Pesticide residues and associated health effects in marketed fruits in Saudi Arabia

1 Introduction

Fruits are one of the supplementary sources of carbohydrates, lipids, vitamins, minerals, antioxidants and other important nutrients. The consumption of these commodities with vegetables is almost 160 kg/per capita/year (OECD/EU 2010). High intake of fruits has been encouraged to prevent micronutrient deficiencies and reduce the incidence of major diseases such as cancer cardiovascular diseases and obesity (Qin, Chen et al. 2021). However, fresh fruit consumption can also be potential sources of harmful and toxic substances accumulated from its cultivation. Thus, food safety has become a major public concern worldwide (Radwan and Salama 2006).

Pesticides are defined as substances or mixtures of substances that are widely recognized to play an important role in agriculture, plant crops against pests, weeds, and disease (US-EPA 2018). Certainly, its use has increased the quantity and quality of crop yields as well as reduced harvest losses. More than a thousand pesticides are in active use globally, mostly manufactured to selectively destroy specific pests. They are generally classified as insecticides, herbicides, fungicides and rodenticides, to name a few (Turinek, Grobelnik-Mlakar et al. 2009, Selim, El-Saeid et al. 2011, Sarkar, Gil et al. 2021). Currently, the use of pesticides has increased as they are less labor intensive than other pest control strategies, aside from the increased demand for food supply (Farha, Abd El-Aty et al. 2018). All pesticides are inherently toxic, and hence, are potentially hazardous to humans and animals through exposure or dietary intake. These issues led to widespread concern over the potential adverse effects of these pesticides on human health when exposed through different routes, including skin contact, ingestion, or inhalation (Tudi, Li et al. 2022). Pesticide exposure through ingestion was found more harmful than skin contact (Juraske, Mutel et al. 2009), putting raw intake of fruits and vegetables from unknown sources potentially damaging (Kumari, Kumar et al. 2001). Pesticide contact even at low doses can cause acute detrimental side effects with symptoms such as headaches, rashes, dizziness, nausea, and long-term consequences, including malignancy, multi-system toxicity, birth and fertility issues, and disruption of the metabolic system (Alavanja, Ross et al. 2013). Globally, 385 million cases recorded in 2020 were attributed to inadvertent acute pesticide poisoning, 11,000 of which were fatal (Boedeker, Watts et al. 2020). Agricultural workers and pesticide applicators are more prone to pesticide exposure (Willenbockel, Prinz et al. 2022). Many countries have passed laws to limit pesticide residues exposure via the establishment of the maximum residue limits (MRLs) (Ramadan, Abdel-Hamid et al. 2020).

Pesticide exposure has increased rapidly in Saudi Arabia (SA) as the development of agriculture increased (Saggu, Rehman et al. 2016). Recently, many researches were carried out in several Saudi agriculture regions for pesticide analysis and reported the persistence of residual pesticides in different commodities (Osman, Al-Humaid et al. 2010, Selim, El-Saeid et al. 2011). Al-Wabel and others used simple micro-wave-assisted extraction (MAE) technique in monitored a residue of different chemical groups of pesticides in soil samples collected from 15 regions in SA (Al-Wabel, El-Saeid et al. 2011). In a study conducted in the Al-Qassim region, pesticide residues were examined in 160 vegetable samples. The results indicated that the most often discovered pesticide residues (carbaryl, biphenyl, and carbofuran) had MRL values that were surpassed mostly in cabbage, squash, green pepper, and carrots. (Osman, Al-Humaid et al. 2011). In this work, we used a developed, validated, sensitive and expeditious multiresidue “QuEChERS” method to evaluate residues of 412 pesticides residues including different chemical groups of pesticides which used in controlling the agricultural pests in various eleven vegetable and fruit types of the Saudi markets. It is worthy to note that several other techniques for agriculture products are available for assessing quality and safety including quantifying pesticide residues such as the matrix solid phase dispersion (MSPD) technique (Mujahid, Latif et al. 2022), near infrared (NIR) spectroscopy for quality inspection (Wang, Wang et al. 2023, Zhang, Wang et al. 2024), in situ optical sensing system for monitoring (Wang, Zhang et al. 2023) to name a few, most of which have arguably not been documented in SA.

There is limited data available on the levels of pesticide residues in fruits sold in local markets of SA. Therefore, this study's goal was to evaluate contamination by pesticides residues in fruits collected from different local markets during 2020 to 2022 to provide useful contamination data for relevant decision makers in SA to be used as a reference for the future monitoring.

2 Materials and methods

3 Results

Based on analytical studies of pesticides residues for 161 samples of different types of fruits (Table 1 & Fig. 1), pesticides residues were not detected in only 10 (6.2 %) analyzed samples. The rest of the 151 (93.8 %) samples were overwhelmingly contaminated. In most of the analyzed samples, 132 (87.4 %) pesticide residues were below the MRLs. whereas, 19 samples (11.8 %) contain pesticide residues above safety limits. Pesticide residue levels were compared to EU-MRLs (Osman, Al-Humaid et al. 2011).

Close

Fig. 1

Percentage of fruits according to contamination and MRL status.

Export to PPT

Results in Table 2 revealed that the 44 compounds detected in 151 contaminated samples belonged to different pesticides groups (organophosphates, pyrethroids, organochlorines, neonicotinoid, fungicides etc.). Using the WHO (2019) classification, 23 pesticides were moderately hazardous (class-II), 10 pesticides belonged to class III (slightly hazardous), 8 compounds were in class U (unlikely to pose an acute hazard with normal use), while 3 highly toxic compounds (class Ib and Ia) were detected. 40.91 % of the detected pesticides were fungicides. Likewise, 40.91 % were insecticides. Acaricide and nematicides represent 9.09 % and 6.82 % respectively, while 2.72 % belonged to herbicides (Fig. 2).

Close

Fig. 2

Classification of the detected pesticide residues and their percentage.

Export to PPT

Table 3 and Fig. 3 showed the frequency and concentration of pesticide residues in the analyzed samples. The fruits contaminated with 44 types of pesticides are shown below with different percentages:

Close

Fig. 3

Frequency of presence of pesticide residues in different types of collected fruit samples.

Export to PPT

4 Discussion

In this study, 161 samples of 12 different types of locally purchased fruits in SA were analyzed for pesticide residues and concomitant health risk. Pesticide residues were found in 151 (94 %) samples. While most analyzed samples (87.4 %) had pesticide residues below MRLs, around 12 % contained pesticide residues above safety limits. Our study revealed that 44 pesticides belonged to different chemical groups were detected in 151 contaminated fruit samples. 40.91 % of the detected pesticides belong to fungicides pesticides. 40.91 % belong to insecticides. 2.72 % belong to herbicides. However, acaricide and nematicides represented 9.09 % and 6.82 % respectively. The findings indicated that eight chemicals were in class U, ten pesticides were in class III (slightly hazardous), twenty-three pesticides were classified as moderately harmful (class II), and three very toxic compounds (class Ib and Ia) were also found. The use of different types of pesticides to protect fruits against pests may accumulate multiple residues in samples (Łozowicka, Kaczyński et al. 2012). Several pesticide residues were found in 1,146 samples of fruits and vegetables in Incheon, Korea belonged to different types of pesticides [15 fungicides (46.9 %), 14 insecticides (43.7 %), 2 herbicides (6.3 %) and 1 growth regulator (3.1 %)] that had different toxicity levels (Park, Kwon et al. 2022). In Egypt, reported pesticide residues were estimated in 176 samples of the most popularly consumed vegetables collected from markets in Dakahlia, Egypt, and revealed that 111 (63.1 %) samples were contaminated with pesticide residues of which 29 samples (16.5 %) had higher than the maximum residue limits (MRL) (Shalaby, Abdou et al. 2021). Moreover, our results revealed that each of 11 types of analyzed samples had multiple of pesticides residues some of these residues exceeds MRLs established by EU may result from misinformed farmers on the proper methods, and pre-harvest intervals for pesticide application. Inadequate supervision by relevant departments, a lack of proper guidance regarding the application of pesticides, and non-compliance with best agricultural practices can also result in contaminated fruit and vegetables, which are thought to pose a risk to consumer health (Li, Nie et al. 2018, Yu, Hu et al. 2018). To assess risk of human exposure to the pesticide residues, individual components of dietary intakes were taken according to 13 GEMS/Food Consumption Cluster Diets based on FAO Food Balance Sheet data from 183 countries (Vandevijvere, Monteiro et al. 2013). Results of the present study showed that the consumption of orange > grapes > pomegranate > banana > mandarin > apple > pear > apricot > fig > lemon > peach > kiwi. Risk assessment was calculated separately for individual pesticides detected positively in each type of collected fruit. The well-developed assessment method considers the average exposure levels in comparison to the ADI values set for specific pesticides. Consumers exposed to persistently harmful pesticide residues would only be at risk for health problems if they consumed more food than the ADI on a daily basis for an extended period of time. The estimated daily intake (EDI) was compared with ADI to calculate hazard Index (HI) and Hazard Risk (HR) if the EDI was less than ADI then HI is less than one that mean there was no hazard risk on consumers (Akoto, Azuure et al. 2016). Our results revealed that most of the investigated samples had hazard index below one so there was no risk dangerous on human health these findings were in consistence within (Liu, Bei et al. 2023). The dietary risk assessment of pesticide residues in analyzed fruit samples revealed that HQa for all pesticides did not exceed the unit value (HQa < 1). Therefore, the pesticide residues in these fruits can be considered safe for human consumption (Hossain, Fakhruddin et al. 2015), and that while the individual and cumulative health risk assessments linked to pesticide exposure in vegetables revealed minimal effects on consumers, the intake of vegetables and fruits can raise concerns due to the consumption of uncooked foods that may be unwashed. As observed in the present study, the most consumed fruits (orange, grapes and pomegranate) were contaminated with fluopyram, imazalil, chlorpyrifos, finamiphos and indoxacarb respectively. In addition to malathion detected in peach with limits exceeding MRLs. Typically, a scientific risk assessment is used to set MRLs (Torres, Picó et al. 1996) and control pesticide residue regulations, which vary among nations because of various agricultural circumstances that directly affect pesticide application rate (Wang, Wang et al. 2013). Exceeding MRLs may be due to non-compliance, contamination from a prior use of persistent pesticides, cross-contamination or spray drift, and/or unexpectedly slow pesticide residue degradation (Wang, Wang et al. 2013). In addition, the calculated HI of the previous detected pesticides in the present study were more than one. These findings suggested that pesticide residues in samples may accumulate over time and could be the root cause of harmful long-term impacts on human health. Health risk would be done if dietary intake exceeded the ADI every day for an extended period of time (Gad Alla, Thabet et al. 2013). As the detected pesticides belongs to different chemical classes long exposure period may elicit cancer development (Araoud, Gazzah et al. 2012). Meanwhile, long-term pesticide exposure to parents or kids can cause a variety of cancers in kids, including brain tumors, lymphomas, leukemia, neurological disorders, colorectal cancer, germ cell cancer, Hodgkin's disease, eye cancer, kidney, liver, thyroid, and skin cancer. However, pesticides are linked to a number of malignancies, including adult leukemia. Cancers of the brain, testicles, lungs, ovary, pancreas, prostate, bladder, kidney, stomach, colon, rectal, lip, and connective tissue (Watts 2012).

The authors acknowledge some limitations. While the fruits were purchased locally, it was difficult to confirm whether they were harvested within or imported elsewhere, since SA imports most of its produce. Further investigations targeting only locally grown crops could provide a clearer picture of the pesticide residue status within the domestic sphere. Lastly, while the use of QuEChERS, LC-MS/MS and GC–MS/MS was chosen for low cost accuracy, the authors do acknowledge emerging techniques for enhanced detection and monitoring of agriculture products such as plasmon enhanced sensors (Singh, Pombeiro et al. 2024), metal organic frameworks (MOFs) based luminescent and electrochemical sensors (Mohan, Singh et al. 2023), nanocomposite platforms(Mohan, Virender et al. 2024) and metal organic framework (MOF) materials (Mohan, Kamboj et al. 2023) should be considered in future studies, in collaboration with experts, to reinforce findings and transfer technology in SA.

5 Conclusions

In conclusion, 161 samples of 12 different types of locally purchased fruits in SA different markets were analyzed for pesticide residues. 44 Pesticide residues were found in 151 (94 %) samples. While most analyzed samples (87.4 %) had pesticide residues below MRLs, around 12 % contained pesticide residues above safety limits. HIs of detected pesticides indicate that majority were less than one and therefore pose no risk. Orange, grapes and pomegranate were the most consumed fruit types contaminated with pesticide residues fluopyram, imazalil, chlorpyrifos, finamiphos and indoxacarb with level exceeds MRLs having HIs > 1. Fruits purchased from SA markets might still be harmful to people's health; thus, care should be taken. Regular monitoring of local agricultural products, as well as using good agricultural practices, is necessary to eventually reduce the usage of highly toxic pesticides. The results provide important information about the current state of pollution in marketed fruits in different Saudimarkets. The obtained data can be used to develop strategies and improve pesticide MRLs for the safe management of vegetables in SA.

Funding

This project was funded by the National Plan for Science, Technology and Innovation (MAARIFAH), King Abdulaziz City for Science and Technology, Kingdom of Saudi Arabia (Award No: 14-ENV2482-02).

CRediT authorship contribution statement

Majed S. Alokail: Writing – review & editing, Funding acquisition, Conceptualization. Manal E.A. Elhalwagy: Writing – original draft, Formal analysis, Data curation. Sherif H. Abd-Alrahman: Writing – review & editing, Supervision, Investigation, Formal analysis. Abdullah M. Alnaami: Writing – review & editing, Methodology, Investigation. Syed D. Hussain: Writing – review & editing, Formal analysis. Osama E. Amer: Writing – review & editing, Investigation, Data curation. Shaun Sabico: Writing – review & editing, Project administration, Investigation. Nasser M. Al-Daghri: Writing – review & editing, Project administration, Investigation.