Determination of levels of organochlorine pesticide residues in some common grown and consumed vegetables purchased from Ho Municipal markets, Ghana

Abstract

Using gas chromatography—electron capture detector protocol, pesticide residue levels on four common vegetables (cabbage, carrot, lettuce, and tomatoes) consumed in Ho Municipal, Ghana, were investigated. A total of 5 kg each of the vegetables were randomly sampled in triplicate and from three different markets. Organochlorine pesticides, including residues of γ-HCH, δ-HCH, heptachlor, aldrin, p, p’-DDT, o, p’-DDT and p, p’-DDE detected in vegetables sampled were above recommended EU MRL. Lettuce recorded the highest aldrin (1.23 mg/kg) as well as γ-HCH (0.013 mg/kg) residue levels, while heptachlor (1.05 mg/kg) and δ-HCH (0.23 mg/kg) were highest for cabbage. Maximal residues of p, p’-DDT (1.194 mg/kg) and p, p’-DDE (0.147 mg/kg) were found in tomatoes. Though consumption of these vegetables does not currently pose significant health risk to both adults and children, consumers should be careful as residues could accumulate and pose chronic health hazards. Hence, there is a need for constant surveillance to regulate pesticide use in vegetable farming.

Keywords:

• Vegetables
• Organochlorine pesticides
• Gas chromatography
• Pesticide residue
• Maximum residue level
• Health risk
• Market

1. Introduction

The regular consumption of fruits and vegetables is established to promote good health, as well as boost immunity against various forms of diseases that affect humans. The improved availability of fruits and vegetables on the supermarket shelves all year round has contributed to the satisfaction of the needs of consumers. The United Nations Food and Agricultural Organization (FAO) projected that, by the year 2030, global population would surpass eight billion (United Nations, 2015). As global population is fast-growing, it is critical to make all efforts to increase crop production and to ensure food security and sufficiency (Zhang, 2008). To achieve this target, farmers need to adopt and use modern and safe methods of food production. Using inorganic farming inputs like fertilizers and pesticides are some ways of boosting production. However, the lack of strict regulations surrounding the selling and application of these farming inputs, especially pesticides, has allowed most farmers to continuously apply wrong doses or even banned chemicals in the management of pests and diseases during the cultivation of vegetables for human consumption.

Pesticides usage has been intensified recently due to its rapid results in killing pests reduced toxicity, and less labour-intensive application methods compared to other methods of pest management. However, the undesirable impact of these pesticides on the environmental quality and health of humans constitutes the main course of concerns locally, regionally, nationally, and globally (Ntow, 2001). Most farmers do not adhere to harvest intervals when applying pesticides; as a result, raw vegetables become contaminated with pesticide residue (Ntow et al., 2006). The regulations on pesticide maximum residue level (MRL) have been established and documented in many countries, nevertheless, these regulations have not been fully implemented and enforced in such countries (Ambrus & Yang, 2016; MacLachlan & Hamilton, 2010). Most vegetables sold in markets and supermarkets contain pesticide residues resulting from the unregulated use of pesticides in vegetable cultivated fields, culminating in harmful effects on human health (Chowdhury et al., 2011).

The key concerns of pesticides are their lethal effects on poor development of the foetus (Gilden et al., 2010) and parent reproductive health, prominent in underdeveloped countries (Aktar et al., 2009). A recent analysis of pesticide contamination on vegetable farmers located in Ghana discovered that, organochlorine pesticide (OCP) residues, including DDT, were present in their breast milk and blood (Northern Presbyterian Agricultural Services and Partners, 2012). The immense benefits of vegetables to human health have made it important to guarantee product safety by dealing with common fields of concern including growing, pest control, harvesting activity, sorting, packing, storage, as well as distributing fresh produce. OCPs are synthetic products generally used worldwide. They are chlorinated hydrocarbon derivatives, often used in the chemical and agriculture industries. These compounds are well known for degrading slowly, their high toxic levels, and bioaccumulation (Jayaraj et al., 2016).

There is although evidence of continuous use in the Ghanaian community of OCPs and their presence in vegetables, despite its ban (Kumah et al., 2014). Additionally, a recent study on fruits and vegetables retailed in some markets in Ghana revealed that 51% of the samples analyzed gave results of traces of pesticide residues with 9.8% of the samples containing pesticide residues exceeding the MRL (C. K. Bempah et al., 2011). Reports on routine surveys and monitoring programs on pesticide residue levels on sold vegetables in the Ho Municipality of Ghana are lacking. Hence, this study aims at investigating the levels of OCP residues in cabbage, carrot, lettuce, and tomatoes retailed in three different markets of Ho municipality. The study will make available scientific data on pesticide residues on vegetables for the municipal agricultural authority and other concerned agencies to step up the management and control of pesticide use, to improve the quality of vegetables production, marketing, and consumption.

2. Materials and methods

2.1. Study location

The research was undertaken in the Volta region of Ghana. The region has an overall land size of 20,572 km² (2021). Sampling was done in the Ho municipality of the region in three different locations (Figure 1). The Municipality has an estimated population of 177,281 representing 8.4% of the region’s total population (Ghana Statistical Service GSS, 2010).

Figure 1. District map of Ho Municipal showing the sampling sites. Source: 2010 population and housing census, District analytical report, (Ho Municipality) (Ghana Statistical Service GSS, 2010).

2.2. Sampling method

Four (4) ready-to-eat fresh vegetables (cabbage, carrot, lettuce, and tomatoes) weighing 5 kg each, were sampled in triplicate from wholesalers (Market Queens) in three (3) different market locations (Ho Central, Ho Dome, and Shia). Market queens were carefully selected to ensure vegetables were not coming from the same sources to prevent bias. The experimental layout was a completely randomized design (CRD) with a 4 × 3 factorial arrangement with three (3) replications. All samples were carefully collected, sealed in sterile bags, and labelled before placing them in an ice box, and moved to the chemistry laboratory of the Ghana Atomic Energy Commission (GAEC) for analysis.

2.3. Pesticide analysis

2.3.1. Sample preparation

Analysis of pesticide residue was conducted using the gas chromatography method and fresh vegetable samples were prepared using the method described by Bempah et al. (C. Bempah et al., 2012). Accordingly, samples of fresh vegetables were completely grated and blended, and 20 g of these samples were macerated using 40 ml of ethyl acetate. Next was, the addition of sodium bicarbonate (5 g) as well as anhydrous sodium sulfate (20 g), to eliminate moisture before further maceration for three (3) minutes with the Ultra-Turrax macerator type T 25 generator. For the attainment of the two (2) phases, centrifugation of samples were done for five (5) minutes at 3,000 rpm. Finally, transferring of supernatant into an uncontaminated graduated cylinder (25 ml) was undertaken for measurement of its volume.

2.3.2. Solid-phase extraction

A solid-phase extraction (SPE) was done employing the SPE column in accordance with the Netherland analytical method of pesticide residues and foods but modified (Ministry of Public Health, Welfare and Sports, Netherlands, 2007). Thus, the florisil column (500 mg/8 ml) cartridge was conditioned using 5 ml of a mixed solution comprising acetone: n-hexane (3:7 v/v) in the column. The insoluble mixtures were not permitted to dry throughout the conditioning and sample loading stages. The extract column was fitted using a 20-port vacuum manifold that has a flask positioned under the column for collection of the eluate. Loading of sample was accomplished under vacuum at 5 milliliter per minute flow rates. Following the passing of extracts, drying of the column was achieved by suction aspiration in an expanded vacuum for half an hour. The pesticides were eluted using 10 (3, 3, 4) milliliter of ethyl acetate, later concentrated until 1 milliliter employing rotary evaporator, before drying by utilizing a mild nitrogen stream. It was then dissolved in 1 ml of ethyl acetate, after which a gas chromatograph comprised an electron capture detector (GC-ECD) was utilized to quantify the pesticides.

2.3.3. Gas chromatography analysis

Gas chromatography analysis was performed following the technique described by Bempah et al. (C. Bempah et al., 2012). Hence, gas chromatograph involving GC-2010 composed of a ⁶³Ni Electron Capture Detector (ECD) prepared using split/splitless injector capable of detecting contaminants at trace concentrations (within the smaller μg/g range) in the matrix was used. Detection of residues based on analysis with GC were verified by analyzing the extract from two extra columns comprising various polarities. The coating of first column involved the use of ZB-1 (methyl polysiloxane) fixed to ECD while the second used ZB-17 (50% phenyl, methyl polysiloxane), while ECD was employed for detection purposes. The length of the column was 60 m. The conditions applied for the columns were not different. Temperatures for injector and detector were fixed at 280ºC and 300ºC, correspondingly. Also, a fused silica ZB-5 (comprising 30 m by 0.25 mm and 0.25 μm thickness of the film) was employed with these oven temperature arrangement: original temperature of 60ºC was maintained for 1 minute and ramped at 30ºC per minute to 180ºC; later retained for 3 minutes and ramped at 3ºC per minute to 220ºC; and finally holding it for 3 minutes before ramping at 10 ºC per minute to 300ºC. The total instrumental run time per sample was 32 minutes. Furthermore, nitrogen was utilized as carrier gas at a flow rate of 1 ml per minute. The injection volume of the gas chromatograph was 1 microliter.

2.3.4. Identification of peaks

An external calibration technique was used to determine the amounts of residues within sample extracts and the calibration standard used was 6 calibrations as previously illustrated (C. Bempah et al., 2012). So, a benchmark mixture with established pesticide amount was run before the detector response for individual compound determined. After the calibration curve was done, the sampled extracts were run on the GC, and their peak retention times were compared with that of the standard and pesticide compound in the extract were identified. The area of the corresponding peak within the sample was compared immediately with the standard. All the analyses were done in triplicates with the average concentrations computed correspondingly.

2.3.5. Control and assurance of quality

The analytical method comprised quality control as well as quality assurance earlier described by Bempah et al. (C. Bempah et al., 2012). Consequently, in addition to recovery and precision, the linearity of pesticides investigated was also assessed by the addition of a mix to 20 grams of sliced raw samples. Prior to extraction, spiked samples remained standing for a minimum of 1 hour. The concentration of the standard used to spike the sample was ~1–5 mg/ml. Extraction and analysis of samples comprising ten (10) replicates were done based on the suggested procedure described earlier. Calculation of precision was centered on repeatability of a total of 10 samples every day, while reproducibility was undertaken on 5 separate days. In addition, calculation of recoveries for samples in triplicates resulted in percent recoveries recorded within spiked samples ranging from 87% to 120%. Consequently, data for sample analysis were appropriately adjusted for the recoveries. The limit of detection (LOD) were calculated using the guidelines provided by the International Conference on Harmonization (ICH) (Branch, 2005), which were 0.001 mg/kg. As well, solvent blank analyses were conducted to check interference of species inside the reagents. No targeted compound was found in the blank. QC standard of known concentration was used.

2.3.6. Health risk assessment: Vegetables

To fully understand the potential risks of these OCPs to human health, a health risk assessment study on the detected compounds was conducted using the United States Environmental Protection Agency (US EPA) risk assessment model (Kuranchie-Mensah et al., 2011). Body weight of 10 kg were utilized for children and 60 kg for adult. The vegetable consumption rate was estimated as 0.137 × 10⁻³ mg/kg/day in Ghana (Bolor et al., 2018; Kuranchie-Mensah et al., 2011). Thus, for every type of organochlorine pesticide exposure, the estimated daily intake (mg/kg) was obtained with the following formula:

$\mathrm{E}\mathrm{D}\mathrm{I}=\frac{\left(C\times \hspace{0.17em}CR\right)}{\mathrm{B}\mathrm{W}}$

where EDI is the estimated daily intake, C represents the concentration of pesticide residue (mg/kg), CR represents the consumption rate (kg/day), and BW is the average body weight (kg) of children and adults in Ghana.

Hazard index (HI) for each detected OCP for humans were calculated as the ratio between estimated daily intake (EDI) and the acceptable daily intake (ADI), which are regarded as harmless levels of exposure throughout the lifetime. When HI is >1, it suggests that lifetime consumption of vegetables that contain the quantified level of OCP residues could pose health risks (Wang et al., 2011). The HI was computed from the following equation:

$\mathrm{H}\mathrm{I}=\frac{\mathrm{E}\mathrm{D}\mathrm{I}}{\mathrm{A}\mathrm{D}\mathrm{I}}$

2.4. Data analysis

Data on OCP residues detected in the four (4) selected vegetables sampled from three (3) different markets were processed with Microsoft excel (version 2013) and Statistix 9 software and then subjected to Analysis of Variance (ANOVA) at 1% significance. Thus, significance was set at p ≤ 0.01. LSD at 1% was used to identify OCP on vegetables whose means are statistically different. The calculation of OCP residues found for each sample was in mg/kg. Values of mean concentrations for every OCP residue were compared to current maximum residue levels of the European Union (EU MRL) accessed from the EU-Pesticides database (EU, 2021). Samples with <LOD were treated as 0.000 in the statistical calculations.

3. Results

3.1. Differential OCP residue levels in vegetables

The concentrations of organochlorine pesticide residues found in the sampled vegetables showed significant (p ≤ 0.01) when compared within the pesticide residues (Table 1). γ-HCH residue was not identified in carrots and tomatoes (Table 1). However, γ-HCH was recorded for lettuce (0.013 mg/kg) as well as cabbage (0.012 mg/kg) (Table 1). Cabbage had the highest and tomatoes the least concentration of δ-HCH residue levels of 0.23 and 0.08 mg/kg, correspondingly, and these concentrations were above the recommended MRL (Table 1). Heptachlor, detected in the vegetable samples had significantly higher levels in cabbage (1.05 mg/kg) than in any other vegetable type (Table 1). Compared to the other vegetables, lettuce samples recorded a higher concentration of Aldrin (1.23 mg/kg). Among the vegetables studied, the degree of p, p’-DDT found in tomatoes was highest (1.194 mg/kg), while lettuce showed the least residue (0.193 mg/kg). Only cabbage recorded an o, p’-DDT residue level of 0.060 mg/kg. Tomato samples recorded higher residual levels of p, p’-DDE (0.147 mg/kg) compared to the recommended levels of MRL (Table 1).

Table 1. Mean concentration levels (mg/kg) of OCPs residue of selected vegetables. Values are means of 3 replicates (n = 3) with standard errors (±SE). Values showing the same letters indicate no significant differences in the vegetables within same OCPs residue at p ≤ 0.01

Vegetable	γ-HCH	δ-HCH	Heptachlor	Aldrin	p, p’-DDT	o, p’-DDT	p, p’-DDE
Cabbage	0.012 ± 0.012b	0.23 ± 0.067a	1.05 ± 0.402 a	0.90 ± 0.213 b	0.741 ± 0.103b	0.055 ± 0.055a	0.034 ± 0.034c
Carrot	ND	0.19 ± 0.044 b	0.55 ± 0.101b	0.58 ± 0.075c	0.517 ± 0.120 c	ND	0.055 ± 0.055b
Lettuce	0.013 ± 0.013a	0.15 ± 0.009c	0.38 ± 0.127c	1.23 ± 0.687a	0.193 ± 0.102 d	ND	0.056 ± 0.056b
Tomatoes	ND	0.07 ± 0.00d	0.08 ± 0.042d	0.39 ± 0.031d	1.194 ± 0.609 a	ND	0.147 ± 0.088a
MRL	0.01	0.01	0.01	0.01	0.05	0.05	0.05
LSD	0.0004	0.02	0.02	0.03	0.039	0.005	0.017

Note: ND=Not Detected

3.2. Differential OCP residue levels at various markets

Vegetables sampled in the different markets showed significant levels (p ≤ 0.01) in the organochlorine residues annotated (Table 2). Vegetables from Ho Dome and Shia markets on average showed detectable levels of γ-HCH, with the Shia market having the topmost level (0.01 mg/kg), similar to the values of MRL allowed in vegetables (Table 2). Ho Dome market vegetables recorded a higher mean concentration (0.18 mg/kg) of δ-HCH residue compared to other markets, with the Shia market recording the least (0.13 mg/kg). Vegetable samples from Ho central market recorded higher heptachlor mean concentration (0.76 mg/kg) and were followed in a decreasing trend by the Ho Dome market (0.40 mg/kg) and the Shia market (0.37 mg/kg; Table 2). The aldrin mean residue concentration of sampled vegetables was highest (1.01 mg/kg) in the Shia market and lowest (0.49 mg/kg) in Ho Dome market. However, these are higher compared to the standard values of MRL (Table 2). The degree of p, p’-DDT found in vegetables obtained from the market in Ho central was higher (1.089 mg/kg) than the other markets (Table 2). The concentration of o, p’-DDT in vegetables from the Ho Dome market (0.042 mg/kg) was noticed to be within the acceptable limit of 0.05 mg/kg, but below detectable limits in vegetables from the Ho central and Shia markets (Table 2). Ho central and Shia markets recorded equal and highest quantities of p, p’-DDE (0.076 mg/kg). Also, there was no significant difference in the levels of p, p’-DDE found in the vegetables among the markets, although the levels exceeded the MRL recommended (0.05 mg/kg) (Table 2).

Table 2. The level of OCPs mean concentrations (mg/kg) of vegetables selected from different markets in Ho Municipal. Values are means of 4 replicates (n = 4) with standard errors (±SE). Values showing the same letters indicate no significant differences in the market within same OCPs residue at p ≤ 0.01

Market	γ-HCH	δ-HCH	Heptachlor	Aldrin	p, p’-DDT	o, p’-DDT	p, p’-DDE
Ho central	ND	0.1675 ± 0.06b	0.765 ± 0.374a	0.82 ± 0.195 b	1.085 ± 0.467a	ND	0.07625 ± 0.076a
Ho Dome	0.00875 ± 0.009b	0.185 ± 0.044a	0.40 ± 0.162b	0.4975 ± 0.131c	0.412 ± 0.142c	0.042 ± 0.0415a	0.06675 ± 0.041a
Shia	0.010 ± 0.01a	0.13 ± 0.029c	0.37 ± 0.138c	1.01 ± 0.515 a	0.487 ± 0.083b	ND	0.07575 ± 0.044a
MRL	0.01	0.01	0.01	0.01	0.05	0.05	0.05
LSD	0.0004	0.01	0.02	0.03	0.034	0.004	0.015

Note: ND=Not Detected

3.3. Comparing concentration of OCP residues found in vegetables and their market source interaction

The quantity of pesticide residue identified in vegetables obtained from different market sources showed a significant difference (p ≤ 0.01) (Table 3). Lettuce tested from the market in Shia and cabbage from the Ho Dome market were significantly different in γ-HCH residual levels, recording 0.04 and 0.035 mg/kg, individually (Table 3). γ-HCH residue levels were not detected in the other vegetables and their respective market sources except lettuce from the Shia market and cabbage sampled from the Ho Dome market (Table 3). In quantifying δ-HCH residues in the samples selected from different market sources, the results revealed a different outcome in the levels of concentration in considering the interaction between the vegetable and their market sources. Three similar significant groups of δ-HCH residues were noticed. These were lettuce and cabbage (Shia market), carrot (Ho central market), lettuce (Ho Dome and Ho central markets), and tomatoes (from the three markets) (Table 3). Cabbage from Ho central market recorded significantly higher δ-HCH levels (0.34 mg/kg) relative to the rest and was above the approved levels of MRL. This residue (δ-HCH) was also detected in all vegetables interacting with market sources (Table 3). In considering heptachlor residual levels, cabbage from Ho central market recorded a significantly higher heptachlor residual level of 1.85 mg/kg compared to other vegetables sampled from other market sources (Table 3). Although heptachlor residues were not detected in tomatoes from the Shia market, it was significantly detected in all other vegetables in interaction with market sources (Table 3). Aldrin levels were recorded in all market and vegetable interactions, with lettuce from the Shia market showing significantly higher concentration levels (2.55 mg/kg; Table 3). High p, p’-DDT residues were found in all market and vegetable interactions, except lettuce from Ho Dome market, and the residue found in tomatoes from Ho central market was significantly higher (2.410 mg/kg) relative to the rest (Table 3). O, p’-DDT was merely discovered in the cabbage sample from the market in Ho Dome (0.166 mg/kg) and this was above the MRL (Table 3). The highest p, p’-DDE level (0.305 mg/kg), above the MRL was recorded for tomatoes collected within the market of Ho central (Table 3). Sampling of these vegetables including cabbages, carrots, and lettuce within the market of Ho central; lettuce and tomatoes in the market of Ho Dome; as well as cabbages and carrots obtained from the market of Shia did not show any detectable p, p’-DDE residue (Table 3).

Table 3. Interaction effect of market and vegetable type on the mean concentration levels (mg/kg) of OCPs residue. Values are means of 3 biological replicates (n = 3) with standard errors (±SE). Values showing the same letters indicate no significant differences in the interaction between vegetables and market within same OCPs residue at p ≤ 0.01

Markets * Vegetable	γ-HCH	δ-HCH	Heptachlor	Aldrin	p, p’-DDT	o, p’-DDT	p, p’-DDE
Ho central cabbage	ND	0.34 ± 0.015 a	1.85 ± 0.010 a	1.28 ± 0.021 b	0.948 ± 0.007b	ND	ND
Ho central carrot	ND	0.11 ± 0.012 f	0.53 ± 0.012d	0.71 ± 0.006 e	0.747 ± 0.008c	ND	ND
Ho central lettuce	ND	0.15 ± 0.01de	0.55 ± 0.006d	0.93 ± 0.025 c	0.234 ± 0.011 h	ND	ND
Ho central Tomatoes	ND	0.07 ± 0.006 g	0.13 ± 0.021 g	0.35 ± 0.01 h	2.410 ± 0.040a	ND	0.305 ± 0.001a
Ho Dome cabbage	0.035 ± 0.002 b	0.25 ± 0.000 b	0.63 ± 0.025c	0.86 ± 0.01d	0.646 ± 0.006d	0.166 ± 0.002 a	0.101 ± 9.81E-18d
Ho Dome carrot	ND	0.26 ± 0.010 b	0.73 ± 0.01b	0.45 ± 0.01 g	0.463 ± 0.001f	ND	0.166 ± 0.0006bc
Ho Dome lettuce	ND	0.16 ± 0.006d	0.13 ± 0.00 g	0.23 ± 0.00i	ND	ND	ND
Ho Dome Tomatoes	ND	0.07 ± 0.000 g	0.12 ± 0.006 g	0.45 ± 0.012 g	0.538 ± 0.001e	ND	ND
Shia cabbage	ND	0.11 ± 0.015 f	0.66 ± 0.006c	0.55 ± 0.00f	0.628 ± 0.006d	ND	ND
Shia carrot	ND	0.21 ± 0.015 c	0.38 ± 0.006f	0.58 ± 0.015f	0.341 ± 0.006 g	ND	ND
Shia lettuce	0.040 ± 0.001a	0.13 ± 0.006 e f	0.45 ± 0.012 e	2.55 ± 0.006a	0.345 ± 0.00 g	ND	0.167 ± 0.003b
Shia Tomatoes	ND	0.07 ± 0.006 g	ND	0.37 ± 0.01 h	0.634 ± 0.002d	ND	0.136 ± 0.002c
MRL	0.01	0.01	0.01	0.01	0.05	0.05	0.05
LSD	0.0003	0.03	0.04	0.06	0.067	0.008	0.029

Note: ND=Not Detected

4. Discussion

Several vegetable growers have turned to using chemicals with extremely high potency to control pests and diseases on individual farms. For instance, approximately 87% of the vegetable growers within Ghana apply pesticides (Dinham, 2003). Organochloride and organophosphate pesticide residues take a long period to breakdown after use and these can persist in fruits and vegetables until they end up on the table of consumers for consumption (Van Emden, 1983). The failure of farmers to properly adhere to instructions on pesticide applications poses a threat to consumers. Vegetable growers apply extreme volumes of chemicals disregarding preharvest intervals during production. These poisonous chemical residues beyond acceptable levels end up in our foods when tested, especially if the time permitted is not sufficient for the chemicals to completely disintegrate (Bajwa & Sandhu, 2014).

Cabbages, carrots, lettuce, and tomatoes sampled from the three markets showed significant differences in the quantification of δ-HCH, heptachlor, aldrin, as well as p, p’-DDT residues that were above the MRL (Table 1). Among the vegetables, total cabbage sampled from all three markets recorded the highest residual level for both δ-HCH (0.23 mg/kg) and heptachlor (1.05 mg/kg; Table 1). Likewise, cabbage notably exhibited the greatest residual quantity of OCPs above MRL in an assessment of vegetables from certain agricultural regions within Togo (Kolani et al., 2016). Aldrin pesticide residue was significantly higher (1.23 mg/kg; Table 1) in total lettuce sampled from the three markets. The mean concentration of carbendazim, a very persistent and toxic fungicide, was reported to be higher in lettuce than other vegetables in a similar study on vegetables in China between the years 2014 and 2016 (Xu et al., 2018). This could be an indication that the pesticides administered to these leafy vegetables were in high dosage than required, having tendencies of posing high risk to consumers of lettuce. The extensive application of pesticides alongside their ability to be stable, and the propensity to bioaccumulate cause them to be especially hazardous for humans and even to unintended species (Fenik et al., 2011). Pesticides consumed through vegetables should be seen as highly dangerous to individual healthiness (Horna et al., 2007; Mukherjee & Gopal, 1996). Pesticide poisoning has resulted in approximately 849,000 deaths worldwide, with a higher number in developing countries (WHO, 2002).

Ho Dome was the only market which recorded the entire OCPs understudy. This may be as a result of the sources of their supply (Table 2). All organochlorine residues found within vegetables sampled from three different marketplaces were above European Union (EU) MRLs (Table 3). This finding is similar to a recent report on the high incidence of pesticide contamination of vegetables in United States of America (Fillion et al., 2000). Also, in agreement, several pesticide residues exceeded MRL detected in citrus fruits and vegetables reported to have been irrigated with water containing various pesticides in the Jordan valley (Al-Nasir et al., 2020). Similarly, a study on 13 different fresh fruits plus vegetables within Algeria between the years 2013–2014 reported 12.5% of 160 samples having pesticide residues above MRL (Mebdoua et al., 2017). There have been reports of vegetable growers in Ghana engaged in the application of high doses of pesticides to vegetable farms beyond the recommended dosage (Fenik et al., 2011). The findings of the present research are similar to the results of an investigation that indicates pesticide residues on fruits as well as vegetables at Ghanaian marketplaces had pesticide residues above the MRL (Ghana Statistical Service GSS, 2010). Vegetable quality is compromised by these chemicals, making it unsafe to consume and pose a health hazard to consumers, particularly when residue levels exceeds the internationally accepted EU MRL. Previous studies suggest that, vegetables containing traces of insecticides beyond the recommended MRL, endangers the health of individuals who consume these vegetables (Akomea-Frempong et al., 2017; Akoto et al., 2013).

The γ-HCH residue detected in cabbage in this study (0.012 ± 0.012) was above that previously reported in Ghana (0.00140 ± 0.41) (Bolor et al., 2018) and Togo (<0.000001) (Kolani et al., 2016), but below what was again reported in Ghana (0.100 ± 0.004) (C. Bempah et al., 2012) [Table 4]. In carrot, γ-HCH was not detected in the present study; however, it was below the limit of detection (<LOD) reported in Ghana (C. Bempah et al., 2012). Regarding lettuce, the present study found a higher γ-HCH residue (0.013 ± 0.013) compared to various locations in Kumasi of Ghana (0.006 ± 0.002) (C. Bempah et al., 2012); (0.00954 ± 0.02, 0.00519 ± 0.01, 0.00716 ± 0.14 (Bolor et al., 2018) except Anglican Hostel in Kumasi (0.01682 ± 4.80) (Bolor et al., 2018). Extremely low residue (0.000017 ± 0.008) was found in Togo (Kolani et al., 2016). With respect to tomatoes, no residue of γ-HCH was detected in this study, though it was earlier found in Ghana (0.02) (C. K. Bempah & Donkor, 2011), (<0.01–0.02) (C. K. Bempah et al., 2011), (0.008 ± 0.002) (C. Bempah et al., 2012), (<0.0025) (Ntow, 2001) and Togo (0.000002 ± 0.000) (Kolani et al., 2016).

Table 4. Mean concentration (mg/kg) of OCP residues in the present study compared with other studies

Vegetable	Location	Country	γ-HCH	δ-HCH	Heptachlor	Aldrin	p, p’-DDT	o, p’-DDT	p, p’-DDE	Reference
	Ho Municipal	Ghana	0.012 ± 0.012	0.23 ± 0.067	1.05 ± 0.402	0.90 ± 0.213	0.741 ± 0.103	0.055 ± 0.055	0.034 ± 0.034	This study
	Local markets	Ghana	0.100 ± 0.004			<LOD	0.032 ± 0.010		0.008 ± 0.004	(C. Bempah et al., 2012)
Cabbage	Ayigya	Ghana	0.00140 ± 0.41	0.00150 ± 1.81			0.00567 ± 0.44			(Bolor et al., 2018)
	Gyenyase	Ghana		0.01241 ± 0.14			0.00034 ± 0.02			(Bolor et al., 2018)
	Kentinkrono	Ghana		0.00953 ± 0.28			0.03173 ± 0.07			(Bolor et al., 2018)
	Anglican Hostel	Ghana		0.00791 ± 0.02			0.01029 ± 0.07			(Bolor et al., 2018)
		Togo	<0.000001	0.000507 ± 0.079	0.000007 ± 0.002	0.000177 ± 0.010	0.000190 ± 0.000	0.000001 ± 0.000	0.000215 ± 0.021	(Kolani et al., 2016)
Carrot	Ho Municipal	Ghana	ND	0.19 ± 0.044	0.55 ± 0.101	0.58 ± 0.075	0.517 ± 0.120	NF	0.055 ± 0.055	This study
	Local markets	Ghana	<LOD			0.010 ± 0.021	0.004 ± 0.002		<LOD	(C. Bempah et al., 2012)
	Ho Municipal	Ghana	0.013 ± 0.013	0.15 ± 0.009	0.38 ± 0.127	1.23 ± 0.687	0.193 ± 0.102	NF	0.056 ± 0.056	This study
	Local markets	Ghana	0.006 ± 0.002			0.008 ± 0.004	0.020 ± 0.002			(C. Bempah et al., 2012)
	Ayigya	Ghana	0.00954 ± 0.02		0.00229 ± 0.14	0.02266 ± 0.15	0.00934 ± 0.22			(Bolor et al., 2018)
Lettuce	Gyenyase	Ghana	0.00519 ± 0.01		0.00230 ± 0.14	0.01558 ± 0.28	0.00509 ± 3.53			(Bolor et al., 2018)
	Nsenie	Ghana			0.00020 ± 0.01	0.02150 ± 0.42	0.01150 ± 4.38			(Bolor et al., 2018)
	Kentinkrono	Ghana	0.00716 ± 0.14		0.00108 ± 0.14	0.02392 ± 0.28	0.00451 ± 0.83			(Bolor et al., 2018)
	Anglican Hostel	Ghana	0.01682 ± 4.80	0.00523 ± 0.09		0.02178 ± 1.19	0.00220 ± 0.02			(Bolor et al., 2018)
		Togo	0.000017 ± 0.008	0.000201 ± 0.019	0.000032 ± 0.031	0.000262 ± 0.022	0.000232 ± 0.1	<0.000001	0.000081 ± 0.047	(Kolani et al., 2016)
	Ho Municipal	Ghana	ND	0.07 ± 0.00	0.08 ± 0.042	0.39 ± 0.031	1.194 ± 0.609	ND	0.147 ± 0.088	This study
	Accra Metropolis	Ghana	0.02	0.02	0.02	ND	0.01	ND	<0.01	(C. K. Bempah & Donkor, 2011)
Tomatoes	Accra Metropolis	Ghana	<0.01–0.02	0.01–0.02	0.01–0.02		<0.01–0.01			(C. K. Bempah et al., 2011)
	Local markets	Ghana	0.008 ± 0.002			<LOD	0.012 ± 0.006			(C. Bempah et al., 2012)
	Akumadan	Ghana	<0.0025						<0.0001	(Ntow, 2001)
		Togo	0.000002 ± 0.000	0.000089 ± 0.010	<0.000001	0.000166 ± 0.010	0.000165 ± 0.021	<0.000001	0.000080 ± 0.010	(Kolani et al., 2016)
Cucumber	Local markets	Ghana	<LOD			<LOD	0.009 ± 0.003			(continued on next page) (C. Bempah et al., 2012)
	Benin City	Nigeria	0.00 ± 0.00	0.00 ± 0.00		0.00 ± 0.00	0.00 ± 0.00			(Atuanya & Onuoha, 2018)
	Local markets	Ghana	0.019 ± 0.002			0.006 ± 0.002	0.035 ± 0.005			(C. Bempah et al., 2012)
	Ayigya	Ghana		0.00078 ± 0.23						(Bolor et al., 2018)
Onion	Gyenyase	Ghana				0.00788 ± 0.27	4.42 ± 0.54			(Bolor et al., 2018)
	Nsenie	Ghana			0.00090 ± 0.14	0.00549 ± 0.14				(Bolor et al., 2018)
	Anglican Hostel	Ghana					4.49 ± 1.45			(Bolor et al., 2018)
	Benin City	Nigeria	0.00 ± 0.00	0.00 ± 0.00		0.00 ± 0.00	0.00 ± 0.00			(Atuanya & Onuoha, 2018)
Watermelon	Benin City	Nigeria	0.0002 ± 0.00							(Atuanya & Onuoha, 2018)
Amaranths	South West	Nigeria			0.052 ± 0.025	0.509 ± 0.133				(Adeleye et al., 2019)
Fluted Pumpkin	South West	Nigeria			0.323 ± 0.048	0.391 ± 0.065				(Adeleye et al., 2019)
Leafy vegetables	Local farms	Qatar			7000 ± 7.93	2780 ± 3.08				(Elobeid et al., 2021)
Fruiting vegetables	Local farms	Qatar			3430 ± 4.11	920 ± 2.16				(Elobeid et al., 2021)

Note: ND—not detected; <LOD—below limit of detection

Detected δ-HCH for cabbage in the current study (0.23 ± 0.067) is extremely higher than reported earlier in Ghana (0.02) (C. K. Bempah & Donkor, 2011), (0.00150 ± 1.81, 0.01241 ± 0.14, 0.00953 ± 0.28, 0.00791 ± 0.02) (Bolor et al., 2018) and Togo (0.000507 ± 0.079) (Kolani et al., 2016) [Table 4]. Also, in this study, lettuce recorded higher levels of δ-HCH (0.15 ± 0.009) compared to that detected in Ghana (0.00523 ± 0.09) (Bolor et al., 2018) and Togo (0.000201 ± 0.019) (Kolani et al., 2016). As well, δ-HCH residues detected in tomatoes in this study (0.07 ± 0.00) is higher than reported in Ghana (0.02) (C. K. Bempah & Donkor, 2011), (0.01–0.02) (C. K. Bempah et al., 2011), and Togo (0.000089 ± 0.010) (Kolani et al., 2016).

Heptachlor residue level recorded in Ho Municipal of Ghana for this study (1.05 ± 0.402) is very high compared to earlier records from Togo (0.000007 ± 0.002) (Kolani et al., 2016) [Table 4]. Similarly, levels of heptachlor residue found in lettuce for the present work (0.38 ± 0.127) is extremely higher than previously reported in Ghana (0.00229 ± 0.14, 0.00230 ± 0.14, 0.00020 ± 0.01, 0.00108 ± 0.14) (Bolor et al., 2018), and Togo (0.000032 ± 0.031 mg/kg) (Kolani et al., 2016). Likewise, heptachlor residue on tomatoes for this research is higher (0.08 ± 0.042) than reported elsewhere in Ghana (0.02) (C. K. Bempah & Donkor, 2011), (0.01–0.02) (C. K. Bempah et al., 2011), and Togo (<0.000001) (Kolani et al., 2016).

Aldrin residue level detected in this work for cabbage (0.90 ± 0.213), carrot (0.58 ± 0.075), lettuce (1.23 ± 0.687) and tomatoes (0.39 ± 0.031) were all above earlier reports for the respective vegetables [Table 4). Thus, for cabbage (<LOD) (C. Bempah et al., 2012), (0.000177 ± 0.010) (Kolani et al., 2016), carrot (0.010 ± 0.021) (C. Bempah et al., 2012), lettuce (0.008 ± 0.004) (Kolani et al., 2016), (0.02266 ± 0.15, 0.01558 ± 0.28, 0.02150 ± 0.42, 0.02392 ± 0.28, 0.02178 ± 1.19 (Bolor et al., 2018), and tomatoes (ND—not detected) (C. K. Bempah & Donkor, 2011), (<LOD) (C. Bempah et al., 2012), (0.000166 ± 0.010) (Kolani et al., 2016).

The p, p’-DDT residue level in this study for cabbage (0.741 ± 0.103); carrot (0.517 ± 0.120); lettuce (0.193 ± 0.102); and tomatoes (1.194 ± 0.609) were again, respectively, above that indicated in other studies for cabbage (0.032 ± 0.010) (C. Bempah et al., 2012), (0.00567 ± 0.44, 0.00034 ± 0.02, 0.03173 ± 0.07, 0.01029 ± 0.07) (Bolor et al., 2018); carrot (0.004 ± 0.002) (C. Bempah et al., 2012); lettuce (0.020 ± 0.002) (C. Bempah et al., 2012); (0.00934 ± 0.22, 0.00509 ± 3.53, 0.01150 ± 4.38, 0.00451 ± 0.83, 0.00220 ± 0.02) (Bolor et al., 2018), (0.000232 ± 0.1) (Kolani et al., 2016); and tomatoes (<0.01–0.01) (C. K. Bempah et al., 2011), (0.012 ± 0.006) (C. Bempah et al., 2012), (0.000165 ± 0.021) (Kolani et al., 2016) [Table 4].

The present study showed higher level of o, p’-DDT residue in cabbage (0.055 ± 0.055) compared to report from Togo (0.000001 ± 0.000). However, this pesticide residue was not found in carrot, lettuce and tomatoes for this study and as well, not detected in tomatoes in Accra by Bempah & Donkor (C. K. Bempah & Donkor, 2011). Yet, it was below the detection limit in lettuce (<0.000001) and tomatoes (<0.000001) in Togo (Kolani et al., 2016) (Table 4).

Similarly, p, p’-DDE exhibited higher residue levels in the current study for cabbage (0.034 ± 0.034), carrot (0.055 ± 0.055), lettuce (0.056 ± 0.056), and tomatoes (0.147 ± 0.088) when compared to same vegetables from other locations, including cabbage (0.008 ± 0.004) (C. Bempah et al., 2012), (0.000215 ± 0.021) (Kolani et al., 2016); carrot (<LOD) (C. Bempah et al., 2012); lettuce (0.000081 ± 0.047) (Kolani et al., 2016); and tomatoes (<0.01) (C. K. Bempah & Donkor, 2011), (<0.0001) (Ntow, 2001), (0.000080 ± 0.010) (Kolani et al., 2016) (Table 4).

The organochlorine pesticides of interest have been found in other vegetables not considered in the present study (Table 4). These vegetables include cucumber (C. Bempah et al., 2012), onion (Bolor et al., 2018; C. Bempah et al., 2012), Amaranth and fluted pumpkin (Adeleye et al., 2019), watermelon (Atuanya & Onuoha, 2018), leafy vegetables and fruiting vegetables (Elobeid et al., 2021). Nevertheless, Atuanya and Onuoha did not detect these pesticides in onion and cucumber in Nigeria (Atuanya & Onuoha, 2018).

The detection of traces of banned OCPs like DDT and high levels of banned aldrin above the MRL on sampled vegetables is indications that, a number of these banned chemicals are still in use or are persisting within the soil years after their ban. Heptachlor, for instance, can persist in the environment years after use. Acute or chronic inhalation or exposure can cause neurological disorders or nervous disorders (Environmental Protection Agency EPA, 2021). Apparently, Ghanaian vegetable growers normally use banned chemicals such as DDT as well as 1,2,3,4,5,6-hexachlorocyclohexane (HCH) because obtaining these harmful chemicals is cheap regarding cost (Okoffo et al., 2016). Pesticide residues recorded in high levels in vegetables sampled within the study may also be a result of direct chemical treatment or spraying of the vegetables a few days before harvesting. The samples might have also been contaminated with a polluted water source. The utilization of polluted water has been reported in several vegetable growing areas in Ghana (Obuobie et al., 2006). Chemical remnants found within water mostly occur indirectly through contamination of the environment due to the ability of chemicals to persist, be mobile, and soluble, enabling them to contaminate both surface and spring waters (Hamilton & Crossley, 2004). These high residual levels of OCPs established in our findings negates the safety and overall quality of vegetable production in some parts of the country.

However, to fully understand the potential risks of contamination of the vegetables by these OCPs to human health, a health risk assessment study on the detected compounds was conducted using the United States Environmental Protection Agency (USEPA) risk assessment model (Kuranchie-Mensah et al., 2011). The hazard index (HI) for all OCPs on the vegetables were below one (HI < 1), an indication that the exposure of Ghanaian population (both children and adults) through the consumption of any of the studied vegetables within the study locations of the Ho Municipality is relatively minimal and does not currently pose significant health risk (Table 5). Generally, the consumption of these vegetables pose a greater risk to children compared to adults.

Table 5. Health risk estimation for OCP residues detected in vegetables from Ho Municipal

Sample	Pesticide	Mean ± SE (mg/kg)	ADI (mg/kg)	EDI (mg/kg)		HI	HR
	γ-HCH	0.012 ± 0.012	3 × 10^−3	2.74 × 10^−8	Adult	9.13 × 10^−6	No
				1.64 × 10^−7	Child	5.48 × 10^−5	No
	δ-HCH	0.23 ± 0.067	3 × 10^−3	5.25 × 10^−7	Adult	1.75 × 10^−4	No
				3.15 × 10^−6	Child	1.05 × 10^−3	No
	Heptachlor	1.05 ± 0.402	0.1 × 10^−3	2.40 × 10^−6	Adult	2.4 × 10^−2	No
Cabbage				1.44 × 10^−5	Child	1.44 × 10^−1	No
	Aldrin	0.90 ± 0.213	0.2 × 10^−3	2.06 × 10^−6	Adult	1.03 × 10^−2	No
				1.23 × 10^−5	Child	6.15 × 10^−2	No
	p, p’-DDT	0.741 ± 0.103	20 × 10^−3	1.69 × 10^−6	Adult	8.45 × 10^−5	No
				1.02 × 10^−5	Child	5.1 × 10^−4	No
	o, p’-DDT	0.055 ± 0.055	20 × 10^−3	1.26 × 10^−7	Adult	6.3 × 10^−6	No
				7.54 × 10^−7	Child	3.77 × 10^−6	No
	p, p’-DDE	0.034 ± 0.03	20 × 10–3	7.76 × 10^−8	Adult	3.88 × 10^−6	No
				4.66 × 10^−7	Child	2.33 × 10^−5	No
	δ-HCH	0.19 ± 0.044	3 × 10^−3	4.33 × 10^−7	Adult	1.44 × 10^−4	No
				2.60 × 10^−6	Child	8.67 × 10^−4	No
	Heptachlor	0.55 ± 0.101	0.1 × 10^−3	1.26 × 10^−6	Adult	1.26 × 10^−2	No
				7.54 × 10^−6	Child	7.54 × 10^−2	No
Carrot	Aldrin	0.58 ± 0.075	0.2 × 10^−3	4.57 × 10^−7	Adult	2.29 × 10^−3	No
				2.74 × 10^−6	Child	1.37 × 10^−2	No
	p, p’-DDT	0.517 ± 0.120	20 × 10^−3	1.18 × 10^−6	Adult	5.9 × 10^−5	No
				7.08 × 10^−6	Child	3.54 × 10^−4	No
	p, p’-DDE	0.055 ± 0.055	20 × 10^−3	1.26 × 10^−7	Adult	6.3 × 10^−6	No
				7.54 × 10^−7	Child	3.77 × 10^−6	No
	γ-HCH	0.013 ± 0.013	3 × 10^−3	2.97 × 10^−8	Adult	9.89 × 10^−6	No
				1.78 × 10^−7	Child	5.93 × 10^−5	No
	δ-HCH	0.15 ± 0.009	3 × 10^−3	3.43 × 10^−7	Adult	1.14 × 10^−4	No
				2.06 × 10^−6	Child	6.87 × 10^−4	No
Lettuce	Heptachlor	0.38 ± 0.127	0.1 × 10^−3	8.68 × 10^−7	Adult	8.68 × 10^−3	No
				5.21 × 10^−6	Child	5.21 × 10^−2	No
	Aldrin	1.23 ± 0.687	0.2 × 10^−3	2.81 × 10^−6	Adult	1.41 × 10^−2	No
				1.69 × 10^−5	Child	8.45 × 10^−2	No
	p, p’-DDT	0.193 ± 0.102	20 × 10^−3	4.41 × 10^−7	Adult	2.21 × 10^−5	No
				2.64 × 10^−6	Child	1.32 × 10^−4	No
	p, p’-DDE	0.056 ± 0.056	20 × 10^−3	1.28 × 10^−7	Adult	6.4 × 10^−6	No
				7.67 × 10^−7	Child	3.84 × 10^−5	No
	δ-HCH	0.07 ± 0.00	3 × 10^−3	1.60 × 10^−7	Adult	5.33 × 10^−5	No
				9.59 × 10^−7	Child	3.20 × 10^−4	No
	Heptachlor	0.08 ± 0.042	0.1 × 10^−3	1.83 × 10^−7	Adult	1.83 × 10^−3	No
				1.1 × 10^−6	Child	11 × 10^−3	No
Tomatoes	Aldrin	0.39 ± 0.031	0.2 × 10^−3	8.91 × 10^−7	Adult	4.46 × 10^−2	No
				5.34 × 10^−6	Child	2.67 × 10^−2	No
	p, p’-DDT	1.194 ± 0.609	20 × 10^−3	2.73 × 10^−6	Adult	1.37 × 10^−4	No
				1.64 × 10^−5	Child	8.2 × 10^−2	No
	p, p’-DDE	0.147 ± 0.088	20 × 10^−3	3.36 × 10^−7	Adult	1.68 × 10^−5	No
				2.01 × 10^−6	Child	1.01 × 10^−4	No

Note: HR—health risk

In spite of the low hazard indices obtained in this study for both children and adults, it does not mean complete safety. Residues from pesticides are known to accumulate after a period of time, and this can adversely have chronic effects on even adult consumers (Akoto et al., 2015).

5. Conclusion

Residues of OCPs detected in sampled vegetables from the various markets demonstrated in this study were above MRLs. Vegetables with high pesticide residues above the MRL may mean higher toxicity levels and makes vegetables unwholesome. The presence of banned pesticides such as Heptachlor and Aldrin, as well as restricted pesticides like γ-HCH above the MRL on vegetable samples indicates the continuous use of these unlawful chemicals or their persistence in the soil. The danger is that, the bulk of these vegetables is eaten in a raw state without heat treatment and may be harmful to the consuming population. Though, consumption of these vegetables in this study suggest no significant health risk to both adult and children, care should be taken because accumulation of residues is inevitable and can pose chronic health hazards. Farmers should therefore be made conscious of the necessity of allowing adequate interval between the last pesticide application and harvest. Also, farmers must be educated on the right approach to pesticide application. Additionally, safety practices related to postharvest handling of vegetables including proper washing prior to eating should be adhered to.

Acknowledgments

The authors appreciate the staff and National Service Personnel of the Ghana Atomic Energy Commission (Chemistry Laboratory) for their assistance in pesticide residue analysis.

Disclosure statement

No potential conflict of interest was reported by the authors.

Data Availability Statement

Derived data supporting the outcomes of this research are available from the corresponding author [J.A] when requested.

Additional information

Funding

This work had support from the Ghana Government Book and Research Allowance for tertiary institutions.