generated from chlorine combustion processes [9]. OCPs are environmentally persistent, even for extended periods in soils and sediments, and also accumulate in non-human organisms [10–12]. These pesticides have profound toxic effects on populations, leading to devastating consequences [13]. Exceptionally elevated concentrations of OCPs residues have been identified worldwide in diverse matrices, encompassing organisms, sediments, soils, water, and food products [14-17]. In the Stockholm Convention, OCPs were considered among the original 12 persistent organic pollutants (POPs) [18] and are known for a range of properties including toxicity, long-distance transport, environmental persistence, and bioaccumulation within the food chain. Consequently, OCPs are considered a threat to both human health and the environment [18, 19].
The improper use and persistence of OCPs continue to pose significant environmental and public health concerns. Despite their potential to cause chronic health effect such as malignant tumours, endocrine disruption, and neurological disorders [20] there are limited published work on the potential health risk of OCPs in different species of fish from Nigerian rivers and lakes, especially the Dandaru River and Eleyele Lake in Ibadan. These water bodies (Dandaru River and Eleyele Lake) are critical for commercial fishing in Ibadan, yet their proximity to intensive farming practices raises concerns about pesticide runoff and subsequent contamination of fish populations, which are widely consumed. Moreover, fishermen’s inappropriate use of OCPs for fishing and the introduction of pesticide-contaminated agricultural products into fish feeds increase the risk of bioaccumulation. OCPs exposure through contaminated water of the water bodies can have serious health implications for humans and animals. Since fish serves as a bioindicator of freshwater pollution, this study was aimed at addressing the paucity of data on potential OCPs contamination of different fish species from Dandaru River and Eleyele Lake in Ibadan, Nigeria and evaluation of the potential human health risks posed by consuming the fish from these water bodies.
The objective of this study, therefore, was to investigate the human health risk (non-carcinogenic and carcinogenic) of selected OCPs in commonly consumed fish species found in Dandaru River and Eleyele Lake in Ibadan, Nigeria to adult, children and infants. Five fish species Oreochromis niloticus (Nile Tilapia), Oreochromis aureus (Blue Tilapia), Oreochromis mossambicus (Mozambique Tilapia), Oreochromis lidole (Chambo Tilapia) and Clarias gariepinus (African sharptooth catfish) were collected and analysed for five OCPs (aldrin, beta-endosulfan, beta-lindane, endosulfan ether and heptachlor epoxide). The findings provide insights to inform better regulation, monitoring, and safe pesticides use while ensuring food safety and public health.
Materials and Methods
Chemicals and Reagents
Analytical standards of beta lindane, endosulfan ether, aldrin, heptachlor epoxide and beta endosulfan as well as acetonitrile HPLC grade were obtained from Scharlau (Barcelona, Spain). Liquid chromatography grade of n-hexane was obtained from Merck KGaA (Darmstadt, Germany). SPE cartridges (Bond Elut C18, 200 mg/3mL) were from Agilent. Sodium chloride salt (NaCl) and anhydrous sodium sulphate were purchased from Fisher Scientific (United Kingdom).
Description of the study areas
Eleyele Lake is situated upstream on River Ona in the city of Ibadan within geographical coordinates: Latitudes between 7025′ and 7026′N and longitudes between 3051′ and 3052′ E [21]. Eleyele Lake is man-made and was formed in 1939 [22] by damming River Ona, which is part of a dense network of inland watercourses that flows southward into Lagos Lagoon [23].
It falls within the North West LGA of the Ibadan, Oyo State Nigeria. It is bounded by Eleyele urbanisation in the south, the areas of Apete in the east, Awotan in the north and Ologuneru in the north-west. Surrounded by the lake is a variable margin of woodland beyond which is urban development on all sides of the lake. The catchment area of Eleyele Lake and Dandaru River is characterized by dry and wet seasons and the mean annual rainfall and mean annual temperature are 1250 mm and 27ºC, respectively [24]. Eleyele Lake has a dendritic drainage system and the region is on top of sandy clay and worn crystalline rocks, according to geophysical data gathered using vertical electronic sounding [24]. Eleyele Lake is a key resource for fishery, domestic water supply and flood control; the lake is fast being degraded due to various anthropogenic activities around its catchments [25, 26]. Domestic farming was prevalent near the lake, and there is a solid waste dumpsite which receives wastes from the nearby residence. The Dandaru River is situated in the city of Ibadan within geographical coordinates: Latitude 7024′N and longitudes 3054′ E. The river was selected for this study due to the intensive farming activities around its catchments. Dandaru River, located close to the University College Hospital (UCH), Ibadan flows through the Agodi gardens [27]. The river was formerly used majorly by fishermen but now seriously impaired by anthropogenic activities. Wastewater discharges from the University College Hospital (UCH), Ibadan and domestic wastes from other sources are released into the river. The map showing the sampling locations in this study is shown in Figure 1 while Table 1 shows the description of fish species in this study.
Map showing the sampling locations.
Description of fish species collected from Dandaru River and Eleyele Lake.
Sample collection, preservation and pre-treatment
The fish species were chosen based on their prominent availability in the river and lake under study, common food fish species as a preferable source of protein and commercial importance in the community [23]. A total of five different fish species were collected (five species were collected from Dandaru River and four species from Eleyele Lake) during January 2023. Thirty samples of five different fish species were collected from Dandaru River. Six samples were collected for each of the species and composited to form one sample, making five samples altogether from Dandaru River. Five samples were collected for each of the four species collected from Eleyele Lake, making a total of twenty samples. Five samples of each of the species were composited to form one sample, making four samples altogether from Eleyele Lake. All fish samples were collected using gillnets. Different species with variable size and weight were collected. All the samples were wrapped in aluminum foil and samples were transported to the laboratory in hermetically sealed coolers, fish samples were properly washed and characterized by a fish taxonomist on the basis of morphometric characteristics. The samples were frozen until chemical analysis. Sample extraction was carried out within 48 hours of sampling.
Sample extraction and clean-up
In the laboratory, fishes were thawed at room temperature before dissection. Fish samples were dissected to separate the muscle. The collected fish samples was chopped and blended separately in an electric blender with microcutters to obtain an isolated homogenous composite of fish samples. Extraction was carried out using the quick, easy, cheap, effective, rugged, and safe (QuEChERS) procedure by Anastassiades et al. [28] with slight modifications. Briefly,5 g homogenized sample was weighed into a 50 mL centrifuge tube, and 10 mL of acetonitrile was added. The mixture was vortex-mixed for one minute followed by the addition of 4 g of activated anhydrous sodium sulphate and 1 g of sodium chloride to get rid of the water in the samples. The sample was shaken vigorously with an electric shaker and afterwards was centrifuged at 5000 rpm for 5 min. The supernatant was decanted and filtered for clean-up. The filtered supernatant was passed through solid phase extraction using a C18 cartridge. Analytes were eluted with 1 mL n-hexane into a glass vial for gas chromatography-mass spectrometry(GC-MS) analysis.
Instrumental analysis
The extracts were analysed for the target OCPs using a gas chromatograph coupled with mass spectrophotometer detector. Separation of OCPs residues was achieved by the injection of about 1.0 μL of the clean extracts into the GC-MS (Agilent technologies,GC-MS-5975.USA) using a HP5-MS capillary column of length 30 m, internal diameter of 0.32 mm and film thickness of 0.25 mm. The scan range was between 50 to 500, and the following operating conditions were used: injector temperature of 250°C; detector temperature of 250°C; the oven temperature was at 60°Cinitially for 0.5min and increased to 140°C at 20°C/min and to the final temperature of 280°C at 11°C/min to give a total run time of 23 minutes. The carrier gas used for the mobile phase was helium and the flow rate was 2 mL/min. Acquisition MS mode used was selected ion monitoring (SIM) mode; ion source temperature of 200°C and interface temperature of 250°C were used. Detection of each analyte was achieved from the identification of their respective retention time. The peak area was used to calculate the concentrations of the analytes.
Quality Assurance
The column of the gas chromatograph was baked at 250℃ for 2hours. Blank reagent (solvent) was run to establish the absence or presence of target OCPs. In order to maintain the quality of analytical results method blank samples and standard solutions were analysed after every run of five samples. The reference standards of the pesticide compounds were used for calibration. A 5-point calibration curve was established for each analyte of interest. The linearity of the instrument response was established by analysing series of standard solutions at different concentrations and coefficient of determination was greater than 0.9880 for each of the compounds, indicating good linearity. The limit of detection (LOD) and limit of quantification (LOQ) were determined as the concentrations corresponding to signal-to-noise ratio of 3 and 10, respectively. LOD for each of the target OCPs was 5.2 x 10-5 mg /kg while LOQ for each of the compounds was 1.56 x 10-4 mg/kg.
Human health risk assessment
Human health risk through dietary consumption of fish was carried out using standard human health risk models [29]. The assessment was carried out for adult (70 kg), children (30 kg) and infants (10 kg) populations for both non-carcinogenic and carcinogenic health risks. The estimated daily intake, hazard quotient (HQ) and hazard index (HI) were used to assess the risk of human exposure through fish consumption. The description and values of parameters used for the various estimations are presented in Table 2. The estimated daily intakes (EDI) (mg/kg/day) of OCPs in the fish samples were estimated using Equation 1according to Ogbeide et al. [11], while non-carcinogenic and carcinogenic health risks were assessed using standard models and indices [29] according to equations 2 to 5.
Reference dose and oral slope factors of target OCPs.
where EDI is Estimated Daily Intake, C= mean concentration of OCPs in fish (mg/kg), IRF= fish ingestion rate (kg/capita/day), BW= body weight, RfD= Reference Dose (mg/kg/day), SF= Oral Slope Factor (mg/kg/day)-1. While HQ is the hazard quotient of individual pesticide, HI stands for hazard index which is the summation of HQ values for all pesticides measured in the fish sample. CR represents carcinogenic risk of individual OCP while TCR denotes total (cumulative) carcinogenic risk of the OCPs.
Table 2 shows the values of RfD and SF used in this study. The per capita consumption of fishes in Nigeria reported as 8 kg/year [30], equivalent to ingestion rate of 0.02 kg/day, was used. Body weights of 70 kg, 30 kg and 10 kg were used for adult, children and infant populations, respectively.
Results and Discussion
Concentration levels of target OCPs in fish species from Eleyele Lake and Dandaru River
Pesticide residues that accumulate in the aquatic environment can be transferred to humans through the consumption of livestock, including aquatic organisms and fish that have been reared in these environments [33]. The presence of pesticide residues in these products poses potential health risks to humans if they are consumed [20]. Furthermore, the substitution of fish ingredients with plant-based ingredients like rice bran, maize, wheat flour, and mustard cake in fish feeds also introduces commonly used pesticides from terrestrial agriculture into the fish feed supply chain [34].
The concentrations of target OCPs (mg/kg) in fish species from Eleyele Lake and Dandaru River in Ibadan, Nigeria are presented in Table 3. Oreochromis niloticus, Oreochromis aureus, Oreochromis mossambicus, Oreochromis lidole and Clarias gariepinus were analysed for target OCPs. All target OCPs were detected in at least one sample. Concentrations of beta-lindane ranged from non-detected (ND) to 0.0012mg/kg while aldrin concentrations ranged from ND-0.0026 mg/kg. Heptachlor epoxide concentration ranged from ND-0.013 mg/kg whereas beta-endosulfan levels ranged from ND-0.0011mg/kg. Endosulfanether amount ranged from ND-0.012mg/kg. Among the five fish species Clarias gariepinus had the lowest mean concentration: 7.0 x10-4 mg/kg for beta-lindane, aldrin and beta-endosulfan while Oreochromis niloticus had the highest concentrations of OCPs: 0.0128 mg/kg for heptachlor epoxide in samples from Dandaru River and 0.012 mg/kg for endosulfan ether in samples collected from Eleyele Lake. None of the investigated OCPs was detected in Clarias gariepinu ssamples collected from Eleyele Lake. Endosulfan ether was quantified in all the fish samples except for Clarias gariepinus from Eleyele Lake. Meanwhile, heptachlor epoxide was also found in almost all the fish samples, the exceptions were Clarias gariepinus and Oreochromis aureus samples obtained from Eleyele Lake. The concentrations of beta-lindane and aldrin measured in all the species of fish collected from Eleyele Lake and Dandaru River were below the permissible limit of 0.3 mg/kg [35] and the levels of beta-endosulfan in all fish species were below the acceptable limit of 5 mg/kg [35].
Concentrations of organochlorine pesticides (OCPs) (mg/kg) in fish species from Eleyele Lake and Dandaru River
In comparison with previous studies, aldrin concentrations in all the fish species from Eleyele Lake and Dandaru River were at similar levels to the levels determined in fish collected from Ogbese and Owan Rivers, Nigeria [11, 36], Volta Lake, Ghana [37] but higher amounts of aldrin were measured in fish from other studies such as Lake Chad [38] and Ogbese River [39]. Heptachlor epoxide was determined at similar concentrations in this study in some previously studies in Nigeria [11, 39], Lake Ziway, Ethiopia [40] and Manzala Lake in Egypt [41]. Also, similar concentrations of beta-endosulfan in this present work were quantified by Gbeddy et al. [37] and Ezemonye et al. [36]. However, higher levels of beta-endosulfan were measured in fish from Lake Geriyo [42] and Ogbese River [36] in Nigeria and Lake Taabo in Cote d’Ivoire [43]. Even though some researchers reported similar concentration levels in fish, as compared with the current study, for beta-lindane [36, 37, 40] much higher concentration (3.177 mg/kg) of beta-lindane was determined in fish sampled from Lagos lagoon, Nigeria [44].
Estimated daily intake of target OCPs
Using the OCPs concentrations measured in the fish species from both water bodies, the estimated daily intakes (EDIs) of OCPs via fish consumption were evaluated for three different population groups including adult, children and infants. The EDIs of the assessed OCPs via fish consumption by the three population groups are presented in Table 4 for Eleyele Lake and Dandaru River. Generally, among the target pesticides endosulfan ether had the highest estimated daily intake of 3.4 x 10-5 mg/kg/day of Oreochromis niloticus for the infant population. The estimated daily intakes of heptachlor epoxide for all the fish species in both Eleyele Lake and Dandaru River, and for all categories of population (adult, children and infants) were below the recommended acceptable daily intake of 0.013 mg/kg/day [11, 45]. Similarly, the recommended acceptable daily intakes of 0.03 and 0.005 mg/kg/day [11, 46] for aldrin and beta lindane, respectively were not exceeded for adult, children and infants due to consumption of all fish species collected from both Eleyele Lake and Dandaru River.
Estimated daily intake (EDI) of target OCPs (mg/kg/day).
Non carcinogenic risk
Pesticides have been associated with various chronic health effects, including malignant tumours, blood disorders, endocrine disruption, reproductive effects, and neurological disorders. These health effects are known to be linked to the exposure and use of pesticides. Values for HQ and HI for non-carcinogenic risk of target OCPs associated with consumption of the fish species collected from Eleyele Lake and Dandaru River by the three population groups are presented in Table 5 and Table 6, respectively. The results indicate that based on HQ values no non-carcinogenic risk was posed to adult and children by all investigated OCPs due to consumption of all fish species (except Clarias gariepinus from Eleyele Lake in which none of the OCPs was detected) collected from Eleyele Lake and Dandaru River. However, while other studied OCPs posed no non-carcinogenic risk to infants by consuming all the fish species, heptachlor epoxide posed high non-carcinogenic risk to infants by consuming fish species Oreochromis niloticus and Oreochromis lidole collected from Eleyele Lake as well as all studied fish species from Dandaru River except Oreochromis aureas. Similarly, hazard indices (HI) indicate that non-carcinogenic risk to adults and children was not apparent by consuming all fish species from Dandaru River and Eleyele Lake. However, a high non-carcinogenic risk to infants was expected by consuming Oreochromis niloticus and Oreochromis lidole from Eleyele Lake, apparently due to the contribution of heptachlor epoxide, as well as all fish species (except Oreochromis aureas) from Dandaru River due to the high HQ of heptachlor epoxide. In some previous studies in Nigeria such as Lake Chad [38], Lake Geriyo [42] and Lagos Lagoon [44] HI exceeded 1, indicating potential non-carcinogenic risk due to consumption of fish collected from these water bodies. Nantogo et al. [6] also found out that hazard quotient of heptachlor epoxide was above 1 in fish collected from Lake Nakuru, Kenya. Heptachlor epoxide could cause changes in nervous system and immune dysfunction in animals during gestation and infancy [47]. High dose of aldrin could lead to kidney damage and nervous system effects [48]. Large concentration of lindane may affect the nervous system which could lead to certain symptoms like dizziness, seizures, headache, convulsions and even death [49]. Beta lindane was also linked to increased occurrence of diabetes [50] and an altered thyroid hormone level which could affect brain development was observed in prenatal exposure. Moreover, certain OCPs have been linked to endocrine disruption and neurotoxicity [51]. It was found that prenatal exposure to OCPs disrupts reproductive hormones of foetuses even at relatively low levels [52]. Endosulfan is also known to be highly neurotoxic, causing both developmental neurotoxicity and chronic neurodegeneration [53].
Non-carcinogenic hazard quotient (HQ) and hazard indices (HI) of target OCPs in fish species from Eleyele Lake.
Non-carcinogenic hazard Quotient (HQ) and hazard indices of target OCPs in Dandaru River samples.
Carcinogenic risk
Carcinogenic risk was evaluated for beta lindane, aldrin and heptachlor epoxide. The results are presented in Table 7 and Table 8 for the fish species collected from Eleyele Lake and Dandaru River, respectively. CR for heptachlor epoxide due to consumption of Oreochromis niloticus and Oreochromis lidole from Eleyele Lake and Dandaru River by infants exceeded the threshold of tolerable risk of 1 x 10-4 whereas the CR values for adult and children were below the threshold value. Furthermore, among the fish species collected from Dandaru River, CR of heptachlor epoxide due to consumption of Oreochromis mossambicus and Clarias gariepinus by infants also exceeded the permissible limit. CR values for beta lindane and aldrindue to exposure to allinvestigated fish species from Eleyele Lake and Dandaru River were lower than the permissible limit. Considering the total carcinogenic risk due to beta lindane, aldrin and heptachlor epoxide, consumption of Oreochromis niloticus and Oreochromis lidole from Eleyele Lake by infants and Oreochromis niloticus from Eleyele Lake by children were higher than the permissible limit. Except for Oreochromis aureaus the TCR for all investigated fish species collected from Dandaru River indicate possible carcinogenic effects to infants. The combined effect of beta lindane, aldrin and heptachlor epoxide in Oreochromis niloticus from Dandaru River also posed carcinogenic risk to children. However, no carcinogenic risk was expected in adult due to consumption of all investigated fish species from both Eleyele Lake and Dandaru River. Aldrin is a probable human carcinogen and apart from being a probable carcinogen, heptachlor epoxide could induce tumours of liver in mice and rats [54].
Carcinogenic risk (CR) and Total carcinogenic risk (TCR) of target OCPs in Eleyele Lake samples.
Carcinogenic risk (CR) and Total carcinogenic risk (TCR) of target OCPs in Dandaru River samples.
Conclusions
In this study, the concentration levels and human health risk of five OCPs were investigated in five different species of fish from Dandaru River and Eleyele Lake in Ibadan, Nigeria. Clarias gariepinus exhibited the lowest OCPs concentrations. Oreochromis niloticus had the highest concentrations of endosulfan ether and heptachlor epoxide. While non-carcinogenic risk to adult and children was not apparent by consuming all fish species from Dandaru River and Eleyele Lake, a high non-carcinogenic risk to infants was expected by consuming Oreochromis niloticus and Oreochromis lidole from Eleyele Lake, as well as all investigated fish species (except Oreochromis aureas) from Dandaru River. There was no carcinogenic risk to adult due to consumption of all investigated fish species from both Eleyele Lake and Dandaru River whereas consumption of Oreochromis niloticus and Oreochromis lidole from Eleyele Lake by infants and Oreochromis niloticus from Eleyele Lake by children, as well as consumption of all investigated fish species (except Oreochromis aureaus) from Dandaru River by infants could present carcinogenic effects. Future studies should consider investigating the fish species in more lakes and rivers in Ibadan as well as a larger number of samples.
The findings emphasize the need for stricter monitoring and regulation of pesticides use in agriculture and awareness campaigns for fishermen and the public on the possible health effect of pesticides due to consumption of fish from the water bodies. In particular, policy implementation could involve restrictions on pesticide types to limit the use of hazardous ones, correct choice of application methods to minimize run-off and leaching into the water bodies, and appropriate disposal procedures of pesticide residues to prevent contamination of the water bodies.
Notes
Acknowledgement
Authors thank the fishermen at the investigated lake and river for the assistance in the collection of fish samples.
Conflict of interest
The authors declare that there is no conflict of interest.
CRediT author statement
OO: Investigation, formal analysis, Writing-Original draft preparation; GOA: Conceptualization, Methodology, Supervision, Writing- Review & Editing; AA: Conceptualization, Methodology, Formal analysis, Data curation, Supervision, Writing-Original draft preparation, Writing- Review & Editing.