Heavy metals concentration in food crops irrigated with pesticides and their associated human health risks in Paki, Kaduna State, Nigeria

Abstract

The widespread use of pesticides containing heavy metals on agricultural farms has evolved into a significant source of metal pollution in food crops. In Paki, Nigeria, this study investigated the probable health dangers linked with consuming heavy metals contaminated crops fumigated with pesticides containing metals and grown exclusively from borehole water sources. An atomic absorption spectrometry test was used to determine the amounts of heavy metals (Cd, Pb, Cr, Cu, and Zn) in the (root, stem, leaf, and fruit) of certain selected food crops and soil. Potential non-cancer health risks (hazard quotient and hazard index) and target cancer risk (TCR) were computed based on USEPA 2019 guidelines. Heavy metals were found in all of the tested food crops and ranged from 1.00 ± 0.04 to 9.50 ± 0.35, 0.50 ± 0.29 to 5.33 ± 0.16, 0.25 ± 0.12 to 1.50 ± 0.03, 3.17 ± 0.17 to 31.8 ± 0.44, 14.08 ± 0.88 to 44.00 ± 0.29 mg/kg for Cd, Pb, Cr, Cu, and Zn, respectively. The levels of cadmium and lead in all of the studied food crops analyzed were higher than the acceptable limit. Heavy metals in the soil of the investigated crops ranged from 0.33 ± 0.00 to 1.17 ± 0.17, 0.83 ± 0.33 to 3.08 ± 0.05, 0.50 ± 0.02 to 1.1 ± 0.17,4.83 ± 0.20 to 31.50 ± 0.29, 5.00 ± 0.09 to 61.3 ± 0.29 mg/kg for Cd, Pb, Cr, Cu, and Zn, respectively. Heavy metal concentrations in the corresponding soil of all pesticide fumigated crops were significantly higher than in control soil. The Hazard quotient showed that children will experience potential non-cancer risks through the consumption of Allium cepa, Daucus carota, and Solanum lycopersicum for cadmium. The combined multiple effects of the studied metals (HI) indicated that children will experience severe non-cancer health risks through the intake of most of the studied crops. The target cancer risk (TCR) of Cr and Pb were within the range of 10⁻⁶ −10⁻⁵ indicating minimal-to-moderate risk of developing cancer based on the USEPA 2019 standard. Long-term intake of agricultural food crops contaminated with pesticide-derived heavy metals could constitute a national health risk. Heavy metals in pesticides should be screened and monitored regularly.

Keywords:

• Bioaccumulation
• Heavy metals
• Pesticides
• Health hazard

1. Introduction

Heavy metals are naturally occurring elements in the soil, but human actions have tampered with their equilibrium and biochemical and geochemical cycles (Singh et al., 2010). Heavy metals are hazardous elements in the environment; they are not easily degradable, persistent, and can accumulate in plant tissues through bioaccumulation (Yang et al., 2018). Heavy metals such as Zn, Fe, Cu, Mn, and Ni are regarded as essential metals and are associated with important biological activity in humans (Jarup, 2003). However, the overconsumption of these metals interrupts important physiological activity (Abdell & Riffat, 2014). However, Pb, As, and Cd are categorized as carcinogenic heavy metals and are toxic even at low concentrations (USEPA/IRIS, 2006). Therefore, prolonged intake of heavy metals through food consumption has been linked to increased diseases such as cancer, neurological diseases, birth deformity, anemia, and renal dysfunction (Chang et al., 2014; Koh et al., 2014; Rehman et al., 2013).

Hazard characterization of the potential human risk through the consumption of food crops is crucial. Hazard characterization is an estimate of toxicity based on dose exposure evaluation of effects of metal pollutants (carcinogenic and non-carcinogenic). The USEPA (2019) guidelines for human health risk assessment categorize the oral reference dose (RFD) as an average daily oral exposure of pollutants to humans that is not likely to cause significant unfavorable health non-cancer effects throughout a lifetime. The cancer potency slope factor (CPSF) is an estimate of an upper bound of potential cancer risk based on a unit dose USEPA 2019. The risk characterization determines the estimate of the probability of developing a potential health risk of pollutants through oral exposure (USEPA, 2019). The risk characterization further provides an estimate of the potential risk of developing non-cancer and cancer that humans risk through oral exposure to the population. This study determines the non-cancer risk through hazard quotient (HQ) and hazard index (HI) and target cancer risk (TCR) based on the USEPA 2019 established approaches.

The use of pesticides for agricultural purposes has polluted the environment and put people’s health in danger by contaminating food crops. Nigeria is one of The Africa’s top-pesticide users, with an estimated annual use of 15,000 metric tons of pesticides spread around the country under more than 200 different product brands (Peters et al., 2018). Due to occurrences of insecticide resistance among insect pests and the development of agricultural activities in Nigeria, farmers have recently increased their demand for new pesticides (Ogbo & Patrick-Iwuanyanwu, 2019). Despite the importance of chemical pesticides in the management of agricultural pests, studies have discovered heavy metal residues in pesticides at levels exceeding acceptable limits (Bawa et al., 2021a; Barau et al., 2018; Defarge et al., 2018, Yuguda et al., 2015). The unregulated use of these agrochemicals might result in a rise in heavy metal accumulation in agricultural soils and crops over time (X. Wang et al., 2005).

Farmers in northern Nigeria apply pesticides indiscriminately and uncontrollably, including locally produced and branded pesticides. There is an alarming pace of unregistered and unscreened new pesticides entering the market, with chemical concentrations of heavy metals and other compounds not disclosed, or purposefully ignored by producers. Despite the widespread use of metal-based agrochemicals in agricultural farmlands across northern Nigeria, there is a lack of data on the levels of heavy metals in food crops from pesticides-related sources. Most studies have linked sources of heavy metal contamination in food crops to wastewater irrigation, contaminated lands, and use of industrial effluents. However, pesticide-related sources of heavy metals in food crops are mostly neglected or overlooked by previous studies. Moreover, there is a lack of data on health risks for both adults and children (cancer and non-cancer) from the uptake of food crops contaminated with heavy metals from pesticides. Therefore, this research determined the levels of heavy metals and their health risks (non-cancer and cancer) in some selected food crops irrigated with borehole water and fumigated solely using metal-based pesticides as the only source of metals.

2. Materials and method

3. Study area

The research area is located in Paki, Kaduna state, northern Nigeria at longitude 11.5004 and latitude 8.150848, about 75 km northeast of the city of Zaria (Figure 1). Makarfi local government in the west, Soba in the south, and Tudun Wada in Kano State in the north borders the local government. The inhabitants of the town depend mainly on farming covering both dry and rainy seasons. Two agricultural farmlands were selected at random that practiced dry season farming with borehole water irrigation and pesticide application for more than 10 years (Yahaya et al., 2015).

Figure 1. The location of the sampling points in the study.

4. Samples collection

A total of 90 samples were collected from the study area. Three replicated samples from leaves, stems, roots, fruit, and soil were collected from six selected commonly consumed crops (Allium cepa, Solanum lycopersicum, Daucus carota, Cucumis sativus, Brassica oleracea, and Zea mays) fumigated with metal-based pesticides and grown exclusively with borehole water irrigation. These crops were selected based on personal information obtained from farmers as the most commonly consumed crops grown in the study area exclusively fumigated with metal pesticides. At each sampling site, 20 g of each of the six selected crops and their corresponding soil were taken at random from three separate places on each farm to give each crop’s representative samples from October 2019 to December 2019. Three replicates of soil samples for each plant were collected at a depth (0–10 cm) using a spiral auger of 2.5 cm diameter at each sampling site. Soil samples from non-agricultural soil that had not been fumigated with pesticides were collected as control. The soil samples were bulked together to form composite samples as described by Arora et al. (2008). All the samples were collected in a clear, transparent labeled plastic bag and conveyed to the Department of Biological Sciences at Abubakar Tafawa Balewa University (ATBU) in Bauchi, Nigeria.

5. Preparing samples

At ATBU’s Biology Laboratory, each plant part was sliced into tiny pieces, dried in the oven at 80°C, crushed using a stainless steel blender model (HL-2571), and was filtered using a 2-mm screen. The resulting powder was kept at room temperature prior to examination. Samples of soil were dried in the lab, squashed, and filtered using a sieve of 2-mm-sized mesh nets.

6. Heavy metal analysis

Plant and soil samples (1 g) were digested with 15 ml combination of three acids (70% high-purity Sigma Aldrich (nitric acid) HNO₃, 65% (per chloric acid) HClO₄, and 70% (sulfuric acid) H₂SO₄ in a 5:1:1 ratio). At 80°C, the solution was digested until it became translucent. The resulting solution was sieved and diluted to 50 mL with distilled water before being analyzed for Cr, Cu, Cd, Zn, and Pb with an atomic absorption spectrophotometer (AAS) Buck scientific 210 GP as described by Zhong et al. (2018) (Atomic absorption spectrometry instrumentation and condition of operation is presented in Table 1).

Table 1. Details of Atomic absorption spectrometry instrumentation and condition of operation

Heavy metal	Wavelength (nm)	Slit width (nm)	Lamp current (ma)	Flame type
Cd	228.9	0.7	8.0	Air/Ace thane
Pb	283.2	0.7	8.0	Air/Ace thane
Cr	357.9	0.7	8.0	Air/Ace thane
Cu	324.7	0.7	6.0	Air/Ace thane
Zn	213.9	0.7	8.0	Air/Ace thane

7. Quality assurance and control

The reagents and chemicals used were all analytical grade. Deionized water was used for dilution of the sample. The determination of the concentration of metals was based on their respective calibration curves prepared by a stock solution (1000 ppm), from which a standard working solution of 100 ppm was prepared through a serial dilution formula (C₁V₁ = C₂V₂). One milliliter of HNO₃was added to each working standard and diluted with deionized water to the desired volume. The working standard solutions of each metal were prepared from standard solutions of their respective metals, and their absorbances were taken using the AAS at wavelength (Table 1). Calibration curves for each metal ion concentrations to be analyzed were prepared by plotting the absorbance as a function of metal ion standard concentration. Metal ions in the sample were determined by reading the absorbance using the AAS (BUCK scientific model 210 GP) and comparing it to the respective standard calibration curve. Three replicates’ determination was carried out on each sample, and blanks were run at intervals to ensure the quality of the analysis. The detection limit (LOD) was 0.005 ppm, 0.02 ppm, 0.8 ppm, 5.0 ppb, 0.05 ppm for Cu, Cr, Pb, Cd, and Zn, respectively. The limit of quantification (LQD) was 0.0165 ppm, 0.066ppm, 2.64 ppm, 16.5 ppb, and 0.165 ppm for Cu, Cr, Pb, Cd, and Zn, respectively. The calculated recovery percentage range from 75% to 120%.

8. Bioaccumulation factor

Bioaccumulation factor is the ratio of metal concentration in the edible part of plant tissue and concentration of metals in irrigated soil samples, was calculated using the formula below as described by (EPA and IRIS, 2006; Zhong et al., 2017).

BCF (Edible) =$\frac{\mathrm{C}\mathrm{e}\mathrm{d}\mathrm{i}\mathrm{b}\mathrm{l}\mathrm{e}\mathrm{p}\mathrm{a}\mathrm{r}\mathrm{t}}{Csoil}$

9. Assessment of health risks

Health risk assessment indices in this study were estimated using the average mean value of heavy metal content in the edible parts of all the investigated crops as described by EPA and IRIS (2006).

10. Estimated Daily Intake (EDI)

The estimated daily intake of metals (EDI) was estimated using the formula below to ascertain the health risks of taking food crops contaminated with heavy metals from pesticide application (EPA and IRIS, 2006; Zhong et al., 2018).

EDI = (M×K×I)/W

M = Level of metal concentration in food crops (mg/kg), K = conversion factor, I = daily vegetable intake, W = average body weight. According to Rattan et al. (2005) the conversion factor 0.085 was utilized to convert the fresh weight of food crops to dry weight. The daily rate of food crop intake (I) for adults in Nigeria is 0.086 kg/d, according to (Hart et al., 2005), and the estimated average adult body weight is 60 kg, as indicated by (Hart et al., 2005), children average weight age (6–12 years) in Nigeria was taken as 29.37 kg as described by Eze et al. (2017).

11. Hazard quotient

The Hazard Quotient is an estimate of the ratio of human exposure rate to oral reference dose (RfD) and was used to measure the health danger posed by food crop consumption by local inhabitants.

HQ = DIM/RfD

The RfD is a calculation of daily human exposure rate that is not likely to cause significant unfavorable health effects over the course of a lifetime. Cr = 1.5 mg/kg/bw/day, Cd = 0.001 mg/kg/bw, Pb = 0.004 mg/kg/bw/day, Cu = 0.04 mg/kg/bw/day, Zn = 0.3 mg/kg/bw/day was used as the oral reference doses for heavy metals (EPA, 2006).

12. Hazard index

The hazard index (HI), which is the entire sum of all the hazard quotients as given in the equation and was used to determine the potential harm to humans from multiple heavy metals, as reported (EPA, 2006).

HI = HQ=HQCd +HQPb +HQCr + HQCu +HQZn

13. Target Cancer Risk (TCR)

TCR is described as the probability of an individual adults or children developing cancer risk during their lifetime due to long-term exposure to carcinogenic metals (Q. Liu et al., 2020). TCR was computed based on the CPSF equation by USEPA (2019) (Q. Liu et al., 2020).

TCR = EDI×CPSF

CPSF value was taken as Cr = 0.5 and Pb = 0.0085 (mg/kg/day) as described by USEPA (2019).

14. Statistical analysis

Statistical program “R” 2014 version was used to analyze the data. One-way ANOVA and Duncan mean multiple-comparison test was employed to determine the mean difference in the concentration of each heavy metal between plant parts at p < 0.05 as described by (Dytham, 2011). Pearson correlation analysis was used to determine the association between heavy metal concentrations in plant tissues.

15. Results and discussion

15.1. Concentrations of heavy metals in the studied food crops

The concentrations of heavy metals in different portions of food crops (root, stem, leaf, and fruit) grown in the research area are listed in Tables 2 and 3. Cd, Pb, Cr, Cu, and Zn values ranged from 0.13 to 1.33, 0.50 to 5.33, 0.25 to 1.50, 3.17 to 31.8, 14.08 to 44.00 mg/kg, respectively (Tables 2 and 3). The level of heavy metals varies significantly (p < 0.05) in different regions of most of the crops tested, with no discernible pattern. Differences in absorption capacity, soil physicochemical qualities, plant type, soil organic matter, and pH, among other factors, could be to responsible (C. Wang et al., 2013; Sharma et al., 2008; Wilson & Pyatt, 2007). Heavy metals in the examined food crops were found in the order of Zn >Cu> Cd> Pb> Cr. All of the examined crops, Cd and Pb, had concentrations well above the FAO/WHO limits, while chromium, copper, and zinc concentrations were below the Organization’s (2019) tolerable limits. Heavy metals above permitted limits were detected in all of the investigated crops for Cd and Pb, which could be due to the widespread application of pesticides with metal contents in the research region. Heavy metal residues have been found in pesticides used by farmers in northern Nigeria in previous investigations (Bawa et al., 2021b; Bawa et al., Bawa et al., 2021; Bawa et al., 2021c; Bawa et al., 2021; Yuguda et al., 2015). This implies that year-round use of metal-based pesticides has resulted in high metal buildup, particularly in cadmium and lead at levels exceeding WHO acceptable limits. Furthermore, as compared to other metals, cadmium has been demonstrated to efficiently translocate to crop shoot biomass (Tan et al., 2011; Kulkarmi et al., 2017).

Table 2. Mean Heavy Metals (mg/kg) Concentrations Dry Weight in Food Crops

Sampling Site	Name of Sample	Botanical Name	Hausa Name	Heavy metals mg/kg
				Cd	Pb	Cr	Cu	Zn
Kaduna	Onion	Allium cepa	Albasa	Mean±SD	Mean±SD	Mean±SD	Mean±SD	Mean±SD
	Root			0.17 ± 0.01a	2.33 ± 0.73a	0.67 ± 0.17a	17.83±a	21.33 ± 0.17b
	Stem			ND	ND	ND	ND	ND
	Leaf			0.18 ± 0.00a	1.17 ± 0.17a	ND	10.00±a	15.17 ± 0.33a
	Bulb			1.16 ± 0.03b	4.33 ± 0.33b	1.25 ± 0.06b	15.33±a	23.33 ± 0.16b
	Tomato	Solanum lycopersicum	Tomatur
	Root			0.11 ± 0.01b	2.67 ± 1.00a	0.67 ± 0.16a	11.58 ± 0.22b	17.92 ± 0.21a
	Stem			0.21 ± 0.02b	3.33 ± 0.66a	0.50 ± 0.50a	9.08 ± 0.66b	36.58 ± 0.38a
	Leaf			0.67 ± 0.06a	1.75 ± 0.91a	0.25 ± 0.25a	3.17 ± 0.17a	14.08 ± 0.88a
	Fruit			0.87 ± 0.33a	3.08 ± 0.25a	0.50 ± 0.04a	12.33 ± 0.50b	34.25 ± 0.27a
	Carrot	Daucus carota	Karas
	Root			ND	ND	ND	ND	ND
	Stem			ND	ND	ND	ND	ND
	Leaf			ND	ND	ND	ND	ND
	Taproot			1.18 ± 0.04	4.50 ± 0.50	1.50 ± 0.03	21.3 ± 0.44	19.00 ± 0.29
	Cucumber	Cucumis sativus	Kokwamba
	Root			0.30 ± 0.00a	0.67 ± 0.17a	ND	7.83 ± 0.17a	15.67 ± 0.44a
	Stem			ND	ND	ND	ND	ND
	Leaf			0.27 ± 0.02a	5.33 ± 0.16c	0.67 ± 0.17	15.8 ± 0.60b	44.00 ± 0.29c
	Fruit			0.98 ± 0.29b	1.83 ± 0.17b	ND	22.5 ± 1.76c	37.50 ± 0.29b
	Cabbage	Brassica oleracea	Kabeji
	Root			ND	ND	ND	ND	ND
	Stem			ND	ND	ND	ND	ND
	Leaf			0.88 ± 0.17	0.50 ± 0.29	ND	10.8 ± 1.33	22.50 ± 0.29
		FAO/WHO, 2019 limits		0.2	0.3	2.3	40	60

Note: NB: Mean values indicated by the same letter is not significantly different p > 0.05 across rows, ND=Not Detected.

Table 3. Mean Heavy Metals Concentrations (mg/kg) dry weight in Food Crops

Sampling Site	Name of Sample	Botanical Name	Hausa Name	Heavy metals mg/kg
				Cd	Pb	Cr	Cu	Zn
	Maize	Zea mays	Masara	Mean±SD	Mean±SD	Mean±SD	Mean±SD	Mean±SD
	Root			ND	ND	ND	ND	ND
	Stem			0.13 ± 0.01a	4.00 ± 0.29a	1.17 ± 0.17	31.8 ± 0.44a	17.33 ± 0.17a
	Leaf			ND	ND	ND	ND	ND
	Fruit			1.33 ± 0.04b	0.67 ± 0.44b	ND	16.3 ± 0.17b	39.67 ± 0.25b
		FAO/WHO, 2019 limits		0.2	0.3	2.3	40	60

Note: NB: Mean values indicated by the same letter is not significantly different p > 0.05 across rows, ND=Not Detected.

Cadmium concentrations in the investigated crops ranged from 0.13 mg/kg in the stem of Z. mays to 1.33 mg/kg in fruit of Z. mays (Table 2 and 3). Cadmium concentrations of 7.67 mg/kg in Spinacia oleracea, 4.68 mg/kg in S. lycopersicum, and 6.14 mg/kg in Z. mays were observed previously in food crops sprayed with pesticides containing heavy metals in northern Nigeria (Bawa et al., 2021a; Bawa et al., 2021b; Bawa et al., 2021d). The maximum cadmium concentrations in the food crops sprayed with metal-containing pesticides in this study were comparably similar to sources reported from wastewater irrigations, such as 0.177 mg/kg in China by Dai et al. (2017), 1.20 mg/kg in Saudi Arabia by Balkhair and Asharaf (2016), 0.41 in Ethiopia by Eliku and Leta (2017), 0.67 mg/kg in Pakistan by Khanum et al. (2017). The high levels of cadmium in the analyzed food crops may constitute a significant risk to consumers and have negative consequences for human health. Cadmium accumulates in some human organs such as bones, lungs, liver, nerves, kidneys, and the skeletal system, posing a danger to humans (Chakraborty et al., 2013; Tsutsumi et al., 2014).

Lead levels in the food crops investigated varied from 0.50 mg/kg in the stem of B. oleracea to 5.33 mg/kg in the leaf of C. sativus (Tables 2 and 3). Lead values of 8.17 mg/kg in Oryza sativa, 38.08 mg/kg in Capsicum annuum, and 23.34 mg/kg in O. sativa were previously observed in some food crops sprayed with pesticides containing metals in northern Nigeria (Bawa et al., 2021, 2021a, 2021b). Conversely, lower lead values of 2.18 mg/kg in India (Kumar et al., 2017), 1.73 mg/kg in Ethiopia (Eliku & Leta, 2017), and 2.76 mg/kg in Pakistan (Khanum et al., 2017) from wastewater irrigation sources were reported in previous studies. Hypertension, vertigo, mental illness, and renal malfunction have all been linked to lead exposure through diet (Patrick, 2006).

Chromium concentrations vary from 0.25 mg/kg in S. lycopersicum leaf to 1.50 mg/kg in D. carota tap root in the crops studied (Table 2 and 3 The maximum chromium content found in this study was slightly greater than that found in China (0.077 mg/kg) by Liang et al. (2019), Nigeria (0.84 mg/kg) by Peters et al. (2018), and India (0.32 mg/kg) by Kulkarni (2017). Similar levels of chromium have been found in food crops fumigated with pesticides in northern Nigeria in previous research (Bawa et al., 2021, 2021a, 2021b). Human chromosomal damage, changes in DNA replication and transcription, ulcer, and pulmonary cancer have all been connected to chromium intake (O’brien et al., 2001; Spector et al., 2011).

Copper concentrations vary from 3.17 mg/kg in S. lycopersicum leaf to 31.8 mg/kg in Z. mays stem among the crops investigated (Tables 2 and 3). The maximum concentration of copper in food crops fumigated with pesticides in this study was significantly more than 1.32 mg/kg in India by Kumar et al., 0.56 mg/kg in Saudi Arabia by Balkhair and Asharaf (2016), 5.77 mg/kg in Pakistan by Mahmood and Malik (2014), and 1.68 mg/kg in Kenya by Njuguna et al. (2019).

Copper values of 32.83 mg/kg, 28.75 mg/kg, and 214 mg/kg were discovered in pesticides-fumigated crops in northern Nigeria (Bawa et al., 2021, 2021b, 2021c). Copper poisoning has been linked to gastrointestinal distress, including nausea, vomiting, and liver problems (Kim et al., 2009; Yargholi & Azimi, 2008).

Zinc levels in the crops studied ranged from 14.08 mg/kg in S. lycopersicum leaves to 44.00 mg/kg in C. sativus leaves (Tables 1a and 1b). Zinc concentrations in food crops fumigated with pesticides in previous studies (186.08 mg/kg and 79.83 mg/kg) observed by Bawa et al. (2021b, 2021c) were higher compared to this study. The maximum zinc content in this study was higher than the 39.41 mg/kg obtained by Kumar et al. (2017) in India, 1.88 mg/kg reported by Balkhair and Asharaf (2016) in Saudi Arabia, and 14.4 mg/kg reported by Eliku and Leta (2017) from wastewater irrigation sources. Excessive zinc intake through the diet can result in gastrointestinal problems (Environmetal Protection Agency, 2005).

16. Heavy metal concentration in soils

The mean levels of Cd, Pb, Cr, Cu, and Zn in the soil samples of the examined crops were 0.33–1.17, 0.83–3.08, 0.5–1.1, 4.83–31.50, and 5.00–61.3 mg/kg, respectively (Table 4). The mean content of heavy metals in the soil samples of all the crops investigated was lower than the limit set by the (Unep et al., 2013). The control soil samples differed significantly p < 0.05 compared to the corresponding soil samples of crops fumigated with pesticides for all the studied heavy metals (Table 4 and 10). The maximum concentration of Cd 1.17 mg/kg in the soil of D. carota in this study was comparatively lower to 14.78 mg/kg and 7.67 mg/kg in food crops grown with metal-based pesticides in Nigeria (Bawa et al., 2021a, 2021b). However, cadmium concentration in the soil of food crops in this study was higher compared to 0.85, 0.73, and 0.93 mg/kg from non-pesticide sources reported by Eliku & Leta (2017); G. Liu et al. (2014);and Khanum et al. (2017). Comparisons of heavy metals concentrations in soil obtained in this study with reports from other studies are shown in (Table 11).

Table 4. Heavy Metals Concentrations (mg/kg) in Soil Sample of Each Crop

Sampling Site	Soil from the land of	Botanical Name	Hausa Name	Heavy metals mg/kg
				Cd	Pb	Cr	Cu	Zn
				Mean±SD	Mean±SD	Mean±SD	Mean±SD	Mean±SD
Kaduna	Onion	Allium cepa	Albasa	0.33 ± 0.07a	3.08 ± 0.05b	0.5 ± 0.02a	4.83 ± 0.20a	61.3 ± 0.29a
	Tomato	Solanum lycopersicum	Tomatur	0.92 ± 0.12a	2.76 ± 0.33b	0.5 ± 0.03a	18.33 ± 0.47ab	38.8 ± 0.29a
	Carrot	Daucus carota	Karas	1.17 ± 0.17b	1.83 ± 0.20ab	1.1 ± 0.17b	31.50 ± 0.29b	22.0 ± 0.15a
	Cucumber	Cucumis sativus	Kokwamba	1.17 ± 0.17b	2.17 ± 0.16ab	1.00 ± 0.02b	31.00 ± 0.50b	19.1 ± 0.17a
	Cabbage	Brassica oleracea	Kabeji	ND	2.67 ± 0.17b	0.50 ± 0.02a	6.50 ± 0.58a	12.3 ± 0.12a
	Maize Control	Zea mays Soil	Masara Soil	ND 0.16 ± 0.02c	0.83 ± 0.33a 0.20 ± 0.04c	0.50 ± 0.01a 0.03 ± 0.01c	15.17 ± 0.17ab 1.53 ± 0.03c	5.00 ± 0.09a 2.73 ± 1.36c
		Unep et al. (2013) Limits		10	200	200	50	250

NB: Mean values indicated by the same letter is not significantly different p > 0.05 across rows, ND=Not Detected.

Table 5. Estimated Bioaccumulation Factor of Heavy Metals of the Studied Crops

Sampling Site	Name of Sample	Botanical Name	Hausa Name	BAF
				Cd	Pb	Cr	Cu	Zn
Kaduna	Onion	Allium cepa	Albasa	3.52	0.85	1.92	2.98	0.32
	Tomato	Solanum lycopersicum	Tomatur	0.95	0.98	0.96	0.49	0.66
	Carrot	Daucus carota	Karas	1.01	2.45	1.29	0.68	0.86
	Cucumber	Cucumis sativus	Kokwamba	0.84	1.20	0.67	0.50	1.69
	Cabbage	Brassica oleracea	Kabeji	ND	0.19	ND	1.66	1.82
	Maize	Zea mays	Masara	ND	2.80	2.34	1.07	5.7

Note: Bioaccumulation factor value>1 denotes greater metal uptake ND=Not Detected

Table 6. Pearson correlation coefficient of heavy metals in the investigated food crops samples

Metals	Cd	Pb	Cr	Cu
Cd
Pb	0.557*
Cr	0.585*	0.614*
Cu	0.190	0.131	0.468*
Zn	−0.048	0.092	−0.143	−0.048

Note: N.B Correlation coefficient with an asterisk (*) is significant at p < 0.05

Table 7. Computed Hazard Quotient and Hazard Index of Adult upon Consumption of the Studied Food Crops

Name of Sample	Botanical Name	Hausa Name	Hazard Quotient					Hazard Index
			Cd	Pb	Cr	Cu	Zn
Onion	Allium cepa	Albasa	0.141327	0.13188	5.08E–02	0.04669	0.00947	0.38014
Tomato	Solanum lycopersicum	Tomatur	0.105995	0.09381	0.02E–06	0.03756	0.01391	0.27158
Carrot	Daucus carota	Karas	0.143763	0.13706	6.09E–02	0.06488	0.00772	0.41433
Cucumber	Cucumis sativus	Kokwamba	0.119397	0.05574	0.00000	0.06853	0.01523	0.25890
Cabbage	Brassica oleracea	Kabeji	0.107213	0.01523	0.00000	0.03290	0.00914	0.16448
Maize	Zea mays	Masara	0.162038	0.02041	0.00000	0.04965	0.01611	0.24820

Table 8. Computed Hazard Quotient and Hazard Index of children upon Consumption of the Studied Food Crops

Name of Sample	Botanical Name	Hausa Name	Hazard Quotient					Hazard Index
			Cd	Pb	Cr	Cu	Zn
Onion	Allium cepa	Albasa	2.157906	0.269427	0.103706	0.095388	0.019356	2.64578
Tomato	Solanum lycopersicum	Tomatur	1.037886	0.191648	0.041482	0.076721	0.028415	1.37615
Carrot	Daucus carota	Karas	2.364488	0.280005	0.124447	0.132536	0.015763	2.91724
Cucumber	Cucumis sativus	Kokwamba	0.74668	0.113869	0.082964	0.140003	0.031112	1.11463
Cabbage	Brassica oleracea	Kabeji	0.540099	0.031112	0.082964	0.067201	0.018667	0.74004
Maize	Zea mays	Masara	0.248893	0.04169	0.082964	0.101424	0.032912	0.50788

Table 9. Estimated Target Cancer Risk (TCR) for Adult and Children

Crops		Adults		Children
Botanical Name	Hausa Name	Metals		Metals
		Cr	Pb	Cr	Pb
Allium cepa	Albasa	5.27538E–05	0.000895833	0.000107771	0.001830099
Solanum lycopersicum	Tomatur	3.75247E–05	0.000358333	7.66592E–05	0.000732039
Daucus carota	Karas	0.000054825	0.001075	0.000112002	0.002196118
Cucumis sativus	Kokwamba	2.22955E–05	ND	4.55475E–05	ND
Brassica oleracea	Kabeji	6.09167E–06	ND	1.24447E–05	ND
Zea mays	Masara	8.16283E–06	ND	1.66759E–05	ND

Table 10. Comparison of mean heavy metal concentration in crops from the present study with some previous studies

Country	Authors	Source of Contamination	Heavy metal Mg/kg
			Cd	Cr	Pb	Cu	Zn
Nigeria	Present study	Pesticides sources	0.88–1.33	0.25–1.50	0.50–5.33	3.17–31.8	14.08–44.00
Nigeria	Barau et al. (2018)	Pesticides sources	0.11–0.94	0.02–0.33	0.36–4.64	————-	3.95–17.19
India	Kulkarni (2017)	Sewage waste	0.30–0.62	0.16–0.32	0.23–0.64	1.1–2.3	————-
China	Dai et al. (2017)	Market survey	ND-0.619	———–	ND-1.822	————	————–
Pakistan	Khanum et al. (2017)	Waste/water irrigation	0.51–0.67	0.37–0.60	1.42–2.766	————	————-
Liberia	Ngumbu et al. (2016)	Market survey	0.04–0.13	———–	0.093–0.47	———–	————–
Nigeria	Patrick-Iwuanyanwu and Chioma (2017)	Market survey	0.02–1.48	0.89–2.4	0.016–1.38	————	————–
China	Zhong et al. (2017)	Agricultural farm	0–1.900	———–	0–3.820	————-	————
Indonesia	Siaka et al. (2014)	Waste/water irrigation	————	ND-152.8	11.11–374	4.34–150.5	5.12–90.69
Saudi Arabia	Balkhair and Asharaf (2016)	Waste irrigation	1.20	1.96	0.88	0.56	1.88
Ethiopia	Eliku and Leta (2017)	Waste/water irrigation	0.17–0.41	0.51–1.73	0.26–0.54	————-	2.07–14.4
Nigeria	Oti (2015)	Mine sites	0.10–12.4	0.01–1.02	0.22–6.72	12.6–82.1	34.2–162.1
	Organization (2019) limits		0.2	3.3	0.3	40	60

Table 11. Comparison of mean heavy metal concentration in soil sample from present study with some previous studies

Country	Authors	Source of Contamination	Heavy metal Mg/kg
			Cd	Cr	Pb	Cu	Zn
Nigeria	Present study	Pesticides	0.33–1.17	0.5–1.1	0.83–3.08	4.83–31.50	5.00–61.3
Nigeria	Barau et al. (2018)	Pesticides	0.03–0.22	0.01–0.02	2.77–4.31	———–	21-38-28.58
Pakistan	Khanum et al. (2017)	Waste/water irrigation	0.62–0.85	0.49–0.69	————	———-	————
India	Kumar et al. (2017)	Agricultura farms	————	————	0.25–2.31	0.30–2.10	0.47–4.74
China	G. Liu et al. (2014)	Near mining site	0.73	47.49	70.36	————–	————
Ethiopia	Eliku and Leta (2017)	Waste/water irrigation	0.52–0.93	10.0–21.8	13.6–27.3	11.9–30.3	44.4–88.5
Nigeria	Oti (2015)	Mine sites	126.0	2.12	116	812.2	995.2
	Unep et al. (2013) Limits		10	200	200	50	250

The maximum concentration of Pb 3.08 mg/kg in the soil of A. cepa in this study was lower compared to 13.83 mg/kg and 8.17mgkg grown with metal pesticides in Nigeria (Bawa et al., 2021b, 2021c). A similar concentration of Pb in the soils of food crops from non-pesticide sources was reported at 2.31 mg/kg, 27.3 mg/kg, and 4.31 mg/kg by Barau et al. (2018); Eliku & Leta (2017); and Kumar et al. (2017). This study observed a lower Cr concentration of 1.1 mg/kg in the soil of D. carota compared to 19.42 mg/kg and 5.75 mg/kg in the soil of food crops grown with metal-based pesticides in Nigeria (Bawa et al., 2021a, 2021c). However, similar concentrations of Cr 0.02 mg/kg, 0.69 mg/kg, and 1.17mg/kg were reported by other studies (Barau et al., 2018; Bawa et al., 2021b; Khanum et al., 2017).

The maximum concentration of Cu 31.50 observed in the soil of D. carota was comparatively lower than the 10.98, 2.10, and 26.33 mg/kg values obtained by (Bawa et al., 2021a, 2021c; Kumar et al., 2017). The maximum Zn concentration of 61.3 mg/kg in the soil of A. cepa obtained in this study was lower compared to the values of 89.50, 186.08, and 88.5 mg/kg reported by Bawa et al. (2021c, 2021b) and Eliku and Leta (2017). Generally, the application of metal-based pesticides has led to a higher accumulation of heavy metals in studied food crops compared to their corresponding soil concentration. Higher levels of heavy metals in plant tissues than in their equivalent soil suggest low soil retention and increased crop efficiency in metal absorption (Jolly et al., 2013). Among the studied food crops, the soil of D. carota and A. cepa showed a high concentration of heavy metals in their corresponding soil compared to other crops. This could be attributed to differences in plant metal absorption capacity (Hattab et al., 2019).

17. Bioaccumulation factor

Bioaccumulation factor (BAF) values for Cd, Pb, Cr, Cu, and Zn in the examined crops were 0.84–3.52, 0.19–2.80, 0.67–1.92, 0.46–2.98, and 0.32–5.7, respectively (Table 5). A. cepa had the maximum BAF value of 3.52 for Cd and 2.98 for Cu, respectively, while Z. mays had the highest BAF value of 1.92, 5.7, and 2.80 for Cr, Zn, and Pb, respectively (Table 5). Compared to other metals, zinc and cadmium had the highest bioaccumulation factor in all the crops studied, while chromium had the lowest (Table 5). This could be due to higher mobility of cadmium compared to other metals (Kulkarni, 2017). BAF >1 values were found in most of the crops studied, which could be attributed to the extensive use of cadmium-based chemical pesticides in the research locations. Furthermore, earlier studies have revealed that most pesticides used in northern Nigeria contain significant levels of cadmium and zinc (Bawa et al., 2021a; Yuguda et al., 2015). The trend of heavy metal transfer (BAF) from soil to crops was Zn >Cd> Cu> Pb> Cr. Bioaccumulation (BAF) has been identified as a significant medium for human metal exposure in the ecological food chain (S. Khan et al., 2008). High BAF values found in majority of the pesticide-treated crops investigated could be one of the reasons for human health concerns. Similar studies have observed significantly lower BAF values in food crops grown with wastewater irrigation in China Yang et al. (2018), Balkhair and Asharaf (2016) in Saudi Arabia, Eliku and Leta (2017) in Ethiopia, and Khanum et al. (2017) in Pakistan compared with values obtained in this study.

18. Correlation analysis

Correlation analysis was carried out among heavy metals in the investigated crops to determine the common sources of metals (Table 6). The result showed a significant positive correlation between Cd-Pb (r 0.55), Cd-Cr (r 0.58), Pb-Cr (0.61), and Cr-Cu (r 0.46), at p < 0.05 indicating that these metals were derived from the same origin.

19. Estimated hazard quotient

The calculated hazard quotient values of Cd, Pb, Cr, Cu, and Zn, through adult intake of all the tested crops were 0.105995–0.162038, 0.01523–0.13188, 5.08E-02-0.020306, 0.03290–0.06853, and 0.00772–0.01611, respectively (Table 7). The calculated hazard quotient values of Cd, Pb, Cr, Cu, and Zn, through the consumption of all the investigated crops for children, ranged from 0.248893 to 2.364488, 0.031112 to 0.280005, 0.041482 to 0.124447, 0.067201 to 0.140003, and 0.015763 to 0.032912 (Table 7). The calculated hazard quotient for all the studied metals through adult consumption of all food crops was <1 and are unlikely to pose a potential health risk (Table 7). However, the study observed HQ values>1 for Cd through children consumption of A. cepa, S. lycopersicum, and D. carota.

The results showed children will experience the greatest potential health through the consumption of A. cepa, S. lycopersicum, and D. carota. This might be due to farmers’ extensive use of chemical pesticides containing heavy metals and the metal’s increased mobility. The HQ values obtained from all of the crops investigated followed a descending trend of health risk. Cd >Pb> Cu> Zn> Cr. Previous studies have reported potential health risk (HQ) in food crops sprayed with pesticides containing metals in northern Nigeria (Bawa et al., 2021, 2021a, 2021b, 2021c) and in other countries (Table 8).

20. Hazard index

The calculated hazard index for all metals from the uptake of all the examined crops varied from 0.1644 to 0.41433 for adults and 0.50788 to 2.91724 for children (Tables 7 and 9). The calculated hazard index values through the ingestion of all the studied metals showed that children will experience severe health risks through the intake of most of the studied crops. HQ values through the ingestion of A.cepa, S. lycopersicum, and D. carota for children showed the highest risk among the studied crops. Similar hazard index values were reported by previous studies on food crops fumigated with pesticides in northern Nigeria, 1.097 in O. sativa (Bawa et al., 2021b), 1.38 in Z. mays (Bawa et al., 2021c), and 4.66 in O. sativa (Bawa et al., 2021c) and in other countries (Table 10 and 12).

Table 12. Comparison of bioaccumulation factor (BAF), hazard quotient (HQ) intake in the present study with some previous studies

Variable	Country	Authors	Source of heavy metals	Heavy metals
				Cd	Cr	Pb	Cu	Zn
BAF	Nigeria	Present study	Pesticides	3.2–0.84	0.67–1.92	0.19–2.80	0.46–2.98	0.32–5.7
	Nigeria	Barau et al. (2018)	Pesticides	1.46–3.31	1.75–10.2	0.18–0.49	———-	0.14–0.19
	Pakistan	Khanum et al. (2017)	Waste/water irrigation		0.906	0.390	———-	————
	India	Kumar et al. (2017)	Agricultura farm	————–	————	0.04–5.21	0.09–1.0	1.42–37.3
	Ethiopia	Eliku and Leta (2017)	Waste/water irrigation	0.3–0.44	0.02–0.16	0.01–0.02	0.09–0.1	0.09–0.16
	Nigeria	Oti (2015)	Mine sites	0.16	0.65	0.01	0.15	0.25
	Saudi Arabia	Balkhair and Asharaf (2016)	Waste water irrigation	0.099–0.18	1.67–1.82	1.01–1.04	0.01–0.02	———-
HQ	Nigeria	Present study	Pesticides	0.10–0.162	5.08E-02-0.02	0.01–0.13	0.03–0.06	0.007–0.01
	Nigeria	Barau et al. (2018)	Pesticides	1.51–17.89	0.01–0.01	1.29–15.3	———-	0.08–1.06
	China	Dai et al. (2017)	Market vegetables	0.324	———-	0.398	———-	———–
	India	Kumar et al. (2017)	Agricultura farm	—————-	———–	0.5590	0.0581	0.1018
	Nigeria	Patrick-Iwuanyanwu and Chioma (2017)	Market survey	7.435	0.008	3.487	———–	———
	Saudi Arabia	Balkhair and Asharaf (2016)	Waste water irrigation	2.904	2.279	1.803	0.873	———
	Ethiopia	Eliku and Leta (2017)	Waste/water irrigation	0.190	0.001	0.076	0.034	0.02

21. Estimated Target Cancer Risk (TCR)

The Target cancer risk is an estimate of the likelihood of the human population developing cancer through exposure to pollutants (NYSDOH, 2017). The New York State Department of Health categorized a Target Cancer Risk as follows: a value of less than 10⁻⁶ indicates minimal carcinogenic risk, a value of 10⁻⁵-10⁻³ indicates moderate cancer risk, and a value of 10⁻³-10⁻¹ indicates high cancer risk (NYSDOH, 2017). The TCR result for all the investigated food crops is presented in Table 13. The TCR values of Cr and Pb through the consumption of all the crops were within the range of 10⁻⁶ −10⁻⁵ indicating minimal to moderate risk of developing cancer. A similar study in Iran reported a high (TCR) value and risk of developing cancer for Cr and Pb (TCR 6.54 × 10⁻³,and 8.54 × 10^–04) compared to the values obtained in this study (Mohammadi et al., 2019). The TCR values of Cr and Pb obtained in the study for both adults and children are within the range of 4.4 × 10⁻⁰⁴, 6.1 × 10⁻⁰⁶ and 2.6 × 10⁻⁰⁵ , 1.5 × 10⁻⁰⁶ for children and adults reported in Bangladesh (Dhar et al., 2021). The estimated target cancer risk for Cr and Pb through the consumption of all the studied food crops grown with metal-based pesticides for both children and adults is within the moderate risk of developing cancer. However, continuous consumption of food crops cultivated with pesticides containing metals in Nigeria could lead to cancer risk.

Table 13. Comparison of Hazard index (HI) from present study with some previous studies

Parameter	Country	Authors	Source of heavy metals	Hazard index (HI)
HI	Nigeria	Present study	Pesticides	0.16–0.696
	Nigeria	Barau et al. (2018)	Pesticides	3.29–35.94
	China	Dai et al. (2017)	Market survey	0.00–2.08
	Nigeria	Patrick-Iwuanyanwu and Chioma (2017)	Market survey	0.370–8.871
	China	Zhong et al. (2017)	Agricultural farm	0.009–0.274
	Ethiopia	Eliku and Leta (2017)	Waste/water irrigation	0.028–0.071

22. Strength and limitations of the study

This study uncovered health risks in children for the first time in Paki from the consumption of food crops grown with metal-based pesticides. Findings from this study will provide information to medical practitioners on potential health risks associated with the consumption of heavy metals-contaminated food crops from the prolonged application of pesticides. Moreover, the outcome of this study will facilitate research on the formation of bio-pesticides that are safe, biodegradable, and environmentally friendly as an alternative to chemical pesticides. The scope of the study was limited only to some selected heavy metals and food crops cultivated in 2019 in Paki, Nigeria.

23. Conclusion

The consumption of food crops grown with metal-based pesticides and their associated health risks in northern Nigeria is a source of concern. This study found substantial quantities of heavy metals beyond the permitted the WHO limits for cadmium and lead in all of the food crops under study. The study revealed that the consumption of A. cepa, S. lycopersicum, and D. carota could expose children to high cadmium with its associated human health risks. The combined cumulative effects (HI) of all the metals through the intake of most of the investigated crops indicated that children will experience adverse non-carcinogenic health risks. The target cancer risk of Cr and Pb showed that the population is exposed to a minimal and moderate risk of developing cancer. Even though non-cancer risks was not detected, nonetheless increased long-term intake could result in cancer risk. Crops produced in the study area are transported to other neighbouring states, such as Kano and Jigawa, and thus the health risks extend beyond just Paki or Kaduna state. The level of heavy metals and their health risks in food crops grown with metal-based pesticides were comparatively similar to the values obtained in food crops grown with wastewater and other sources. Heavy metal sources in food crops sprayed with metal-based pesticides should not be ignored. Effective monitoring and regulation of heavy metals in pesticides by regulatory agencies in Nigeria should be enforced.

Disclosure statement

No potential conflict of interest was reported by the author.

Dr. Usman Bawa has a PhD in Ecology and Environmental Biologist in the department of Biological Sciences, Bayero University, Kano with specialisation in ecotoxicology, pollution, and biodiversity conservation.

Additional information

Funding

This research receives no funding.