Heavy metals concentration and distribution in soils and vegetation at Korle Lagoon area in Accra, Ghana

The call for reclamation of land around Korle Lagoon in Accra, Ghana, where burning of E-waste and cultivation of vegetables takes place, make risk assessment of heavy metal contaminations important. This study aimed at evaluating the levels and risk of heavy metal contamination in soils and vegetation around the Korle lagoon area in Accra. Geoaccumulation index, enrichment factor and pollution load index were determined to assess the risk of contamination. The levels and distribution of nine heavy metals (Pb, Hg, Cd, As, Zn, Sn, Ni, Cu and Cr) in soil (0 – 20 cm) and common vegetation ( Panicum maximum, Imperata cylindrica , Lactuca sativa and Hibiscus sabdariffa ) from the area using Atomic Absorption Spectrometer (AAS) were assessed. The area was divided into five sites namely; the e-waste site (S1), gardens area (S2), recreational area (S3), reclaimed area (S4) estuary (S5), and the control (S6) which was about 700 m away. Soil analysis showed that the concentration of Pb (184.44 mg/kg), Cd (103.66 mg/kg), Cu (202.99 mg/kg), Ni (72.00 mg/kg) and Sn (705.32 mg/kg) at S1 exceeded their WHO/FAO thresholds for agricultural soils. Concentrations of heavy metals in soils from the e-waste site was significantly different ( p < 0.01) from the other sites. High accumulations of heavy metals were also observed in the plants samples collected from the study sites, with the concentrations of Cu, Pb, Ni and Cd exceeding their acceptable limits. Laws against open burning of e-waste should be enforced and animals should be restricted from grazing on the forage.


Introduction
The fast technological change occurring with increase in demand for information technology has resulted in large volumes of e-waste globally (Wagner, 2009). E-waste contains many different substances that are classified as hazardous (Cd, Pb, As, Be, Cr, Hg, polycyclic aromatic hydrocarbons (PAHs), chlorofluorocarbons, polybrominated diphenyl ethers and dioxin-like compounds) and non-hazardous (Zn, Cu, Se, precious metals Ag, Au, Pt, among others.) which have significant harmful environmental impacts when not well disposed off (Lim, 2010;Tsydenova & Bengtsson, 2011). However, some non-hazardous chemicals such as Zn, Cu, and Se can become hazardous to humans and ecosystems depending on the dose and concentrations, and the target receptors (Musee, 2011;Tchounwou, Yedjou, Patlolla, & Sutton, 2012;Itai, et al., 2014).
In West Africa, the informal recycling of e-waste is becoming an emerging problem due to the high use of electric and electronic equipment (EEE) imported from the developed world (Feldt et al., 2014). Currently, West Africa serves as the major route in Africa, with Ghana and Nigeria serving as the main import hubs. It is estimated that about 215, 000 tons of new and used EEE were imported into Ghana and 129, 000 tons were generated in 2009 alone (E-waste Africa Programme, 2011). The methods mostly used in the recycling of these EEE include melting of electronic boards on open fire to extract metals and valuable chips, burning of cable wires to recover copper and open burning of residual waste materials (Feldt et al., 2014). These methods result in the emission of high concentration of toxins into the atmosphere there by polluting the environment, endangering the health of recycling workers and residents in the surrounding communities. Apart from a number of heavy metals and variety of organic toxins, like shown that PAHs constitute an important emission from informal e-waste recycling (Asante et al., 2012;Ma et al., 2009;Wang et al., 2012;Wang et al., 2010).
The Agbogbloshie slum is one of Ghana's largest E-waste dump sites. Obsolete electronic gadgets of no perceived value are disposed off in a large area on the edge of the e-waste market (also located in the Agbogboloshie slum) that is also used for the disposal of a wide range of other types of waste (Brigden, Labunska, Santillo, & Johnston, 2008). The north-eastern part of Agbogbloshie in Accra is where Korle lagoon is located, with the reclaimed site few meters away. Workers involved in the e-waste recycling, use open fire to extract metals, valuable chips and copper from electronic gadgets as well as cable wires. In addition, residents burn discarded electronic gadgets at a section of the Korle lagoon reclamation area to extract copper and other valuable metals. The fumes originating from the burning of the e-waste materials might contain heavy metals and other polyaromatic compounds which eventually end up in soils and vegetation of the reclaimed area. Furthermore, herds of cattle from neighbouring communities graze on the vegetation of the reclaimed waste land exposing them to heavy metals. Adjacent to the reclaimed area is a former dump site, which has been converted to an active vegetable garden by the urban poor in the vicinity. These vegetables and vegetation are likely to take up any heavy metals in the soil, hence, engendering the health of the consumers. Research shows that the presence of heavy metals in food and water in relatively high concentration has serious health implications. For example, mercury and cadmium are known to cause injury to the kidney or kidney dysfunction among others. The negative effect of heavy metal exposure in the environment, either through inhalation or ingestion of contaminated food is thus a major concern to researchers, governments and the general public because of its profound effects on humans and wildlife. Little is however known about the extent of heavy metal pollution of soil and vegetation in the study area. This paper aims to assess the level of heavy metal pollution in soils and vegetation around the Korle lagoon reclamation area in Accra.

Study Area
This study was conducted at the Korle Lagoon area in Accra, Ghana. Korle Lagoon is a coastal wetland comprised of beautiful sand dunes, open lagoon, salt pans, marsh and scrubs. The lagoon also provides roosting and nesting grounds for various species of seabirds. It is 104 m above sea level with its coordinates at 5°33'0" N and 0°13'0" E. Accra is a coastal savannah zone which experiences bimodal rainfall. The average annual rainfall is about 730 mm, and ranges between 635 mm and 1140 mm. The mean temperature is about 28 o C with a minimum and maximum temperature of 25 o C and 35 o C respectively.

Description of the sampling sites
The study area was divided into five (5) sites depending on the activity that was carried out during the time of the research. These comprised of E-waste area (S1) where burning of electronic waste, collected along the length and breadth of the capital are brought for burning in order to retrieve essential components for sale abroad; site 2 was the garden area (S2), where vegetables and plants are grown; site 3 was a reclaimed waste dump site (S3), site 4 a recreational site (S4), and site 5 is the estuary area (S5) of the Korle Lagoon. Each site was about 300 m apart. The control (S6) was 700 m away.

Sample Collection
In each of the selected sites, six quadrats were marked. In each quadrat, four (4) core soil samples were collected randomly at depth 0-20 cm using a soil auger and put together to form a composite sample. The composite samples were well mixed and sub-samples taken (Qin et al., 2014). Six soil replicates were collected from each site, making a total of 36 soil samples from the study area. The soil samples were kept in zip-locked plastic bags, labelled and transported to the laboratory for further treatment and analysis. The soil samples were air dried at room temperature for 4 days, and ground to fine powder. They were then sieved with a 2 mm sieve to remove the coarse soil components. Sub-samples of the sieved soils were then taken for soil physico-chemical and heavy metals analysis.
In addition, twelve samples each of dominant plant species in each of the sites were collected for analysis. The plants samples collected were lettuce (Panicum maximum, Imperata cylindrica, Lactuca sativa and Hibiscus sabdariffa). The plant samples were obtained by cutting at a height of 5 cm above the soil surface. The plant samples were freeze dried using the CHRIST Getriertrocknugsanlagen GmbH Freeze dryer at a temperature of 17 ˚C with a vacuum mbar of 6.110.

Analysis of soil properties
The soil properties analysed were soil particle size distribution, pH, organic carbon, organic matter and exchangeable cations (K + , Ca 2+, Na + and Mg 2+ ). These characteristics were determined using the methods described by Wahabu, Fosu-Mensah, and Nyame (2015) and Fosu-Mensah, Okoffo, Darko, and Gordon (2016). The amount of soil organic matter (SOM) was examined by multiplying the percentage carbon by the factor 1.724 (Walkley & Black, 1934). To determine Exchangeable sodium (Na + ), potassium (K + ), Ca 2+ and Mg 2+ the methods described by Wahabu et al. (2015) were followed.

Determination of heavy metals in soil and plant samples
Acid digestion of soil sample was done by weighing a 1.5 g of soil sample into a well labelled 100 mL polytetraflouroethylene (PTFE) Teflon bombs which was previously acid washed. Six sample was weighed in an acid washed Teflon bomb labelled "100 mL polytetraflouroethylene (PTFE)" and a similar procedure followed. Blanks were prepared to check for background contamination by the reagents used. The digested soil and plant samples were analysed for the heavy metals (Cd, As, Pb, Cu, Ni, Sn, Hg, Cr and Zn) using atomic absorption spectrophotometer (AA 240 FS, Varian) (Kumar, Singh, & Garg, 2012). All the readings were taken in five replicates.

Methods of Assessment of contamination in soils
In this study, geoaccumulation index (I geo ), enrichment factor (EF), and pollution load (PL) were calculated to assess the heavy metal contamination levels in soils from the study area.

Geoaccumulation Index ( geo)
The index of geoaccumulation (I geo ) is widely used in the assessment of contamination by comparing the levels of heavy metals obtained to background levels originally used with bottom sediments (Muller, 1969;Atiemo et al., 2011). It is calculated using the equation: Where C n represents the measured concentration of the elements studied and B n is the geochemical background value of the element in fossil argillaceous sediment (average shale) (Taylor & McLennan, 1985). The following classification is given for geoaccumulation index :<0 = practically unpolluted, 0-1 = unpolluted to moderately polluted, 1-2 = moderately polluted, 2-3 = moderately to strongly polluted, 3-4 = strongly polluted, 4-5 = strongly to extremely polluted and >5 = extremely polluted (Lu, Wang, Lei, Huang, & Zhai, 2009).

Enrichment factor (EF)
Enrichment factor (EF) of an element in the studied samples was based on the standardization of measured element against a reference element. Al was used as the reference element in this study. The EF is calculated using the equation: The Pollution index (PI) is defined as the ratio of element concentration in the study to the background content of the abundance of chemical elements in the continental crust. Pollution index and integrated pollution index are also commonly used to assess environments quality (dos Anjos et al., 2000). PLI for the soil samples was determined by the equation below, as proposed by Tomilson, Wilson, Harris, and Jeffrey (1980). PLI = (CF n × CF n × CF n × CF n × CF n × CF n ) 1/n . The PI of each element is classified as either low (PI ≤ 1), middle (1< PI ≤ 3) or high (PI >3) (Chen et al., 2005).

Data Analysis
The data was analysed using SPSS 16.0. The Tukey test was used for pairwise comparison of means to identify significant differences of heavy metals among the sites. Table 1 presents the summary of the physicochemical properties of soil samples from the study sites. The pH of the study sites ranged from 4.67 at S3 to 7.74 at S5 with a mean value of 6.93.

Physicochemical properties of soil samples from the study area
The low pH (4.67) at site S3 might probably be due to the dumping of acid containing waste materials like batteries on the site as the site was once a dumping site. The OC content of the soils ranged from 0.38 % at S5 to 0.85 % at S1 with a mean value of 0.50 %. Similarly, soil organic ranged from 1.13 % at S5 to 2.51 % at S1 with a mean value of 1.48 %. The exchangeable K + ranged from 0.58 cmol/kg at S6 to 1.52 cmol/kg at S1 and S3 with a mean value of 1.07 cmol/kg. In addition, the exchangeable Na + content of the soils analysed ranged from 2.01 cmol/kg at S6 to 6.15 cmol/kg at S1 with a mean of 3.86 cmol/kg. The exchangeable Ca 2+ values ranged from 10.13 cmol/kg at S6 to 97.87 cmol/kg at S1 with a mean value of 30.65 cmol/kg. Site S6 recorded the lowest value (7.60 cmol/kg) of exchangeable Mg 2+ with the highest (73.4 cmol/kg) recorded at S1. Table 2 presents the summary of the mean concentrations of heavy metals (Hg Pb, Cu, Zn, Cr, Cd, Ni, Sn, and As) analysed in the soil samples at the various sampling sites at Korle Lagoon area in the Greater Accra region of Ghana. Analysis of variance (ANOVA) revealed significant (p < 0.05) variation in the concentrations of the nine (9) elements among the sites (Table 2) which is an indication of the extent of metal pollution in the soils. The Tukey test revealed that the concentrations of most of the elements were significantly (p < 0.01) higher at the e-waste site (S1) compared to the other sites (Table 2)  Mercury in the soil samples analysed ranged from <0.001 mg/kg at S2, S5 and S6 to 0.667 mg/kg at S1. The mean concentration of mercury recorded at the different sites were below the WHO/FAO (2001) limit of 2.00 mg/kg for soils. The low concentration of Hg can be attributed to the fact that Hg easily evaporates into organo-mercury forms (Environmental health and safety manual, 2000).

Heavy metal concentration of soils at the different sites in the study area
The concentrations of lead (Pb) in soil samples analysed ranged from 1.28 to 184.44 mg/kg with a mean value of 37.12 mg/kg. The E-waste site (S1) recorded the highest mean concentration of Pb whereas the garden area (S2) recorded the lowest mean concentration. Analysis of variance (ANOVA) showed significant differences (p < 0.05) in the mean concentration of Pb among the sites. The mean concentration of Pb at the e-waste zone (S1) was above the WHO/FAO (2001) permissible limit of 50.00 mg/kg for soils. The higher concentration of Pb recorded at the Ewaste site (S1) could be attributed to the burning of electronic waste (such as refrigerator, used computers, cables, printers, photocopy machines, automobile tires, batteries, air condition among others). The mean value of Pb recorded in this study was however lower than the mean value of 2645.31 mg/kg reported by Pradhan and Kumar (2014) in an e-waste recycling site soil.
The mean concentration of copper recorded from the various sites ranged from 3.47 mg/kg at S2 to 202.99 mg/kg at S1with a mean value of 38.80 mg/kg. The mean concentrations of copper recorded were below the WHO/FAO (2001) permissible limit of 100 mg/kg for soils except at S1 (202.99 mg/kg) which was above the WHO/FAO (2001)   The mean concentration of zinc (Zn) ranged from 0.83 at S2 to 37.33 mg/kg at S5 with a mean value of 8.68 mg/kg. The maximum mean concentration of Zn recorded at the e-waste zone (S1) was below the WHO/FAO (2001) permissible limit of 300.00 mg/kg for soils. The presence of zinc in soil at the various sites could be attributed to the occurrence of dry cells in the municipal waste as reported by Thorpe and Harrison (2008)  The concentration of chromium Cr ranged from 2.28 at S3 to 56.00 mg/kg at S1 with a mean value of 11.55 mg/kg. The high concentration of Cr recorded at S1 could be as a result of the recycling of E-waste such as refrigerator, used computers, cables, printers, photocopy machines, automobile tires and batteries at the site.
Similarly, the concentration of Cd ranged from <0.001 mg/kg at S3 to 103.66 mg/kg at S1 with a mean value of 18.64mg/kg. The mean concentrations of Cd recorded at all sites were above the WHO/FAO (2001) permissible limit of 3 mg/kg for soils except S3, S4 and S6 which recorded values that were below the WHO/FAO permissible limit. Cadmium is very much connected with non-residual fractions of heavy metals and thus makes them mobile and potentially bio-available for uptake by plants (Zhang et al., 2009).
The mean concentrations of nickel recorded in the soil samples ranged from 0.91 mg/kg at S2 to 72.00 mg/kg at S1 with a mean value of 13.60 mg/kg. The mean concentration of Ni recorded at the various sites were below the WHO/FAO (2001) permissible limit of 50 mg/kg for soils except for S1 which recorded a mean value that was above the permissible limit.
On the other hand, the mean concentration of Sn at the sites ranged from 8.77 at S3 to 705.32 mg/kg at S1 with a mean value of 132.86 mg/kg. The mean concentration of Sn obtained at S1 was above the FAO/WHO (1984) permissible value for Sn. The concentration of arsenic (As) recorded in soils ranged from 0.04 mg/kg at (S6) to 3.67 mg/kg at (S1) with mean value of 1.09 mg/kg. The mean concentrations of As at all sites were below the WHO/FAO (2001)  In general, the E-waste site (S1) recorded the highest concentration of heavy metals in soil samples as compared to the other sites. The burning of the E-waste materials results in the emission of toxins such as heavy metal in high concentration, thus exposing the recycle workers and the communities around to health risk. Li, Duan, and Shi (2011) reported that high concentration of heavy metals is recorded at pollution source. Table 2 Summary of mean of Heavy metal concentration of soils within 0-20 cm depth in different sites in Korle Lagoon area in Accra Table 3 presents comparison of heavy metal concentrations in E-waste dump sites of some cities of the world with data from E-waste site at the Korle Lagoon area in Accra. From the results, it was observed that heavy metal such as Hg, Pb, Zn, Cr, As and Ni were the most prominent heavy metals in the E-waste recycling site compared to Sn and Cu. In the current report, the mean

Index of Geoaccumulation (Igeo)
Soil quality was measured using the I geo index of classification proposed by Muller (1981) (Table   4). The results of I geo analysis indicated that, S1 and S2 were practically uncontaminated by Hg, Zn, Cr, Ni and As, while S1 was strongly polluted by Pb and extremely polluted by Cd and Sn which are the major constituents of e-waste (Pradhan & Kumar, 2014). In S3, S4, S5 and S6, only Sn showed moderate contamination with S3 showing strong contamination. The rest of the elements exhibited no pollution at the various sites. This might be due to the absence of e-waste activity and horizontal spread of metal pollutants in these areas.  The PLI values of Cu, Zn, Cr, As and Ni fell within the PLI ≤ 1 category. This means that the presence of these heavy metals in the earth crust was low (Pradhan & Kumar, 2014) and their pollution in the soil is very minimal. On the other hand, Hg and Pb belong to 1 < PLI ≤ 3 category which means that their presence in the study area fell between low to high pollutants in the soil. However, Cd and Sn were within the high category with PLI > 3. This meant that the presence of Cd and Sn was high in the study area.

Heavy metal concentration in plants at different sites from the Korle Lagoon area in Accra
Heavy metals with different concentration were detected in common plants in all sites under study. Table 6  Among the heavy metal analyzed, Hg was not observed in any of the sampled plants while Pb was also not detected at S4. The non-detection of Hg in the plant samples could be attributed to the minimal or no usage of mercury in the activities undertaken at these zones. It might also be the fact that Hg can easily be transformed into other organic forms which are more poisonous (Clarkson, 1997;Boening, 2000). Hg is not essential for plant growth (Lange, Nobel, Osmond, & Ziegler, 2013). The ability of plants to accumulate essential metals equally enables them to acquire other nonessential metals (Djingova & Kuleff, 2000).
The concentration of Pb in plant samples ranged from <0.001 at S4 to 36.72 mg/kg at S1. Tukey test revealed significant differences (p < 0.01) in the mean values of Pb between S1 and the other sites. The mean values recorded at all sites except S4, were above the FAO/WHO (1984) acceptable value of 0.43 mg/kg in edible plants. The high concentration of Pb in plant from the E-waste site could be attributed to the burning of lead containing products like scrap metals and batteries in the e-waste site. Livestock that graze in the e-waste area are likely to be exposed to health risks with regards to lead toxicity through the consumption of forage grasses growing in this area. Lead is reported to cause liver disorders in livestock especially in cattle. Khan, Khan, Hussain, Marwat, and Ashtray (2008) reported that lead causes both acute and chronic poisoning and thus, poses adverse effects on kidney, liver, vascular and immune system.
Cadmium concentrations recorded ranged from 0.25-1.64 mg/kg which was above the WHO/FAO (2007) permissible limit of 0.20 mg/kg for edible plants. Site S6 recorded the least concentration of Cd while the highest was recorded at S1. The high concentration of Cd at S1 might be as a result of the burning of e-waste containing cadmium-nickel batteries, pigments and paints. Significant concentration of Cd may have gastrointestinal effect and reproductive effect on livestock (Maobe, Gatebe, Gitu, & Rotich, 2012). Jabeen, Shah, Khan, and Hayat (2010) reported that cadmium causes both acute and chronic poisoning, adverse effect on kidney, liver, vascular and the immune system.
Similarly, the concentration of Cu ranged from 0.21 mg/kg at S3 and S6 to 95.56 mg/kg at S1.
With the exception of S3 and S6 which recorded mean Cu values that were below the FAO/WHO (1984) permissible limit of 3.0 mg/kg, the other sites recorded values that were above the limit. This could be attributed to continuous dumping of copper-containing electrical gadgets. In a similar study, Pradhan and Kumar (2014)  Additionally, concentration of Zn ranged from 1.33 at S6 to 34.92 mg/kg at S1. However, all the sites recorded mean values of zinc that were below the FAO/WHO (1984) permissible limit of 27.3 mg/kg except for S1. Zinc is required nutrient and becomes toxic to plants only at high concentrations.
Similarly, the concentration of chromium ranged from 1.08 at S3 to 3.84 mg/kg at S4, which was within the critical range of 5.00 to 30.00 mg/kg stated by Radojevic and Bushkin (2008).
The concentration of nickel also ranged from 0.59 at S6 to 6.80 mg/kg at S5. With the exception of S6, the remaining sites were above the WHO/FAO permissible limit of 1.63 mg/kg in edible plants. Nickel in plants could be attributed to cadmium-nickel batteries in the electrical gadgets and some paints used to polish the surfaces of the gadgets which might have spread to adjoining sites as it was also detected in the soil samples. High concentration of nickel can lead to health risks. According to Khan et al. (2008), Ni deficiency results in liver disorder.
The concentration of Sn ranged from 2.52 at S4 to 22.29 mg/kg at S6 which were all below the recommended FAO/WHO (1984) permissible limit of 200.00 mg/kg in edible plants.
Additionally, As ranged from below detection at S2 to 0.32 mg/kg at S1. The presence of As in the vegetation samples could be attributed to the recycling activities in the area. The concentration of As is in line with the findings of Pradhan and Kumar (2014) on Delhi informal re-cycling site. According to Luo et al. (2011) atmospheric deposition is a major factor for high metal accumulation in plant samples, and this could therefore be the cause of the As in the samples analysed.
The uptake of heavy metals by plants occur during the vegetative period (Knezevic et al., 2009;Krstić, Stanković, Igić, & Nikolic, 2007). The presence of toxic heavy metals in the soil results in the bio-accumulation and bio-magnification of these toxins into plant tissues (Fagbote & Olanipekun, 2010;Suciu, Cosma, Todica, Bolboaca, & Jantschi, 2008). animals sometimes graze around the area. The Informal recycling of e-waste also has the potential to pollute the environment and nearby communities. The need for periodic monitoring of toxic metals in this area is crucial to protect human health and the environment.

Recommendation
The occasionally to create awareness on the potential health risks they are exposed to. Herds of cattle crossing from nearby communities should be restricted from grazing on the forage grasses in the study area. Children should be restricted from playing within the recreational area since some levels of heavy metals were found in both the plant and soil sampled from the area. Farmers cultivating vegetables along the borders of the reclamation zones should be educated on the health risk consumers are expose to by consuming vegetable grown as the plants are likely to pick heavy metals from the polluted soil.

Competing interests
All authors declare no competing interests.