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See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/350975560 Heavy metal concentrations in soils and two vegetable crops (Corchorus olitorius and Solanum nigrum L.), their transfer from soil to vegetables and potential human health risks ass... Article in International Journal of Environmental Analytical Chemistry · April 2021 DOI: 10.1080/03067319.2021.1910251 CITATIONS 0 READS 279 8 authors, including: Some of the authors of this publication are also working on these related projects: Food and water security under climate change View project Contamination des eaux View project Amina Aboubakar Institute of Agricultural Research for Development 9 PUBLICATIONS 9 CITATIONS SEE PROFILE Souad El Hajjaji Mohammed V University of Rabat 122 PUBLICATIONS 772 CITATIONS SEE PROFILE Ahmed Douaik Institut National de la Recherche Agronomique 105 PUBLICATIONS 782 CITATIONS SEE PROFILE Jamal Mabrouki Mohammed V University of Rabat 34 PUBLICATIONS 34 CITATIONS SEE PROFILE All content following this page was uploaded by Amina Aboubakar on 31 May 2021. The user has requested enhancement of the downloaded file.

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Page 1: Heavy metal concentrations in soils and two vegetable

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/350975560

Heavy metal concentrations in soils and two vegetable crops (Corchorus

olitorius and Solanum nigrum L.), their transfer from soil to vegetables and

potential human health risks ass...

Article  in  International Journal of Environmental Analytical Chemistry · April 2021

DOI: 10.1080/03067319.2021.1910251

CITATIONS

0READS

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8 authors, including:

Some of the authors of this publication are also working on these related projects:

Food and water security under climate change View project

Contamination des eaux View project

Amina Aboubakar

Institute of Agricultural Research for Development

9 PUBLICATIONS   9 CITATIONS   

SEE PROFILE

Souad El Hajjaji

Mohammed V University of Rabat

122 PUBLICATIONS   772 CITATIONS   

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Ahmed Douaik

Institut National de la Recherche Agronomique

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Jamal Mabrouki

Mohammed V University of Rabat

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Page 2: Heavy metal concentrations in soils and two vegetable

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International Journal of Environmental AnalyticalChemistry

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Heavy metal concentrations in soils and twovegetable crops (Corchorus olitorius and Solanumnigrum L.), their transfer from soil to vegetablesand potential human health risks assessmentat selected urban market gardens of Yaoundé,Cameroon

Amina Aboubakar, Souad El Hajjaji, Ahmed Douaik, Yvette Clarisse MfopouMewouo, Raymond Charly Birang a Madong, Abdelmalek Dahchour, JamalMabrouki & Najoua Labjar

To cite this article: Amina Aboubakar, Souad El Hajjaji, Ahmed Douaik, Yvette Clarisse MfopouMewouo, Raymond Charly Birang a Madong, Abdelmalek Dahchour, Jamal Mabrouki & NajouaLabjar (2021): Heavy metal concentrations in soils and two vegetable crops (Corchorus�olitoriusand Solanum nigrum L.), their transfer from soil to vegetables and potential human health risksassessment at selected urban market gardens of Yaoundé, Cameroon, International Journal ofEnvironmental Analytical Chemistry, DOI: 10.1080/03067319.2021.1910251

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Page 3: Heavy metal concentrations in soils and two vegetable

Heavy metal concentrations in soils and two vegetable crops (Corchorus olitorius and Solanum nigrum L.), their transfer from soil to vegetables and potential human health risks assessment at selected urban market gardens of Yaoundé, CameroonAmina Aboubakara,b, Souad El Hajjaji a, Ahmed Douaik c, Yvette Clarisse Mfopou Mewouob, Raymond Charly Birang a Madongb, Abdelmalek Dahchoura, Jamal Mabrouki a and Najoua Labjard

aLaboratory of Spectroscopy, Molecular Modelling, Materials, Nanomaterials, Water and Environment (LS3MN2E), Department of Chemistry, Faculty of Science, Mohammed V University in Rabat, Rabat, Morocco; bLaboratory of Soil, Plant, Water and Fertilizer Analysis (LASPEE), Institute of Agricultural Research for Development (IRAD), Yaoundé, Cameroon; cResearch Unit on Environment and Conservation of Natural Resources, National Institute of Agricultural Research (INRA), Rabat, Morocco; dLaboratory of Spectroscopy, Molecular Modelling, Materials, Nanomaterials, Water and Environment (LS3MN2E), ENSAM, Mohammed V University in Rabat, Rabat, Morocco

ABSTRACTSoil contamination by heavy metals has received considerable attention in recent years. In this study, heavy metal accumulation in two vegetable crops (Corchorus olitorius and Solanum nigrum L.) was studied. Assessment of soil properties and seven heavy metals (Zn, Cu, Cd, Ni, Pb, Cr and Mn) in soils and vegetables was done. Heavy metal transfer from soil to plant parts, translocation from roots to leaves and estimated potential health risks of heavy metal to humans via consumption of vegetable crops were studied. The ANOVA test showed that variations in the soil characteristics and heavy metal concentrations were statistically significant at level 0.05. Pearson correlation coefficients showed that the concentra-tion of heavy metals has significant relationships with some soil properties like cation exchange capacity (CEC), organic carbon (OC) and soil texture. Bioconcentration factor (BCF) for both leaves and roots for Zn, Cu, Cd, Ni Cr and Mn were found to be greater than one, indicating the hyperaccumulation nature of vegetables. High translocation (TF) from root to leaves (TF>1) was recorded for Zn, Cu, Cd and Mn. The Health Risk Index (HRI) was found generally less than 1, suggesting that it is not risky for the Yaoundé city inhabi-tants to consume vegetable crops, except for Cd and Mn in Solanum nigrum L. Total Hazard Health Risk Index (THRI) expressed to know the overall harmful effects on health posed by several heavy metals taken together showed that the value for vegetables studied was higher than 1, suggesting the probability of adverse effects. The health risk is likely to occur for vegetable consumers.

ARTICLE HISTORY Received 8 February 2021 Accepted 18 March 2021

KEYWORDS Soil properties; bioaccumulation; bioconcentration factor; translocation factor

CONTACT Jamal Mabrouki [email protected]; Souad El Hajjaji [email protected]

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY https://doi.org/10.1080/03067319.2021.1910251

© 2021 Informa UK Limited, trading as Taylor & Francis Group

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1. Introduction

Urban and peri-urban agriculture can be defined as any form of agricultural production in or directly adjacent to the city, which mainly provides urban markets with food products for sale to consumers or for consumption by the city-dwelling farmers themselves [1]. Urban gardening is the urban agriculture sector characterised by vegetable production in the urban and suburban areas to satisfy the daily demand of urban populations. In fact, urban market gardening fulfils social, economic and environmental functions. It contri-butes to the city’s food supply and increases household income. Despite these universal advantages generally recognised in urban market gardening, this activity faces many constraints in Yaoundé [2]. Urban and peri-urban market garden is generally characterised by strong competition for land, elimination of fallow, continuous exploitation in limited space, overuse of fertilisers (organic and mineral), improper use of pesticides and irriga-tion with wastewater often containing dangerous toxic substances [3,4]. These practices can cause potential health and environmental hazards, such as the transfer of diseases by pathogens (e.g. diarrhoeal diseases) and the contamination of crops and soils by heavy metals and pesticides [5].

The origin of heavy metals in the soil can be natural or anthropogenic. Endogenous heavy metals constitute the natural pedogeochemical background. The natural concen-tration of these heavy metals in soils varies according to the nature of the source rock, its location, its age and natural phenomena [6]. Anthropogenic origins or exogenous sources of heavy metals are diverse. In urban agricultural soils, the pollution sources of heavy metals in environment are mainly derived from anthropogenic sources. These latter include traffic emission, industrial emission, domestic emission, weathering of building and pavement surface, atmospheric deposited, mining, smelting, waste disposal, urban effluent, vehicle exhausts, sewage sludge, pesticides, fertiliser application and so on [7,8]. The pollutants generated by human activity have a strong toxicological impact, and they have impacts on plant production, vegetable quality and human health. In his study [9], Sirven distinguished two types of heavy metal contamination due to human activity: Diffuse contamination from atmospheric pollution in the form of dust and aerosols from industrial activity, domestic heating, automobiles and punctual contamination, which can involve a large number of highly concentrated pollutants in localised areas. This is typically the case with agricultural activities. It introduces directly into the soil the various substances which are supposed to fertilise the soil (phosphate fertilisers rich in cadmium, sewage sludge containing most of the toxic metals, animal manure loaded with zinc, compost loaded with copper and so on) or get rid of harmful living organisms to crops (phytosanitary treatments) [4,5,10]. [11] reported that livestock manures and atmospheric deposition were the most important sources of Cu and Zn in agricultural soils. Whatever the origin of metals in the soil, excessive levels of many metals can cause a deterioration in soil quality, consequently poor quality of agricultural products. Vegetables grown in urban areas pose a high threat for consumers as they accumulate metal concentrations to a level that is harmful for living organisms [12].

The mobility of an element characterises its ability to move from one compartment of the soil to another. The more a substance moves in the soil, the more likely a living organism like plant will absorb it. However, a metal is toxic to living organisms only if it is in free form or if it is bioavailable [13]. Some elements, such as cadmium, thallium or zinc, are known to be

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very mobile, they are very soluble and therefore bioavailable while others, such as lead, mercury or chromium, are less mobile. It depends, on the one hand, on the fraction of the element that can be mobilised physico-chemically in the soil and, on the other hand, on the capacity of a given species to absorb it [14]. The mobility and bioavailability of heavy metals depends on several factors including physico-chemical parameters (acid-base and redox conditions, organic matter content, metal type and chemical forms, cation exchange capacity (CEC), pH, clay content, etc.) and biological activities [9,13,15]. The phyto- availability of an element results from several successive processes that contribute to the transfer of the element from the solid phase of the soil to the tissues of the different organs of the plant. Phyto-availability is influenced by factors related to soil, plant, soil microorgan-isms, climate and different farming techniques. Generally, the concentration of metals and metalloids in vegetables depends on soil texture as well as nature and type of plant species [16]. The levels are higher in the vegetative organs (leaves and stems) than in the repro-ductive organs (grains and fruits) [17].

The contamination of the soils with heavy metals can induce the accumulation of toxic contaminants in agricultural crops and thereby entrain to the human food chain [18]. Soils polluted with heavy metals in urban areas can directly affect public health. Indeed, leafy vegetables, which grow in polluted soils, store a significant amount of trace metals compared to those that grow in unpolluted soils [16]. For most people, the main route of exposure to toxic elements is through dietary intake [19], although inhalation of soil particles and dermal contact can play an important role in very contaminated sites [20]. Thus, information about heavy metal concentrations in food products and their dietary intake is very important for health risk assessment. Heavy metals are known to cause deleterious effects on human health. Excessive exposure to heavy metals has been shown to cause various diseases including cancer, brain and kidney damage, heart problems, liver dysfunction, damage to the reproductive system, memory impairment, even death and can cross the placental barrier, with potential toxic effects on the foetus [21,22].

In view of all the elements cited above, it is necessary to know if market gardening practised in urban and peri-urban areas does not involve accumulation of heavy metals in the natural ecosystem. The objective of this study was therefore to contribute to under-standing the dynamics of heavy metals in market gardening sites of Yaoundé, the capital city of Cameroon. More specifically, the aim was to determine the physico-chemical properties of market garden soils, to evaluate seven heavy metals (Zn, Cu, Cd, Ni, Pb, Cr and Mn) in soils and in two vegetable crops, Corchorus olitorius and Solanum nigrum, and finally to evaluate their transfer from soil to vegetables in order to understand the risks to the environment and human health. This work was carried out on two market garden sites located in the neighbourhood of Nkolondom and Nkolbisson.

2. Materials and methods

2.1. Study sites

The study sites are located in Yaoundé, the capital city of Cameroon. The relief of the city of Yaoundé is characterised by a set of hills and valleys with an altitude varying between 700 and 1200 m. The climate is hot and humid with two rainy seasons and two dry

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 3

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seasons. It is characterised by an average rate of annual rainfall of 1600 mm. The annual average temperature is estimated at 23.5°C [23].

This study was conducted between May and July 2015 in two market garden sites of Yaoundé located at Nkolondom and Nkolbisson (Figure 1). The location of the studied sites and their exact centroid coordinates (longitude and latitude in decimal degrees) were determined by the Global Positioning System (GPS) (Garmin, Etrex 20). The Nkolondom market garden site is located at a latitude of 3,954,541 and a longitude of 11,495,386. Nkolondom is attached to the commune of Yaoundé I. The market gardening site is located along a secondary road axis. The vegetables grown on this market garden site are delivered to the city markets. The lowlands of Nkolondom are crossed by run-off from the various hills [24,25]. The Nkolbisson market garden site is located at a latitude of 3,870,976 and a longitude of 11,455,889. Nkolbisson is attached to the commune of Yaoundé VII. The Nkolbisson lowlands are located in rural areas which are agricultural sites in contact with the outskirts. Market gardening activity is less intense compared with Nkolondom. This site supplies the Nkolbisson market with leafy vegetables [24,26].

These market gardens are heavily degraded by human activities. Most market gardeners do not have specific agricultural training. Market gardeners spread on the surface a large quantity of manure from poultry droppings and natural compost, in association with chemical fertilisers, such as urea, and compound fertilisers with nitrogen (N), phosphorus (P) and potassium (P). The majority of market gardeners use water from the city’s streams as the main resource for watering plants, specifically in dry seasons. These streams are polluted by the anthropogenic activities. The pesticides used are insecticides and fungicides [24].

2.2. Sampling and pre-treatment

On each market garden site, the studies were conducted on six cultivated plots, three plots for the same plant. Composite soil samples were collected at the surface (0–30 cm) and at depth (30–60 and 60–90 cm) on cultivated plots. Samples were taken after removing debris using stainless-steel auger. For each soil sample, five sub-samples were collected at distances of about 10 m from each other in different directions. The samples were mixed well in a bucket to form composite samples. Approximately 500 g of composite soil samples was placed in codified plastic bags and transported to the laboratory. The pre-treatment of soil samples was done in accordance with international standards [27]. The samples were air dried; roots and residues have been discarded. Dry soil samples were crushed and passed through a sieve (RETSCH) of 2 mm mesh, then preserved in clean sealed codified plastic bags for physico-chemical analysis. A portion of each soil sample was finely pulverised with laboratory porcelain mortar and pestle and sieved to 0.2 mm, then stored in codified plastic boxes.

Plants were collected at harvest, on the same plots where soil samples of cultivated plots were taken. For each plant, 3 plots at each site were the subject of the study. Two plants selected for our study are leafy vegetables: Corchorus olitorius commonly called ‘Keleng- Keleng’ or ‘Tegue’ or ‘Lalo’ in local languages and Solanum nigrum L. commonly called ‘Zom’ or ‘Njapche’ or ‘Bitossoh’ in local languages. Seven samples of each vegetable species were randomly selected on cultivated plots, to make one composite sample. The plants were slowly pulled out from the roots and transported to the laboratory. Once at the laboratory, the collected plants were washed thoroughly with distiled water. Plant samples were

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separated into leaves (edible parts) and roots, then, air-dried before drying in an oven (MEMMERT) at 40°C. Once dried, the samples were powdered using a grinder (RETSCH ZM 200) and stored in codified boxes for heavy metal analysis.

Figure 1. Location of the study area and sampling sites.

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 5

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2.3. Quality control

The analyses were carried out at the Laboratory of Soils, Plants, Water and Fertilisers (LASPEE) of the Institute of Agricultural Research for Development (IRAD), Yaoundé. Quality assurance for analysis in soil and plant samples was estimated by using blank, duplicate samples analysis, a check solution and standard reference materials supplied by Interprofessional Office of Analytical Studies (BIPEA) for soil and Wageningen Evaluating programmes for Analytical Laboratories (WEPAL) for pant. All chemicals used were of analytical reagent grade with high purity. All solutions were prepared with deionised water.

2.4. Physico-chemical soil analysis

All analyses were done according to international standards. The different analyses carried out were pH (H2O), organic carbon (OC), total nitrogen (N), cation exchange capacity (CEC) and soil texture. Soil pH(H2O) was determined in aqueous extract with a soil-to-water ratio of 1:5 (weight/volume) using a pH metre (Hanna Instrument) according to NF ISO 10390 standard [28]. Organic carbon was determined by the sulfochromic oxidation method by NF ISO 14235 [29]. Determination of total nitrogen (N) was performed by the modified Kjeldahl method (NF ISO 11261) [30]. According to NF X31-130 [31], the cation exchange capacity (CEC) of the soil was determined by extraction with 1.0 M ammonium acetate. Determination of the particle size distribution of soil particles (Pipet method) were performed by determination of five particle size classes: clays (0 to 2 µm), fine silts (2 to 20 µm), coarse silts (20 to 50 µm), fine sands (50 to 200 µm) and coarse sands (200 to 2000 µm) according to NF X31-107 [32].

2.5. Heavy metal analysis of soil and plant samples

Three grams of each soil and each plant samples were mineralised using aqua reguia (HNO3+ HCl) extraction method (NF ISO 11466) [33]. The suspensions were filtered into 50 ml volumetric flask using Whatmann filter paper and made up to mark with deionised water. The solutions were used to determine pseudo-total heavy metal concentrations using inductively coupled plasma optical emission spectrophotometer (ICP-OES) (Perkin Elmer Optima 8000DV).

The Optima 8000 ICP-OES is a dual view instrument, allowing for both axial and radial plasma measurements, which enables the measurement of high and low concentration samples in the same method. The use of compressed air as a shear gas removes the plasma tail plume, which eliminates many interferences and minimises the need for the addition of ionisation suppressants. The photons generated within the plasma are mea-sured by a highly sensitive photon detector, Charge-Coupled Device. The ICP-OES sample experiences temperatures estimated to be in the vicinity of 10,000 K. This results in atomisation and excitation of even the most refractory elements with high efficiency. ICP- OES has advantages in terms of detection and quantification limits as well as speed of analysis.

6 A. ABOUBAKAR ET AL.

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2.6. Bioconcentration and translocation factors

The bioconcentration factor (BCF) is defined as the ratio of the heavy metal concentra-tions in plants (roots or leaves) to those in the soil [15,34]. The translocation factor (TF) is the ratio of the heavy metal concentrations between one part and another part of the plant (i.e. between leaf and root) [10,35].

The BCF was determined by Equation (1):

BCF ¼Cplant

Csoil(1)

where Cplant and Csoil were the concentrations of heavy metals in plants (leaves or roots) and soil, respectively.

The TF was calculated according to Equation (2):

TF ¼Cleaf

Croot(2)

where Cleaf and Croot were the concentration of heavy metal in leaves (edible parts) and roots, respectively.

2.7. Estimated daily intake of metal and health risk index

The estimated daily intake (EDI) of metal for adults was determined by Equation (3) [8,36]:

EDI ¼Cleaf � Cfactor �Wfood

Bw(3)

where Cleaf is the concentration of heavy metal in leaf (edible part) which was converted with a factor (Cfactor) that is 0.085 for the conversion of fresh vegetables to dry weight; Wfood represents the daily average intake of food crops (0.527 kg/(person.day) [36]) and Bw is the body weight. In this study, the average body weight for adult was 58.9 kg according to life expectancy at birth for both sexes in Cameroon [37].

Health risk index (HRI) was evaluated to determine the risk of exposure to each trace metal via ingestion of vegetable crops. The value of HRI depends upon the daily intake of metals (DIM) and oral reference dose (RfD). HRI was calculated using Equation (4):

HRI ¼DIMRfD

(4)

RfD is an estimated per day exposure of metal to the human body that has no hazardous effect during lifetime. RfDs are based on 0.3, 0.04, 0.001, 0.02, 0.004, 1.5 and 0.14 mg. kg−1d−1 for Zn, Cu, Cd, Ni, Pb, Cr and Mn, respectively [38]. An HRI < 1 for any metal in vegetables means that consumer population faces a safety risk for health. However, HRI ≥ 1 does indicate a considerable health risk to the organisms consuming these vegeta-bles [8,16].

In order to know the overall harmful effects on health posed by several heavy metals, the HRIs calculated for each metal were summed and expressed in the form of the Total Hazard Health Risk Index (THRI) [39]. The estimation was demonstrated in Equation (5):

THRI ¼Xn

i¼1HRIi ¼ HRIZn þ HRICu þ HRICd þ HRINi þ HRIPb þ HRICr þ HRIMn (5)

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 7

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HRIi is the Health Risk Index for heavy metal i, and n is the total number of heavy metal studies. THRI < 1 indicates that the health risk is not significant, it is unlikely there will be obvious adverse effects, whereas THRI ≥ 1 indicates the probability of adverse effects, the health risk is likely to occur for vegetable consumers. When THRI ≥10, risk is considered high and chronic, the target population is exposed to considerable health risk [40,41].

2.8. Statistical analysis

The data were statistically analysed using Microsoft Excel 2016 (Microsoft Corp.) and IBM SPSS Statistics 21 (SPSS Inc.) software statistical package. Means and standard deviations were determined. Pearson’s correlation coefficients were performed. Moreover, analysis of variance (ANOVA) was conducted to determine the statistically significant differences between the soil’s parameters and heavy metal concentrations in arable soils, in leaves and in roots of plants studied and a probability of less than 0.05 was taken as the significance level. Significance was established at P < 0.05.

3. Results and discussion

3.1. Soil characteristics

The physico-chemical characteristics of market garden soils are presented in Table 1. Soil pH mean values varied from 4.45 to 5.97 on cultivated soils. pH is one of the factors which influence the bioavailability and the transport of heavy metal in the soil and heavy metals are generally more mobile at pH <7 [42]. The mean values of the pH of the cultivated topsoil (0–30 cm) were 5.14 and 5.97 at Nkolbisson and Nkolondom study sites, respec-tively. Therefore, heavy metal mobility and bioavailability are enhanced. When soil pH decreased, pronounced increases of heavy metal mobility and bioavailability were observed, thus enhancement of the uptake of heavy metals by plants and thereby the threat to human health need be concerned [10]. The mean values of Cation Exchange Capacity (CEC) were 8.92 and 9.54 cmol(+)/kg on Nkolbisson and Nkolondom sites, respectively. The mean CEC values were lower in the subsoil than topsoil at Nkolondom. CEC is an important characteristic related to organic matter and clay content in the soil that greatly influences the bioavailability of a metal in the soil [13]. [43] showed that over- or under-fertilisation by farmers without taking into account the available CEC

Table 1. Soil characteristics (Mean ± Standard deviation) of cultivated plots from the study area (N = 3 for each depth on each site).

Sites Nkolbisson Nkolondom

Depth (cm) 0–30 30–60 60–90 0–30 30–60 60–90

pH 5.14 ± 0.20 4.64 ± 0.29 4.45 ± 0.33 5.97 ± 0.40 5.87 ± 0.48 5.09 ± 0.06OC (g/kg) 14.60 ± 3.89 11.39 ± 2.21 8.84 ± 1.96 16.52 ± 5.67 8.33 ± 0.38 6.28 ± 1.24N (g/kg) 1.72 ± 0.09 1.27 ± 0.21 1.14 ± 0.14 2.26 ± 0.66 0.85 ± 0.10 0.83 ± 0.06CEC(cmol(+)/kg) 8.92 ± 0.22 7.60 ± 0.94 8.22 ± 2.62 9.54 ± 1.72 6.03 ± 1.22 4.98 ± 1.89Soil Texture C (%) 40.31 ± 2.58 42.67 ± 4.60 42.50 ± 7.55 23.75 ± 5.30 30.85 ± 0.54 35.65 ± 2.99

FSi (%) 7.44 ± 1.14 7.35 ± 0.21 8.28 ± 2.42 5.79 ± 0.59 6.94 ± 1.72 6.12 ± 1.41CSi (%) 5.25 ± 0.43 4.95 ± 0.45 4.92 ± 0.27 4.37 ± 1.00 4.34 ± 0.75 3.79 ± 0.86FSa (%) 23.55 ± 1.93 22.56 ± 3.26 21.85 ± 2.02 28.05 ± 2.13 24.25 ± 1.66 22.34 ± 1.81Csa (%) 23.45 ± 1.28 22.47 ± 1.41 22.45 ± 3.23 38.04 ± 4.14 33.63 ± 3.90 32.10 ± 3.81

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can affect the uptake of nutrients, crop growth and environmental pollution. The CEC is directly related to the capacity of adsorbing heavy metals since the adsorption behaviour depends on the combination of the soil properties and the specific characteristics of the element [44]. Nitrogen (N) and organic carbon (OC) contents decreased significantly with depth (Table 1). These parameters give information on the product’s humigenic potential, which makes it possible to judge the degree of evolution of the organic matter, that is to say its ability to decompose more or less rapidly in the soil [15]. The result shows that the soil texture was sandy clay. All the physico-chemical parameters (pH, CEC, OC and clay content) of the soils are factors that are known to influence the solubility and mobility of metal [13,15,42].

The two-way ANOVA test showed that variations in the soil characteristics and heavy metal concentrations were statistically significant due to site, plant and site × plant interaction at level 0.05. The conclusions were shown in Table 2. A very highly significant difference at level 0.001 was observed between the sites for pH and soil texture. This may be due to different agricultural practices by vegetable farmers between sites. Meanwhile, we observe significant differences between depths for all soil parameters analysed at level 0.001 for N (F = 21.774), at level 0.01 for pH (F = 9.081) and OC (F = 10.587) and at level 0.05 for CEC (F = 4.868).

3.2. Heavy metals in cultivated soils

The pollution sources of heavy metals in environment are mainly derived from anthro-pogenic sources. According to several studies, soil contaminated by heavy metals, even at low concentrations, through human activities, such as disposal of industrial waste, mining, smelting and agricultural practices (use sewage sludges, animal manure, agro- chemicals and inorganic fertilisers), can be a public health concern throughout the world [45–47]. The average concentrations of heavy metals in arable surface of agricultural soil (0–30 cm) of Nkolbisson site were 27.6, 6.7, 0.041, 11.9, 16.5, 16.3 and 1012.4 mg/kg for

Table 2. Results of the two-way ANOVA test for soil parameter concentrations in cultivated soils.

Soils parameters Site Depth Site x Depth

pH 34.952*** 9.081** 1.279OC (g/kg) 0.709 10.587** 1.173N (g/kg) 0.225 21.774*** 4.749*CEC (cmol(+)/kg) 3.321 4.868* 2.125Soil Texture C (%) 30.493*** 3.802 1.739

FSi(%) 4.287 0.302 0.585CSi(%) 7.464* 0.686 0.220FSa(%) 4.616 4.396* 1.320Csa(%) 61.676*** 1.960 0.949

Zn (mg/kg) 11.068** 4.596* 7.889**Cu(mg/kg) 21.225** 15.729*** 3.069Cd(mg/kg) 1.095 0.236 0.832Ni(mg/kg) 20.533** 1.922 3.981*Pb(mg/kg) 29.538*** 0.103 0.394Cr(mg/kg) 124.330*** 1.647 0.258Mn(mg/kg) 168.966*** 1.300 0.329

*** Level of significance: p < 0.001 ** Level of significance: p < 0.01 * Level of significance: p < 0.05

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Page 12: Heavy metal concentrations in soils and two vegetable

Zn, Cu, Cd, Ni, Pb, Cr and Mn, respectively. At Nkolondom site, the average concentra-tions at the same depth were, respectively, 27.5, 5.7, 0.071, 5.9, 10.9, 2.4 and 253.3 mg/kg for Zn, Cu, Cd, Ni, Pb, Cr and Mn, respectively. Table 3 presents a summary of the results obtained in arable surface soil (0–30 cm) in this study, compared to those obtained from other sites in Cameroon and Africa. The heavy metal contents were in the range of those found in cultivated soils in Libreville (Capital city of Gabon) [15] and in urban garden soils of Kano, Nigeria [4]. The values of heavy metal obtained at Yaoundé are consider-ably lower than those found in the agricultural soils of Ngaoundéré, Cameroon, pre-sented in Table 3 [42,48]. Cd concentrations for control soils are in ranges found at Shao (Kwara State, Nigeria) [49]. Maximum permissible limits, according to Canadian Environmental Quality Guidelines for the Protection of Environmental and Human Health [50], are also presented in Table 3. It reveals that all heavy metal concentrations in studied soils are below the maximum allowable concentrations in agricultural soils. However, Aboubakar et al. [24] presents the evidence that the surface soils of market garden soils in Yaoundé have been contaminated with heavy metals and the majority of soil samples had a high to very high level of ecological risk, mainly due to Cd. Although the concentrations were below the maximum allowable, even at low concentrations, non-essential heavy metals can cause damages for vegetables cultivated in this soils and for environment [45]. Figure 2 presents the total heavy metals in cultivated soils according to their depth in two studied sites.

According to the two-way ANOVA test presented in Table 2, the difference between sites for heavy metal concentrations in cultivated soils was very highly significant (P < 0.001) for Pb (F = 29.538), Cr (F = 124.330) and Mn (F = 168.966). This difference was very significant (P < 0.01) for Zn (F = 11.068), Cu (F = 21.225) and Ni (F = 20.533). For Cd, there is no significant difference between the sites. The average concentration was not significantly different between the depths of sampling for Zn, Cd, Ni, Pb, Cr and Mn, except for Cu, where the difference was highly significant (F = 15.729; P < 0.001) between depth and for Zn, where the difference is significant (F = 4.596; P < 0.05).

3.3. Correlation between soil properties and heavy metals

Correlation analysis provides an effective way to reveal the relationships among multiple variables. The Pearson correlation coefficients are shown in Table 4. Ni, Pb, Cr and Mn showed positive strong significant (P < 0.01) relationships with pH, clay and coarse silt. Indeed, Ni, Pb and Cd can show greater affinity with the soil at low pH [51]. In addition, the correlations between, on the one hand, Cu and, on the other hand, OC and N were highly significant (P < 0.01) and positive. Positive correlation was significant (P< 0.05) between CEC and Zn (0.501) and Cu (0.588). The high CEC content was responsible for the highest sorption capacity of Zn and Cu [52]. The physico-chemical properties of soils such as pH, CEC, OC and clay are parameters that are known to influence the solubility and mobility of heavy metals [15,42]. Very significant negative correlation was detected between pH and Ni (−0.593), Pb (−0.653), Cr (−0.610) and Mn (−0.659). However, the concentration of Cd showed weak correlation with soil properties in this study.

10 A. ABOUBAKAR ET AL.

Page 13: Heavy metal concentrations in soils and two vegetable

Tabl

e 3.

Hea

vy m

etal

con

cent

ratio

ns (m

g/kg

) fou

nd in

the

ara

ble

soils

of t

he s

tudy

site

s ve

rsus

oth

er A

fric

an c

ities

.Co

untr

y/Ci

tySi

te n

ame

Stat

istic

al p

aram

eter

sZn

CuCd

Ni

PbCr

Mn

Cam

eroo

n/

Yaou

ndé

This

stu

dy

Nko

lbis

son

Mea

n ±

SD

27.6

± 1

.16.

71 ±

0.7

10.

041

± 0

.014

11.9

± 1

.316

.5 ±

3.4

16.3

± 5

.310

12.4

± 1

95.9

Nko

lond

omM

ean

± S

D27

.5 ±

1.6

5.72

± 0

.17

0.07

1 ±

0.0

085.

9 ±

0.2

10.9

± 2

.92.

4 ±

0.6

253.

3 ±

12.

1

Cam

eroo

n/

Nga

ound

éré

[42]

Cam

p pr

ison

Mea

n ±

SD

380.

8 ±

5.3

99.8

0 ±

7.7

3.50

± 0

.49

31.0

3 ±

1.5

307.

2 ±

16.

3-

-N

orve

gien

Mea

n ±

SD

200.

1 ±

4.6

50.1

9 ±

4.3

2.92

± 0

.18

43.9

4 ±

1.7

99.3

8 ±

6.1

--

12 p

otea

uxM

ean

± S

D24

5.4

± 1

8.8

137.

25 ±

7.6

3.85

± 0

.11

40.8

5 ±

4.0

120.

7 ±

7.9

--

Sabo

ngar

iM

ean

± S

D48

4.6

± 1

1.1

81.4

9 ±

2.3

3.97

± 0

.03

47.1

1 ±

3.5

190.

9 ±

7.4

--

Cam

eroo

n/

Nga

ound

éré

[48]

Bali

Mea

n ±

SD

30.6

0 ±

3.5

410

.30

± 0

.28

nd24

.59

± 0

.01

17.5

1 ±

0.1

0-

191.

38 ±

2.0

1Sa

bong

ari

Mea

n ±

SD

164.

73 ±

8.7

119

.66

± 1

.23

0.02

± 0

.00

26.3

0 ±

1.3

053

.37

± 6

.00

-22

3.65

± 1

2.29

Nig

eria

/ M

oro

[49]

Shao

Mea

n ±

SD

64.5

± 0

.014

16.9

3 ±

0.0

010.

033

± 0

.003

7.17

± 0

.001

27.0

0 ±

0.0

0555

.33

± 0

.003

-

Nig

eria

/ Ka

no

[4]

Koki

Mea

n ±

SD

136.

2 ±

21.

0-

0.7

± 0

.2-

--

-Le

gal

Mea

n ±

SD

22.9

± 5

.7-

0.09

± 0

.01

--

--

Gab

on/

Libr

evill

e [1

5]-

Mea

n M

in –

Max

40.0

13

.9–7

9.2

21.5

8.

9–51

.4-

9.7

0.1–

26.8

375

99–1

351

Max

imum

per

mis

sibl

e lim

its [5

0]20

063

1.4

5070

64-

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 11

Page 14: Heavy metal concentrations in soils and two vegetable

Figure 2. Heavy metal concentration in cultivated soils of Nkolbisson and Nkolondom.

12 A. ABOUBAKAR ET AL.

Page 15: Heavy metal concentrations in soils and two vegetable

3.4. Heavy metals in plant parts

The concentrations of heavy metals, on a dry weight basis, in the edible part of Corchorus olitorius ranged across the two sites from 35.2 to 45.6 mg/kg for Zn, from 14.1 to 27.8 mg/ kg for Cu, from 0.2 to 0.3 mg/kg for Cd, from 6.1 to 18.8 mg/kg for Ni, from 0.1 to 0.3 for Pb, from 1.1 to 3.9 mg/kg for Cr and from 82.2 to 139.6 mg/kg for Mn. While in roots it ranged from 33.2 to 45.8 mg/kg for Zn, from 6.4 to 15.4 mg/kg for Cu, from 0.1 to 1.1 mg/kg for Cd, from 16.4 to 35.8 mg/kg for Ni, from 1.1 to 6.5 mg/kg for Pb, from 1.4 to 7.3 mg/kg for Cr and from 69.2 to 177.8 mg/kg for Mn. For Solanum nigrum, the concentrations of heavy metal ranged across the studied sites in the leaves from 40.1 to 58.8 g/kg for Zn, 4.9 to 10.5 mg/kg for Cu, 0.1 to 2.0 mg/kg for Cd, 8.4 to 26.9 mg/kg for Ni, 0.1 to 1.0 mg/kg for Pb, 0.6 to 6.5 mg/kg for Cr and 239.5 to 653.5 mg/kg for Mn. While in roots, it ranged from 21.9 to 36.3 mg/kg for Zn, 3.7 to 6.6 mg/kg for Cu, 0.4 to 2.3 mg/kg for Cd, 16.5 to 27.6 mg/kg for Ni, 1.3 to 3.9 mg/kg for Pb, 2.0 to 5.5 mg/kg for Cr and 102.4 to 130.1 mg/kg for Mn. Heavy metal concentration (mean ± standard deviation) in two vegetables, Corchorus olitorius and Solanum nigrum, are presented in Table 5. There were large differences between the roots and leaves concentrations of heavy metals among the vegetables studied, which indicated an important restriction of the internal transport of metals from roots towards leaves [34].

The results show that plants have different trace element accumulation capacity. Vegetabes can take up metals in various amounts [53]. There are no standard limits on heavy metal contents in plants in Africa. However, the normal content of heavy metals in plants as given by [17] are 50 mg/kg for Zn, 10 mg/kg for Cu, 0.05 mg/kg for Cd, 1.5 mg/kg for Ni, 1.0 mg/kg for Pb, 1.5 mg/kg for Cr and 200 mg/kg for Mn.

The concentration values for Zn were slightly elevated (>50 mg/kg) only in Solanum nigrum leaves. Zinc is an essential trace metal for humans and it is necessary for the function of various enzymes in which it plays catalytic, structural and/or regulatory roles. Nonetheless, at excessive intake, Zn can be toxic and lead to either lung or intestinal tract symptoms [54].

Higher mean concentration than normal values for Cu (>10 mg/kg) was observed in the leaves and roots of Corchorus olitorius regardless of the sampling site. The average concentration of Cu obtained in Corchorus olitorius leaves by [30] at Ngaoundéré market

Table 4. Pearson correlation coefficients between heavy metals and soil properties.Zn Cu Cd Ni Pb Cr Mn

pH −0.329 −0.120 0.200 −0.593** −0.653** −0.610** −0.659**OC 0.408 0.625** 0.159 −0.198 0.146 0.274 0.235N 0.466 0.640** 0.222 −0.313 0.120 0.145 0.162CEC 0.501* 0.588* 0.260 0.045 0.306 0.384 0.357C 0.337 0.152 −0.081 0.807** 0.666** 0.712** 0.647**FSi −0.004 0.042 −0.390 0.261 0.511* 0.345 0.445CSi 0.248 0.445 −0.136 0.328 0.614** 0.529* 0.563*FSa −0.120 0.222 0.000 −0.640** −0.358 −0.398 −0.306CSa −0.368 −0.326 0.193 −0.768** −0.805** −0.797** −0.785**

OC: Organic Carbon; CEC: Cation Exchange Capacity; C: Clay; FSi: Fine Silt; CSi: Coarse Silt (CS). FSa: Fine Sand and CSa: Coarse Sand.

**The correlation is significant at the 0.01 level *The correlation is significant at the 0.05 level

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 13

Page 16: Heavy metal concentrations in soils and two vegetable

Tabl

e 5.

Hea

vy m

etal

con

tent

s (m

g/kg

) in

leav

es a

nd r

oots

of t

he t

wo

stud

ied

plan

ts.

Site

sPl

ants

Part

sZn

CuCd

Ni

PbCr

Mn

Nko

lbis

son

Corc

horu

s ol

itoriu

sLe

aves

39.9

51 ±

5.0

0820

.994

± 6

.578

0.28

1 ±

0.0

478.

613

± 2

.481

0.16

1 ±

0.0

561.

562

± 0

.618

111.

357

± 2

5.22

6Ro

ots

39.8

17 ±

6.3

3013

.781

± 2

.373

0.59

1 ±

0.4

8926

.846

± 9

.825

5.35

3 ±

0.9

941.

802

± 0

.384

171.

400

± 6

.618

Sola

num

nig

rum

Leav

es44

.766

± 5

.753

9.31

0 ±

1.0

721.

351

± 0

.614

9.37

6 ±

1.3

610.

792

± 0

.206

0.97

7 ±

0.3

0345

1.71

5 ±

190

.878

Root

s29

.522

± 7

.257

4.06

2 ±

0.3

091.

948

± 0

.336

22.0

50 ±

5.5

432.

503

± 1

.354

2.27

1 ±

0.4

0311

1.65

7 ±

9.2

45N

kolo

ndom

Corc

horu

s ol

itoriu

sLe

aves

40.5

36 ±

4.9

8715

.298

± 1

.043

0.28

2 ±

0.0

1812

.726

± 5

.241

0.27

5 ±

0.0

343.

445

± 0

.529

122.

107

± 2

5.48

0Ro

ots

40.9

03 ±

2.5

967.

663

± 1

.122

0.17

7 ±

0.0

6522

.903

± 3

.468

1.42

7 ±

0.4

907.

003

± 0

.285

75.8

63 ±

5.9

13So

lanu

m n

igru

mLe

aves

50.5

23 ±

8.2

276.

158

± 1

.215

0.07

9 ±

0.0

1921

.557

± 4

.619

0.15

1 ±

0.0

455.

189

± 1

.300

295.

660

± 4

9.14

9Ro

ots

32.3

39 ±

3.1

145.

809

± 0

.867

0.48

6 ±

0.1

0123

.905

± 3

.914

1.88

3 ±

0.3

944.

856

± 0

.584

117.

010

± 1

2.80

2N

orm

al c

onte

nt in

pla

nt(a

)50

100.

051.

51

1.5

200

Mea

n ±

sta

ndar

d de

viat

ion

(a) [1

7]

14 A. ABOUBAKAR ET AL.

Page 17: Heavy metal concentrations in soils and two vegetable

gardens was less than our results. Cu can be chronically toxic. Its role in carcinogenesis was often mentioned [17].

The concentration of Cd in leaves and roots was higher than the limit value (>0.05 mg/ kg). Cd is a ubiquitous trace metal in the environment; it is one of the pollutants of great concern and is considered to be a human carcinogen [54].

Concentrations of Ni found in the present study were remarkably high for all plant samples if compared to their normal concentration values (1.5 mg/kg). Nickel is a ubiquitous trace metal in the environment. Ni is an essential micronutrient for human beings; it is also a growth factor. But excessive intake may affect health; it can be toxic in high doses [17,55].

The results showed that Pb concentrations in the roots of the two vegetables are significantly higher than the normal value (>1.0 mg/kg). The Pb concentrations in the leaves are lower than the normal values. The average concentration of Pb obtained in Corchorus olitorius leaves by [48] at Ngaoundéré market gardens was higher than our results.

The leaf samples of the two vegetables from Nkolbisson showed lower values of Cr compared to their normal content, while the roots of these plants had higher values (>1.5 mg/kg). At the Nkolondom site, all the samples showed very high values for Cr, both in the roots and in the leaves. It is clear from the results that the plants grown on Nkolondom site accumulate high level of Cr in their edible parts as compared to those plants that grown on Nkolbisson. Concentrations of Cr in plants vary widely for kinds of tissues and stages of growth, and the trend in Cr variation can be irregular [56] according to the different parts of the plant and the species.

Higher concentrations than normal values for Mn (>200 mg/kg) were observed only in the leaves of Solanum nigrum regardless of the agricultural site. Generally, Mn is known to be rapidly taken up and translocated within plants. An excess of phytoavailable Mn is associated with several soil properties, such as strong acidity of soils, aerobic condition and poor aeration (flooded, waterlogged, or compact soils) [56]. However, Mn appeared to have a low mobility when the supply of the plant was limited. Mn uptake is metabo-lically controlled. In this study, Mn concentration fluctuates greatly within the plant parts according to the vegetable species.

Table 6 presented the results of the three-way ANOVA test for heavy metal concentra-tions in plants. The three-way ANOVA test showed that the difference of means concen-trations in plants was significant between the sites for Cd (F = 39.799), for Pb (F = 23.668), for Cr (F = 182.038) at level P < 0.001 and for Cu (F = 9.581) at level P < 0.01. Between the

Table 6. Results of the three-way ANOVA test for heavy metal concentrations (mg/kg) in plants.Metals Zn Cu Cd Ni Pb Cr Mn

Site 1.212 9.581** 39.799*** 2.864 23.668*** 182.038*** 4.111Plants 0.190 57.546*** 25.739*** 0.478 3.279 0.255 18.189**Parts 12.720** 22.918*** 5.874* 26.771*** 88.069*** 21.392*** 18.901***Site x Plants 0.550 5.942* 21.644*** 2.728 5.985* 0.078 0.322Site x Parts 0.069 1.098 1.466 4.795* 14.861** 2.704 0.225Plants x Parts 13.079** 4.691* 2.564 2.544 7.733* 7.611** 21.024***Site x Plants x Parts 0.137 1.552 0.202 0.073 15.166** 23.118*** 5.313*

*** Level of significance: p < 0.001 ** Level of significance: p < 0.01 * Level of significance: p < 0.05

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 15

Page 18: Heavy metal concentrations in soils and two vegetable

plants, the difference was significant for Cu (F = 57.546; P < 0.001), Cd (F = 25.739; P < 0.001) and Mn (F = 18.189; P < 0.01), whereas there is significant difference for all heavy metals; for Cu (F = 22.918), for Ni (F = 26.711), for Pb (F = 88.069), for Cr (F = 21.392) and for Mn (F = 18.901) at level P < 0.001; for Zn (F = 12.720) at level P < 0.01 and for Cd (F = 5.874) at level P < 0.05.

The application of livestock manure containing high concentrations of heavy metals may cause crop toxicity and environmental risk [46]. Nkolbisson and Nkolondom market gardeners overuse chemical fertilisers and organic fertilisers, in particular, chicken man-ure. This livestock manure used is not pre-tested before the application in market garden soils. Fertilisers were the major sources of heavy metals to agricultural lands [4].

3.5. Heavy metal transfer from soil to vegetables

The heavy metal accumulation from soil to plant did not follow any particular pattern and varied with respect to each metal, plant species, plant parts and uptake capabilities. Figure 3 presents the distribution of BCF in Corchorus olitorius and Solanum nigrum plants. BCF values of different heavy metals showed large variations in the two vegetables.

The lower BCF was found in all parts of the two vegetable species for Pb with values ranging from 0.008 to 0.057 in leaves and from 0.072 to 0.374 in roots. Indeed, some metals, such as Pb, have very low solubility in soils and show a particularly strong barrier. Even if they accumulate at the root, they are not usually translocated significantly to the leaves [34].

Higher BCF mean values (>1) in the edible parts (leaves) were recorded for Zn (1.45 for Corchorus olitorius and 1.62 for Solanum nigrum), for Cu (3.09 for Corchorus olitorius and 1.40 for Solanum nigrum) and for Cd (7.62 for Corchorus olitorius and 38.08 for Solanum nigrum) on Nkolbisson site. For Ni, Pb, Cr and Mn, the BCF mean values were low (BCF<1) for both vegetables, while, in the roots, at the same site, higher BCF mean values were recorded for Zn (1.45 for Corchorus olitorius and 1.07 for Solanum nigrum), Cu (2.09 for Corchorus olitorius), Cd (13.68 for Corchorus olitorius and 52.45 for Solanum nigrum) and Ni (2.26 for Corchorus olitorius and 1.86 for Solanum nigrum). For Cu (only for Solanum nigrum), Pb, Cr and Mn, BCF mean values were low (BCF < 1). On Nkolondom site, in the edible parts of vegetable (leaves), mean BCF values were high (BCF > 1) for Zn (1.48 for Corchorus olitorius and 1.85 for Solanum nigrum), Cu (2.68 for Corchorus olitorius and 1.07 for Solanum nigrum), Cd (3.99 for Corchorus olitorius and 1.13 for Solanum nigrum), Ni (2.15 for Corchorus olitorius and 3.61 for Solanum nigrum), Cr (1.45 for Corchorus olitorius and 2.18 for Solanum nigrum) and Mn (1.16 only in Solanum nigrum). BCF mean values were low (BCF < 1) for Mn (only in Corchorus olitorius) and Pb in both vegetables whereas, in the roots, the mean values of BCF were 1.49 Corchorus olitorius and 1.18 for Solanum nigrum for Zn, 1.33 Corchorus olitorius and 1.01 for Solanum nigrum for Cu, 2.51 Corchorus olitorius and 6.95 for Solanum nigrum for Cd, 3.85 Corchorus olitorius and 4.02 Solanum nigrum for Ni, 3.01 Corchorus olitorius and 2.11 for Solanum nigrum for Cr. The BCF mean values were low (BCF < 1) for Pb and Mn.

The leaves of plants cultivated at the two sites studied accumulate Cu, unlike the roots; this is more pronounced for Corchorus olitorius. This is in agreement with the studies of [57], which shows that Cu was accumulated more in leaves than roots for amaranth and roselle. This accumulation of Cu in the leaves can be associated with the use of Cu-based

16 A. ABOUBAKAR ET AL.

Page 19: Heavy metal concentrations in soils and two vegetable

pesticides [58]. Accumulation of Ni and Cr is very observable on Nkolondom site. The greater value of BCF indicates a higher accumulation potential of heavy metals in vegetables, the results indicate that Cd has higher capacity for transferring from soil to the edible parts of vegetables than other heavy metals. The high BCF mean values for Cd were also obtained by [48] in Corchorus olitorius. The higher concentrations of heavy

Figure 3. Bioconcentration factor (BCF) of heavy metal in Corchorus olitorius and Solanum nigrum plants.

INTERNATIONAL JOURNAL OF ENVIRONMENTAL ANALYTICAL CHEMISTRY 17

Page 20: Heavy metal concentrations in soils and two vegetable

metals in a plant can be explained by heavy metal accumulation due to the uptake process [59]. Indeed, heavy metal movement and accumulation in vegetable tissues can be strongly influenced by multiple factors, including high levels of heavy metals in soil, soil properties, plant factors, soil morphology and other environmental conditions [51,60].

3.6. Heavy metal translocation from root to leaves

The physiology of the plant regulates the transfer to the edible part of the plant. Several types of transporter proteins are involved in the root-to-shoot transport of metals. Once taken up by the roots, metal ions are loaded into the xylem and phloem tissues, then transported to the shoots as complexes by two ways known as apoplastic/passive transportation and symplastic/active transportation [8,56]. High translocation factors (TF>1) was recorded in Corchorus olitoriusfor Cu (1.62 at Nkolbisson and 2.03 at Nkolondom) and Cd (1.41 at Nkolbisson and 1.82 at Nkolondom) (Table 7). Similarly, TF was found >1 in Solanum nigrum for Zn, Cu and Mn. These heavy metals (Zn, Cu and Mn) translocated from source to sink tissue via sap, which contains metals arising [61]. The lowest TF was observed in the two vegetable species for Ni, Pb and Cr. The results confirm that Pb is not usually translocated significantly to the leaves [56]. Showed that the translocation from the root to the growth of Cr was quite limited due to the propensity of Cr to bind to the cell walls of the roots. The contamination and accumulation of heavy metal in the edible part of tested vegetable crops are unsafe for consumption [34].

3.7. Human health risk assessment

There are several exposure pathways that mainly depend on contaminated sources of air, water, soil, food and consuming population, but the path of exposure via food chain is one of the key pathways of heavy metal exposure to human [36]. High absorption of heavy metals by vegetables can indicate high dietary intake of toxic metals by human [59]. Vegetable crops presented in the present study are consumed in daily diet by the local inhabitants of Yaoundé. Table 8 shows the mean results for DIM and HRI evaluation. According to the results, the HRI value of each metal is less than 1, suggesting intake of a single metal through consumption of both vegetables did not pose a significant potential health hazard. The only exceptions are Cd and Mn in Solanum nigrum, where the highest HRI values (HRI > 1) were observed. This indicates a possible future human health risk via food crops intake. The HRI of exposed population is dependent on various factors, such as heavy metal concentrations, exposure time and per capita consumption of food products, body weight and toxicity of each element [39]. In the study of [48], HRI values for Pb (0.74) in Corchorus olitorius were higher than the values obtained in this study. Cd is considered as a non-essential metal contributing to the health hazards even at

Table 7. Translocation factor of heavy metal from roots to leaves.Sites Plants Zn Cu Cd Ni Pb Cr Mn

Nkolbisson Corchorus olitorius 1.035 1.615 1.410 0.352 0.030 0.955 0.651Solanum nigrum L 1.553 2.288 0.691 0.543 0.427 0.494 1.598

Nkolondom Corchorus olitorius 0.992 2.029 1.815 0.455 0.202 0.453 4.099Solanum nigrum L 1.564 1.071 0.162 0.943 0.087 1.091 2.543

18 A. ABOUBAKAR ET AL.

Page 21: Heavy metal concentrations in soils and two vegetable

very low level [36]. The presence of Cd is a major cause of concern due to its high mobility and tendency to readily accumulate in vegetables. Dietary intake of metals through contaminated vegetables may cause various chronic diseases [8].

The risk of contaminants for human health is dependent on various factors, such as per capita consumption of foodstuff, exposure time, toxicity and body weight [62]. The results of THRI showed that the value was higher than 1 but lower than 10 in two market garden studied sites (Table 8). This suggests that adverse health effects are not considered high for the exposed population but indicates the probability of adverse effects, the health risk is likely to occur for vegetable consumers. The present study is very important in terms of perspectives of potential health risk evaluation to the human population from heavy metal ingestion by vegetable consumption. The projects of control and reduction of heavy metal levels in urban agricultural soil should be implemented.

4. Conclusion

This study was conducted in order to assess the physical and chemical properties of soils and to evaluate heavy metal accumulation in vegetables grown on market garden fields at Yaoundé City. The results show that significant correlation was detected between soil properties and heavy metals. The vegetable crops (Corchorus olitorius and Solanum nigrum) accumulate and translocate variable amounts of metals from the soil by different extents to their roots and leaves. The vegetable species grown at the Nkolbisson and Nkolondom sites showed high accumulation and trans-location of heavy metals (Cd, Zn and Ni) in the edible parts. Although Pb accumu-lates at the root, it is not translocated significantly to the leaves. High HRI values (HRI>1) were also observed for Cd and Mn consumption in Solanum nigrum. THRI expressed to know the overall harmful effects on health posed by several heavy metals showed that the value was higher than 1, suggesting the probability of adverse effects. The health risk is likely to occur for vegetable consumers. This study gives a brief insight into the current scenario of vegetable crops contamination in market gardens. It is evident that heavy metals can pose a potential risk to the

Table 8. Mean Daily Intake of Metals (DIM) (mg/(kg.day)), mean Health Risk Index (HRI) for each heavy metal in vegetable crops and Total Health Risk Index (THRI) for all heavy metals in vegetable crops.

DIM

Site Plants Zn Cu Cd Ni Pb Cr Mn

Nkolbisson Corchorus olitorius 0,0304 0,0160 0,0002 0,0066 0,0001 0,0012 0,0847Solanum nigrum 0,0340 0,0071 0,0010 0,0071 0,0006 0,0007 0,3435

Nkolondom Corchorus olitorius 0,0308 0,0116 0,0002 0,0097 0,0002 0,0026 0,0929Solanum nigrum 0,0384 0,0047 0,0001 0,0164 0,0001 0,0039 0,2249

HRI

Site Plants Zn Cu Cd Ni Pb Cr Mn THRI = ∑HRI

Nkolbisson Corchorus olitorius 0,1013 0,3992 0,2140 0,3275 0,0306 0,0008 0,6049 1,6783Solanum nigrum 0,1135 0,1770 1,0272 0,3565 0,1505 0,0005 2,4539 4,2791

Nkolondom Corchorus olitorius 0,1028 0,2909 0,2144 0,4839 0,0523 0,0017 0,6633 1,8093Solanum nigrum 0,1281 0,1171 0,0599 0,8197 0,0286 0,0026 1,6061 2,7621

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local consumer of these two vegetable crops. Consequently, some effective measures may be necessary to manage heavy metal contamination in soil and to reduce metal translocation from soil to edible crops. In addition, this study may be useful in order to pursue in-depth studies to control heavy metal contamination of soils and vege-tables grown in urban areas and their implications for environmental health.

Acknowledgments

This research was supported by the Institute of Agricultural Research for Development (IRAD). The authors gratefully especially thank the Laboratory of Soil, Plant, Water and Fertilizer (LASPEE) (Yaoundé, Cameroon) for providing facilities and resources.

Disclosure statement

No potential conflict of interest was reported by the author(s).

ORCID

Souad El Hajjaji http://orcid.org/0000-0003-1467-704XAhmed Douaik http://orcid.org/0000-0001-7374-4674Jamal Mabrouki http://orcid.org/0000-0002-3841-7755

Author contributions

Amina Aboubakar performed conceptualisation, data collection, sample analysis and data analysis and wrote the first original draft of the manuscript. Yvette Clarisse Mewouo Mfopou supervised the data collection, laboratory analysis and provision of materials and reagents. Raymond Charly Birang a Madong and Najoua Labjar contributed to project administration. Ahmed Douaik and Jamal Mabrouki contributed to data analysis. Souad El Hajjaji and Abdelmalek Dahchour supervised and validated the research activity and review the final paper. All the authors commented on previous versions of the manuscript, read and approved the final manuscript.

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