Translocation capacity of some heavy metals in aquatic food chain of crude oil impacted community of Imiringi in Bayelsa state,Nigeria

Abstract

The translocation capacity of metals (Cd, Cr, As, Pb, and Hg) was determined in water and fish, and in the serum and vitreous humor harvested from New Zealand White (albino) rabbits fed with the processed fish. The sample size comprised 12 male rabbits divided equally into control and experimental groups. Both groups were fed with normal rabbit meal void of detectable metals for 3 months. Only animals grouped under the experimental group were fed fish meal harvested from River Imiringi, Bayelsa State, Nigeria. The metals of interest were estimated using Atomic Absorption Spectroscopy. Similarly, the choice statistical tool was the student t-test analyzed on SPSS version 18–22. The findings revealed that the studied heavy metal concentrations were higher in water and fish sourced from River Imiringi when compared with the World Health Organization’s minimum permissible limits. In the same vein, concentrations of cadmium, chromium, and total arsenic were significantly higher, whereas mercury was lower in fish when compared to that in the water. In addition, vitreous cadmium and lead concentrations were higher in the experimental group when compared with the control group, whereas vitreous chromium was lower. Furthermore, serum cadmium and chromium concentration comparisons were similar to that in the vitreous. The findings are indicative of the translocation capacity of metals from water to fish and then to serum and vitreous humor of rabbits. The increase in metal concentrations and their translocation capacity are potential risks to inhabitants of Imiringi that depends heavily on the river water resources.

Keywords

Heavy metals river imiringi fish vitreous serum

Introduction

The term heavy metals refer to any metallic chemical element that has a relatively high density and is toxic at low concentration. The negative impacts of heavy metals cut across both biotics and abiotics.¹ Despite the negative impacts associated with heavy metals, some are still vital for metabolic processes.² Heavy metals of interest in this study include mercury (Hg), cadmium (Cd), arsenic (As), chromium (Cr), and lead (Pb).

The aquatic environment is the habitat for marine life; where nutrition, respiratory and other vital processes take place. These processes are the routes through which nutrients and toxic substances traverse marine lives such as fish. The fate of toxic compounds or molecules in marine lives is quite complex as some are excreted, while others bioaccumulate and biomagnify in the body. Bioaccumulated toxic substances in fish have the tendency of being transferred to end consumers such as humans or animals.

Nutrients and toxic substances are either excreted through the digestive system or assimilated into the circulatory system. Furthermore, the circulatory system aids the transportation of these substances into its complementary reservoirs via the plasma or vitreous as the case may be.^3,4

Heavy metals are transferred to humans and animals through direct and indirect exposure to contaminants from various sources.⁵ One of the major sources is the consumption of fishes exposed to contaminants such as heavy metals. Fish are particularly vulnerable and heavily exposed to contaminants due to the body surface, nutrition, and respiration. Fish, in comparison with invertebrates, are more sensitive to many toxic substances and could serve as an indicator of a healthy ecosystem.^6,7 The transference of heavy metals from an organism to humans is one of the major routes of food chain toxicity. This phenomenon has been validated and reaffirmed by a lot of authors using several organisms.^6–8 The New Zealand White (albino) rabbit was the choice animal model for this study. Its suitability is attributed to its anatomical and physiological similarities to humans and other related studies.^9,10

Imiringi is one of the oldest communities in Bayelsa State of Nigeria known for crude oil and gas exploration and exploitation. The environment and aquatic bodies of Imiringi are exposed to heavy contamination due to effluence from crude oil exploitation, pipeline leakages, and gas flaring. Host communities to oil and gas infrastructures are constantly exposed to immeasurable environmental pollution.^11,12 A study by Ogamba et al.¹³ evaluated the level of some heavy metals in water, sediment and Eichhornia crassipes from Kolo Creek, Niger Delta, Nigeria. Triplicate samples were collected from three locations of which Imiringi was one. The results revealed an increase in concentrations of lead, cadmium, iron, manganese, mercury, and copper above the permissive limits set by the World Health Organization (WHO). Another study by Chinedu and Chukwuemeka,¹⁴ found heavy metals in the study location’s fauna and flora and ascribed it to crude oil and gas exploration and exploitation.

The build-up of these heavy metals in the ecosystem are deleterious to lives as many diseases and poisoning have been demonstrated to have a strong correlation.^15–17 Handful of studies have implicated human health deficits in Nigeria to heavy metal toxicity.^18,19 This current research was therefore carried out to evaluate the transference and translocation capacity of some heavy metals via fish consumption chain in the oil exposed community of Imiringi using rabbits as an end consumer model.

Materials and methods

Study location

The fish samples for the study were collected from various locations within River Imiringi located in Imiringi town of Bayelsa State, Nigeria (Figure 1). Imiringi is a community in Ogbia Local Government Area encompassing Otuabagi (Olobiri) the first-place crude oil was discovered on Sunday 15 January 1956 in Nigeria. Bayelsa state has an area of 695 km² and is well known for its historic value to contemporary Nigerian economy, the mainstay of which is its oil industry. The animals were bred in the Department of Biochemistry Laboratory, Federal University Otuoke, Bayelsa State. Similarly, the heavy metal analysis was carried out at the Eni-yimini Laboratories (eL) Ltd, Igbogene-Epie, Bayelsa State.

Figure 1.

Map of Bayelsa State, showing Imiringi town location. Source; www.google.com/mapofbayelsastateshowingogbia

Research design and sample size

Twelve (12) rabbits constituted the sample size as validated by Mead’s resource equation.²⁰ The rabbits were divided equally into control and treatment groups. The control and the treatment groups were treated similarly, except for the exclusion of grinded fish sourced from River Imiringi from the diet of the control. After 2 weeks of acclimatization in the laboratory, the animals were exposed to the above-stated regimes consecutively for 3 months, which was followed by euthanization using chloroform.

Selection criteria

All the rabbits used for the study were confirmed suitable by a veterinarian. Rabbits showing signs or symptoms of illness were excluded. Also excluded were lysed or turbid samples. The study exclusively used only male New Zealand White (albino) rabbits that were within the age range of seven to 8 months and are weighted between 1.8-2 kg.

The suitability of New Zealand white (albino) rabbits as a choice animal for research of this nature is attributed to its anatomical and physiological similarities to that of human.^10,21 Water samples and fish were harvested from several locations within River Imiringi.

Ethical approval

The ethical clearance approval was obtained from the Directorate of Research and Quality Assurance of Federal University Otuoke, Bayelsa State. To ensure international conformity, the research protocol adhered stringently to the Animal Welfare Act of 1985 of the United State of America for research and Institutional Animal Care and Use Committee (IACUC).

Collection of samples

Vitreous humour and blood

Vitreous humours were collected following Coe’s protocol,²² while Ness’s protocol was followed in the collection of blood.²³ Both samples were collected into plain containers and centrifuged at 2000 g (rev/min) for 10 minutes at 25°C. After centrifugation, the supernatants were separated into plain sterile containers and for the biochemical analysis.

Water

Ten (10) ml of water samples were collected from 10 locations along River Imiringi into sterile containers. The water samples were immediately transported to the laboratory for heavy metal analysis. All the processes involved in the collection were strictly void of contamination.

Fish

Catfish was the choice for the study and were harvested from River Imiringi. The choice is due to availability and consumption preference in the locality. Cat fish is used in the preparation several cuisine varieties in Imiringi. The fishes were washed, sun-dried, and grinded before being used. Aseptic methods were strictly followed to avoid contamination during the collection and processing stages. The total weight of the processed catfish was 2.7 kg. Approximately 0.2 kg of the fish was used for heavy metal estimation, whereas 2.5 kg were included in the diet of the treatment group.

Laboratory procedure

A total volume of 1.2 mL each of vitreous humour and serum samples were thawed separately at room temperature and each was treated separately. A volume of 300 L of each of the samples was added to 300 μL of HNO₃ and 100 μL of H₂O₂. Sample decomposition was then carried out in a water bath at 80^oC for 30 min. After digestion/decomposition, each of the samples was diluted to 10 μL with deionized water. Likewise, water and fish samples were weighed and digested with aqua regia for 1 h. The samples were allowed to cool and filtered into a 50 mL volumetric flask after digestion was completed. The digested samples from all the prepared matrices were then analyzed using Varian Spectra A100 Atomic Absorption Spectroscopy (AAS) for Pb, Cd, Cr, Hg, and As. Hydride method was used for the analysis of the total arsenic.

Statistics

Data were analyzed with the aid of the statistical package for social science (SPSS) program version 22 (SPSS inc. Chicago, IL, USA; Version 18–12) and Microsoft excel. Student t-test was the choice statistical tool for the mean comparisons of the various groups. Data were presented as Mean ± Standard Deviation and the level of significance was pegged at less than or equal to 0.05.

Results

Table 1 shows a significant increase in concentrations of all the heavy metals studied in River Imiringi when compared with that of WHO permissive limits.

Table 1.

Mean comparison of some heavy metal concentrations in River Imiringi and minimum acceptable limits.

Metals	Imiringi waterHeavy metal mean	Minimum acceptable limit of heavy (MALHM) metals mean	MALHMSources
Cadmium mg/L	0.0340 ± 0.035	0.003	WHO²⁴
Chromium mg/L	0.0758 ± 0.0085	0.05	Chiroma et al.²⁵ and aneyo et al.²⁶
Total arsenic mg/L	0.2000 ± 0.081	0.010	WHO²⁴
Lead mg/L	0.1450 ± 0.0129	0.010	WHO²⁴
Mercury mg/L	0.0450 ± 0.0074	0.010	WHO²⁴

Table 2 shows a significant increase (p < 0.05) in concentrations of cadmium, chromium, and total arsenic in the fish when compared to water harvested from river Imiringi, whereas mercury was on the contrary.

Table 2.

Increase in concentrations of Cadmium, Chromium and Total Arsenic in Fish versus Water.

Metals	Heavy metal conc. In water±SD	Heavy metals conc. In fish±SD	t-test	p-value
Cadmium mg/L	0.0340 ± 0.035	0.4355 ± 0.1601	−4.996	0.002
Chromium mg/L	0.0758 ± 0.0085	0.8630 ± 0.0530	−29.33	0.000
Total arsenic mg/L	0.2000 ± 0.081	0.7527 ± 0.1180	−7.706	0.000
Lead mg/L	0.1450 ± 0.0129	0.1918 ± 0.0785	−1.175	0.285
Mercury mg/L	0.0450 ± 0.0074	>0.0001	28.013	0.000

A comparison between vitreous heavy metal concentrations of the control and treatment groups were portrayed in Table 3. The results show a significant increase (p < 0.05) in cadmium and lead in the latter when compared to the former, whereas chromium differed.

Table 3.

Increase in concentrations of Cadmium and Lead, and decrease in chromium in vitreous treatment versus Vitreous Control.

Metals	Vitreous control	Vitreous treatment	t-test	p-value
Cadmium mg/L	0.0002 ± 0.0000	0.0094 ± 0.0016	−29.932	0.000
Chromium mg/L	0.0020 ± 0.0008	>0.0001	−10.628	0.000
Total arsenic mg/L	>0.0001	>0.0001
Lead mg/L	0.0020 ± 0.0001	0.040 ± 0.0165	−4.648	0.004
Mercury mg/L	>0.0001	>0.0001

Table 4 shows a significant increase (p < 0.05) in the concentration of serum cadmium in the treatment group when compared with the control, whereas serum chromium conflicted.

Table 4.

Increase in concentration of Cadmium, and decrease in concentration of total arsenic in serum of treatment versus Serum of Control.

Metals	Serum control	Serum treatment	t-test	p-value
Cadmium mg/L	0.0027 ± 0.0006	0.0055 ± 0.0017	−3.089	0.021
Chromium mg/L	0.6170 ± 0.0587	0.0040 ± 0.0016	0.059	0.000
Total arsenic mg/L	>0.0001	>0.0001
Lead mg/L	0.0250 ± 0.0075	0.0263 ± 0.0084	−0.222	0.831
Mercury mg/L	>0.0001	>0.0001

Table 5 Indicated a significant increase in concentrations of cadmium, chromium, and lead in the serum of the control (p < 0.05), when compared with that of the vitreous of the control.

Table 5.

Increase in concentrations of Cadmium, Chromium and lead in Serum Control versus Vitreous Control.

Metals	Vitreous control	Serum control	t-test	p-value
Cadmium mg/L	0.0002 ± 0.0000	0.0027 ± 0.0006	−7.738	0.000
Chromium mg/L	0.0020 ± 0.0008	0.6170±0.0587	−20.972	0.000
Total arsenic mg/L	>0.0001	>0.0001
Lead mg/L	0.0020 ± 0.0001	0.0250 ± 0.0075	−6.111	0.001
Mercury mg/L	>0.0001	>0.0001

Concentrations of chromium and lead were higher (p < 0.05) in the serum of the treatment when compared to the vitreous of the treatment, whereas cadmium differed as depicted in Table 6.

Table 6.

Increase in concentrations of Chromium and Lead, and decrease in cadmium in Serum Treatment versus Vitreous Treatment.

Metals	Vitreous treatment	Serum treatment	t-test	p-value
Cadmium mg/L	0.0094 ± 0.0016	0.0055 ± 0.0017	4.193	0.006
Chromium mg/L	>0.0001	0.0040 ± 0.0016	−10.682	0.000
Total arsenic mg/L	>0.0001	>0.0001
Lead mg/L	0.040 ± 0.0165	0.0263 ± 0.0084	−20.583	0.000
Mercury mg/L	>0.0001	>0.0001

Discussion

The presence of heavy metal concentrations above the acceptable permissive limits in water bodies is indicative of contamination. Contaminated water is known to contain many compounds that are deleterious to end-users and to an extent the ecosystem. Users of contaminated water have the tendency of picking up metals through a lot of routes; inclusive of oral, inhalation, and absorption. In the case of water, the metals get to the systems via the oral and/or subcutaneous routes. This study was therefore designed to investigate the transference and translocation capacity of some heavy metals within the marine habitat consumption chain using a rabbit as an animal model.

Heavy metals such as cadmium, chromium, total arsenic, lead, and mercury were found in water harvested from river Imiringi in higher concentrations above the WHO permissive limits (Table 1). This can be seen as a potential public disaster and emergency as the concentrations could have an acute or chronic disruptive effect on the health of the inhabitants and by extension, the ecosystem. Similar scenarios have resulted in heavy metal intoxication as reported in handful of reports.^27–29 The increase could be due to years of oil exploration and exploitation and/or the use of herbicides or insecticides for farming. Farmers in Imiringi patronize herbicides to prevent the growth of weeds during crops cultivation. These chemicals are known to access waterways through wash-off during raining season. This study is in line with that posited by Ifenkwe et al.³⁰ on increase in heavy metal concentrations in water bodies resulting from crude oil exploration and exploitation. The findings on increased lead and arsenic concentrations above safe limits in water samples are also in accordance with the reports of handful of authors.^31,32 The increase in arsenic concentration is deleterious as it is a known disruptor of the enzymatic efficiency of glucose-6-phosphate dehydrogenase and pyruvate dehydrogenase.³³ These enzymes play crucial role in metabolic processes such as glycolysis, kreb cycle and electron transport chain (ETC).

Further, the study revealed a significant increase in concentrations of cadmium, chromium, and total arsenic in the fish harvested from Imiringi river when compared to the river water, whereas mercury was on the contrary (Table 2). The higher concentration of cadmium, chromium, and arsenic in the fish could be due to the chronic bioaccumulation effect resulting from crude oil exploitation and exploration, and other anthropogenic sources. The bioaccumulation effect is a known scientific basis for the building up of heavy metals in the tissues of animals due to transportation efficiency in the body.³⁴ This study supports the perspectives of Bawuro et al.³⁵ and Montazer and Ali³⁶ on the bioaccumulation of heavy metals in tissues of fish and other marine bodies.

Moreover, a comparison of heavy metal concentrations between the vitreous of the control and treatment groups revealed a significant increase in cadmium and lead in the latter when compared to the former, whereas chromium decreased (Table 3). The increase in vitreous cadmium and lead could be due to translocation from the consumption of fish sourced from River Imirinigi. Concentrations of cadmium and lead have been shown in the preceding paragraph to be high in River Imiringi. The decrease in chromium concentration may be attributed to the physiological and biochemical importance to the body as it drives several metabolic processes.^2,37

However, the comparison of heavy concentrations in the serum control to that of the treatment exhibited an increase in chromium, whereas cadmium decreased (Table 4). The increase in the treatment group of serum cadmium concentration could be attributed to translocation due to the consumption of meals containing cadmium. On the contrary, the basis of the increase in serum chromium concentration in the control group could be physiological as posited above.²

Comparison between heavy metal concentration between the control vitreous and serum, and on the other hand between treatment vitreous and serum revealed an increase in most of the heavy metals in the serum (Tables 5 and 6). The increase could be attributed to the receptive and cosmopolitan transportation system of the plasma. The plasma carries almost all the molecules in the body to various locations inclusive of the vitreous. In addition, the vitreous serves only the eyes, and its volume is infinitesimal when compared to plasma. An exception was observed for vitreous cadmium. The eye could be one of the storage sites of cadmium for the concentration to be higher in the vitreous than the serum. This opinion is in line with the thinking of Will et al.³⁸ who also advanced that the retina is also the site for the deposition or storage site of cadmium.

The occurrence of the transference and translocation of heavy metals from water bodies to fishes and then to humans have been further validated by this study using rabbit as a model. This has affirmed the arguments that inhabitants of oil exploited communities are at risk of heavy metal-induced intoxications and diseases.

The side effect of the bioaccumulation of metals in the body and the ecosystem is a disaster in waiting. A similar scenario has been experienced in Minamata Bay, Japan, in the middle of the 1950s, resulting in an illness called Minamata disease.³⁹ This study has further advanced the cause of Niger Delta of the Federal Republic of Nigeria that the environment has been battered, molested, and debased. A clarion call for remediation and making available green projects such as borehole water, solar energy, and an effective healthcare system is imperative.

The limitation of the study was mainly on the lack of sophisticated equipment and finance in the speciation of the heavy metals studied. Arsenic and chromium speciation could have been valuable in elaborating toxicity, mechanism of action and valency biology.

Conclusion

This study has brought to bear that water bodies in oil-exploited communities are encumbered with heavy metals which are deleterious to health and disruptive to the ecosystem. The presence of studied heavy metals above the international minimum permissive limits is a clarion call for an emergency intervention to forestall heavy metal-induced diseases and intoxication epidemics. Further studies on this topic and the provision of green projects by government, and oil multinationals are strongly advised.

Significance statement

This study revealed the transference potentials of some heavy metals along the food chain from the aquatic environment. The bioaccumulation of the identified heavy metals in human food materials can have a long-term deleterious effect on various organs of the human body if continuous consumption is not checked. The findings of this study can be extended by further studies in the fields of ophthalmology and toxicology where heavy metals have been linked to a lot of pathologies.

Footnotes

Acknowledgements

Special appreciation to all my project students for the assistance in sample collection, literature gathering and typesetting. Similarly, an appreciation goes to Eni-Yimini Laboratory (eL) Ltd, Igbogene Epie, Yenagoa, Bayelsa State for the sample analysis and other research supports.

Author’s contribution

All authors contributed to the conception and design of the work. Conception and design, Interpretation of the results and revisions performed by Dr E.S. Agoro performed data acquisition and analysis, and literature search and gathering. Mr G. Ikimi did the statistical interpretation and case analysis. All authors read and gave final approval of the manuscript and are accountable for the originality of the work.

Declaration of conflicting interests

The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

Ethical approval

The study protocol was approved by the Directorate of Research and Quality Assurance of the Federal University Otuoke, Bayelsa State, Nigeria. The ethical principles for medical research involving animal subjects as outlined in the Helsinki declaration in 1975 and subsequent revisions were strictly adhered to in the course of this study.

ORCID iD

Eni-yimini S Agoro

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