Carcinogenic and Non-carcinogenic Risk Assessment Induced by Pesticide Residues in Fresh Pistachio in Iran Based on Monte Carlo Simulation

doi:10.21203/rs.3.rs-2069924/v1

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Carcinogenic and Non-carcinogenic Risk Assessment Induced by Pesticide Residues in Fresh Pistachio in Iran Based on Monte Carlo Simulation

https://doi.org/10.21203/rs.3.rs-2069924/v1

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This research is aimed at analysis 88 pesticides in 30 fresh pistachio samples prepared from stores in Iran by QuEChERS-Ultra-High Performance Liquid Chromatography-tandem mass spectrometry (UHPLC-MS/MS). The results showed at least one pesticide was in 67% of fresh pistachio samples. Kresoxim methyl residue was detected in 20 samples with average of 0.11 mg kg^− 1, this average is 2.2 times more than MRL. buprofezin in 5 samples with average of 0.17 mg kg^− 1 was observed with 3.4 times more than MRL, hexaconazole and permethrin were recognized in 3 samples lower than MRL with average residue of 0.030 and 0.028 mg kg^− 1, respectively. In addition, potential non-carcinogenic and carcinogenic health risk assessments were evaluated using probabilistic methods performed with the Monte Carlo simulation algorithm. The order of pesticide ranking based on HQ was hexaconazole > buprofezin > permethrin > kresoxim methyl. Total HQ (HI) was 2.0E-4 and for children 9.0E-4 hence it means fresh pistachio consuming maybe not have significant short-term health risks for cosumers. Ranking based on CR was hexaconazole > kresoxim methyl > metalaxyl > permethrin > buprofezin. However, total CR due to pesticide residues was not higher than 1E-6 value (1.09E-9) therefore, consumers were not at significant risk of carcinogenicity in this product.

Pesticide residue

Health risk assessment

Monte Carlo simulation

Fresh Pistachio

UHPLC-MS/MS

Chemical and microbial contamination of food has become a global concern in the last two decades(Gao et al. 2022, Guo et al. 2021, He et al. 2021, Luo et al. 2022, Su et al. 2021, Sun et al. 2022, Wang et al. 2021). Until protect the crop and prevent economic loss, use of pesticides is inevitable. However, the inappropriate use of pesticides can lead to crop pollution and raise a major food safety risk across the world (Masi´ A. et al. 2014, Tongjai et al. 2021). One of the most significant agricultural crops of Iran is pistachio (Pistaciav era L.), which plays an important role in the world trade (Faraji et al. 2018). Pistachio belongs to the Anacardiaceae family (AL-Saghir 2010), and was used as a common nut and employed for production of different products including pistachio nut, cakes, and ice creams. Pistachio nut is a dietary source of phytochemicals such as antioxidant compounds, vitamins, minerals, phytosterols, and fiber. Phytoestrogens as antioxidant compound prevents cancer and cardiovascular diseases (Gentile et al. 2007). The phytosterols of pistachios can decrease low density cholesterol (LDL) (Kocyigit et al. 2006). The pistachio tree grows in the dry areas of Asia and distributed in the Mediterranean zone. One of the most suppliers of pistachio nuts worldwide is Iran (Mahdavi et al. 2020).

The most common way for protection, conservation and increase the yield of product is the use of chemical pesticides (Panahi et al. 2013). Besides the advantage of the pesticides usage, their application raise different problems like as decrease of nitrogen fixation, and endangering the living organism ecosystems. According to vast usage, accumulative nature and low level of biodegradability, pesticides aggregate in products and enter the human body through diet (Pandey et al. 2010, Taghizadeh et al. 2019), which is five times of the other routes as water and air. They have many adverse health effects such as blindness, headache, nausea, and especially chronic diseases including, liver damage, neurologic disorders, cancers, endocrine problems and genotoxicity (Hulin et al. 2014, Ilyushina et al. 2020, Mazloomi &Sefidkar 2015, Zhang et al. 2019).

The maximum allowable content of pesticide residue in food products is called maximum residue limit (MRL). In order to reduce the associated risk for consumers, residues of pesticides must be less than MRLs in foods that is depended on proper use of pesticides as rate of application, employing permitted pesticides and required pre-harvest intervals (Anastassiades &lehotay 2003).

With the increase of consumer awareness and more demand on safe and healthy foods, pesticides monitoring in foods were employed in the countries (Arabameri et al. 2020). Based on literature review, different studies report the pesticides residue in crops and products (Cebi et al. 2021, Hulin et al. 2014, Ilyushina et al. 2020, Masi´ A. et al. 2014, Pandey et al. 2010, Shi et al. 2011, Taghizadeh et al. 2019) especially pistachio (Arabameri et al. 2020, Kocyigit et al. 2006). Different studies have investigated residue of pesticides in various foods by diverse extraction methods and devices. Measurement of pesticides performed by different instruments such as gas chromatography-mass spectrometry (GC-MS), Ultra-high performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS). (Behbahan et al. 2021, Cajka et al. 2012, Fernandes et al. 2018, García-Valc´ arcel &Tadeo 2009, Pelle et al. 2016). Recent studies suggest liquid chromatography (García-Valc´ arcel &Tadeo) equipped with mass spectrometry (MS) as a gold standard techniques for quantitative analysis of food pollutants (Cebi et al. 2018) as like as pesticides (Shi et al. 2011). The LC-MS method has recently become more valuable than GC because of pesticides’ properties considering the analysis of thermal sensitive, polar and non-volatile pesticides (Masi´ A. et al. 2014). Due to complex matrix of foods and trace residues, sample preparation is a major need. QuEChERS method provide a prepared sample preparation to measure multiple residues (Faraji et al. 2018). A few studies used UHPLC-MS/MS systems for measurement of pesticides in nuts (Cebi et al. 2021, Faraji et al. 2018, Tajdar-oranj et al. 2021). Here identification and measurement of 88 pesticides in pistachio by employing the QuEChERS sample preparation with UHPLC-MS/MS was identified and measured. In Iran, 36 different pesticides have been registered or recommended to control pistachio pests, and more than 50% of them have been investigated in this monitoring insecticides including acetamiprid, imidacloprid, thiacloprid, thiamethoxam as neonicotinoids; diazinon, ethion, fenamiphos, fenitrothion, fenthion, malathion, phosalone, pirimiphos-methyl as organophosphate; fenoxycarb and thiodicarb as carbamate; lufenuron as benzoylurea; permethrin as pyrethroid; spirotetramat as tetramic acid and fenpyroximate as pyrazole acaricide. As different pesticides used in countries and also in different farms, this study aimed to determine the residues of 88 pesticides simultaneously in fresh pistachio by using the UHPLC-MS/MS. Moreover, fresh pistachio consumer’s dietary health risk was also determined.

2.1. Chemicals and reagents

Analytical standards of pesticides with 97.5 to 99.9% purity, were purchased from Bayer Crop Science (Frankfurt, Germany), Fluka (Buchs, Switzerland), Sigma Aldrich (Schnelldorf, Germany), Syngenta (Tokyo, Japan) and Dr. Ehrenstorfer GmbH (Augsburg, Germany) and the individual stock solutions was prepared in ACN with keeping at -18°C. The required solvents, including acetonitrile were obtained from Biochem Co. (Darmstadt, Germany) and deionized water produced by Direct-Q® 3 UV water purification system (Millipore, Bedford, MA, USA). QuEChERS materials such as sodium chloride, and magnesium sulfate were purchased from Merck and Carlo Ebra companies, respectively, and sodium acetate, C18, Graphitized Carbon Black (GCB) and Primary Secondary Amin (PSA) were obtained by Agilent Co. (Santa, California, USA).

2.2. Sample collection

30 fresh pistachio samples were collected in August and September 2020 from different shops and markets in Iran. All samples were not packaged with randomly selection and in combination to obtain the deputy sample (> 1 kg). Paper bags were used to store the sample, the sample was prepared daily and then stored in a freezer at -21 ° C for analysis. As a control an organic sample were purchased from a local market(Santana-Mayor et al. 2019).

2.2. Extraction and sample preparation

For pesticide residues extraction, QuEChERS method was used (Mahdavi et al. 2020). 100 g of pistachio kernels blended and homogenized with 100 g deionized cold water, after 1 h shaking, 20 g of pistachio paste was weighed, and the first extraction step was done by addition of 10 ml of acetonitrile (1% acetic acid). Subsequent, 4 g of anhydrous MgSO₄, 1 g of NaCl and 1.5 g of NaOAc were added to integrate the extraction procedure then vortexed vigorously for 1 min and centrifuged at 3450 rpm for 5 min. Next, 10 ml of the supernatant was transferred to a 15-ml falcon for the clean-up stage after keep overnight in freezer. Clean-up was completed with PSA, C₁₈ and GCB. Again the mixture was 1 min vortexed, and centrifuged 3 min at 3450 rpm. 1 ml of top layer was filtered with 0.45 µm PTFE and injected to UHPLC-MS/MS. Extraction procedure summarized in Fig. 1.

2.3. Ultra-high performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS)

An LC-MS instrument (Agilent, Model 6410)-triple quadruple was used. Separation was done by Agilent LC, 1200 with SB-C₁₈ column, Zorbax Eclipse (3.0×50.0 mm, 1.8 µm). Acetonitrile and water (0.1% formic acid) were as mobile phase, and the elution program was as follows: at first with 10–100% acetonitrile in 13 min, and return to the initial condition from 13 to 20 min. The rate of mobile phase was 0.6 ml min^− 1(Anagnostopoulos &Miliadis 2013). Results including optimized MS parameters and retention times of each pesticides indicated in supplementary Table 1S.

2.4. Validation Evaluation

Matrix effect evaluated with comparison of calibration curves’ slopes of pesticides in the solvent and matrix of fresh pistachio. Nine different concentrations of spiked solutions, 0.005, 0.01, 0.015, 0.025, 0.05, 0.1, 0.25, 0.5 and 1.0 mg kg^− 1 were prepared. As shown in Table 2S, the LOQ values were calculated based on SANTE guideline (SANTE 2015) with RSD lower than 20%. Two different concentrations, 0.1 and 0.5 mg kg^− 1 were spiked for recovery evaluation. Results are illustrated in the Table 3S.

2.5. Health risk assessment

The hazard quotient (HQ) of fresh pistachio consumption assessed by the equations 1 and 2:

Chronic daily intake (CDI) was computed by:

\(\text{C}\text{D}\text{I}=\frac{\text{C}\times \text{I}\text{R}\times \text{E}\text{F}\times \text{E}\text{D}}{\text{B}\text{W} \times \text{A}\text{T}}\) Eq. 1

C is pesticide residue (mg kg^− 1); IR, per capita consumption (kg day^− 1); EF, frequency of exposure, ED, duration of exposure. BW, body weight 15 kg and 70 kg for children and adults; AT, average lifetime (EF×ED). Pistachio consumption is 0.3 kg year^− 1 (Eslami et al. 2021).

\(\text{H}\text{Q}=\frac{\text{C}\text{D}\text{I}}{\text{R}\text{f}\text{D}}\) Eq. 2

Hazard index (HI) was assessed:

\(\text{H}\text{I}=\sum HQ=\text{H}\text{Q}1+\text{H}\text{Q}2+\dots +\text{H}\text{Q}\text{n}\) Eq. 3

Risk is not significant when HI ≤ 1, in HI > 1, health risk concern is noticeable.

The United States Environmental Protection Agency (US-EPA, 2005) ≤ 1E-6 index was used for cancer assessment by Eq. (4):

\(\text{C}\text{R}=\) CDI × CSF Eq. 4

Probabilistic algorithm Monte Carlo simulation (MCS) was used (Van Der Voet &Slob 2007). In MCS, Crystal Ball (version 11.1.2.4.600 (32-bit) Oracle, Inc., USA) applied for non-carcinogen and carcinogen risks assessment. Trial numbers set at 100,000 iteration, and criteria for consumers' risk assigned 95% (Qu et al. 2012).

3.1. Validation

88 pesticide residues were analyzed in total number of 30 fresh pistachio samples as an important pesticides in pistachio harvesting. Spiked standard solutions were performed at 0.005, 0.01, 0.015, 0.025, 0.05, 0.1, 0.25, 0.5 and 1.0 mg kg^− 1 levels in solvent and in pistachio matrix. Linear dynamic range was 0.01–1.0 mg kg^− 1. Table 3S describe pesticide recoveries averages was 70.2–115.1% with RSD < 16.5%. Similar validation parameters was reported by Antonio Molina-Díaz(Gilbert-López et al. 2010) and many other studies these parameters are approved by SANTE (2015) guideline.

The average amount of pesticides in fresh pistachio samples are summarized in Table 1. Among 30 samples, 67% contained residues, 17% of samples had multiple residues and about 10% more pesticide residues. Generally, buprofezin, hexaconazole, kresoxim methyl and permethrin were found with the most frequency. The highest excess to MRLs observed for buprofezin and kresoxim methyl with average residual values to national MRL of 3.40 and 2.20 ratio respectively. The most common pesticides found in fresh pistachio were kresoxim methyl (67%) as strobilurin pesticide class, buprofezin (17%) as thiadiazine pesticide, hexaconazole (10%) as a triazole and permethrin (10%). Among the pesticides observed in the pistachio samples, only permethrin is recommended. The other observed pesticides were used illegally in the pistachio orchards or as a result of cross- contamination from the surrounding fields and orchards.

Table 1

Concentration levels of pesticide residues monitoring in fresh pistachio samples (mg kg^− 1).
Pesticide	Chemical category	Frequency	Average Residue (%RSD)	National MRL	Average Residue/MRL
buprofezin	thiadiazine	5	0.17 ± 0.020	0.05	3.40
hexaconazole	triazoles	3	0.03 ± 0.0010	0.05	0.60
kresoxim methyl	strobilurin	20	0.11 ± 0.010	0.05	2.20
permethrin	pyrethroid	3	0.028 ± 0.0050	0.1	0.28

3.2. Health Risk Assessment

3.2.1. Non-Carcinogenic risk

Figures 2 and 3 show HQ values. HQ rank order of pesticides in adults in fresh pistachio was hexaconazole > buprofezin > permethrin > kresoxim methyl, 1.8E-4, 1.2E-5, 6.7E-6, and 3.7E-6, respectively. While HQ in the children was 8.4E-4, 5.6E-5, 3.1E-5 and 1.7E-5 with the same rank order. Based on the results defined in Figs. 2 and 3, HQ of four pesticides detected in fresh pistachio were lower than 1. As shown in Fig. 4, HI in the adults was 2.0E-4, and in the children was 9.0E-4 respectively. HI < 1, means the consumption of fresh pistachio may not be health concerns. However, for residues in some samples more than MRL especially buprofezin and kresoxim methyl, long-term consumption of fresh pistachios requires more attention to harvest.

3.2.2. Carcinogenic risk

Cancer diet was evaluated for the Iranian household. To evaluate the cancer risk, the average 70 years exposure is multiplied by the cancer slope (Q₁*).

As shown in Fig. 5; CR rank order of adults was hexaconazole > kresoxim methyl > permethrin > buprofezin with value of 4.7E-10, 3.4E-10, 2.8E-10 and 5.2E-13.

TCR of hexaconazole, kresoxim methyl, buprofezin and hexaconazole was 1.1E-9, about 1000 times lower than the 1E-6 value as shown in Fig. 6.

Consumption of fresh pistachios is limited to end of summer and early autumn, which is offered to people in shops for about one month. The common consumption of pistachios is in dried form and usually after long storage. Therefore, it is expected that the pesticides detected in fresh pistachios are different from dried, roasted or processed pistachios. In this study only fresh pistachios have been studied and because of low consumption of this commodity, HI and TCR are in low and safe levels.

To ensure food safety, a QuEChERS-UHPLC-MS/MS procedure was used to investigate 88 residues of pesticides in fresh pistachio has been developed. This methodology could be used in the pesticide laboratories as a reliable and valid method to multi-analysis of pesticides. Previous studies show the efficiency of the QuEChERS for determining 12 pesticides in pistachio by GC–MS (Emami et al. 2017) and 77 pesticides in hazelnuts by LC-MS/MS (Cebi et al. 2021). Their recovery and the RSD values were compatible with the present study.

Findings of current study showed that 67% of samples contained pesticide residues, 17% of them had multiple residual (2 kinds at least) and about 10% with more one pesticides. To date, few studies have been conducted to investigate pesticide residues in pistachio using UHPLC-MS/MS or LC-MS/MS method. Tajdar-oranj et al. (2021) investigated 25 pesticides in pistachio samples by UHPLC-MS/MS. They found acetamiprid (53%), fenitrothion (39%), imidacloprid (34%), and thiacloprid (25%) as the most frequent (Tajdar-oranj et al. 2021), that were not detected in the current study. Another study reported the 18 residues of various pesticides in different pistachio cultivers, Iran by GC–MS (Taghizadeh et al. 2019). They determined permethrin as 0.013 mg kg^− 1 which was less than this study. Arabameri et al. (2020) observed 0.011 mg kg^− 1 of permethrin in pistachio nuts of Damghan, Iran (Arabameri et al. 2020). Emami et al. (2017) observed diazinon, carbaryl and fenitrothion in pistachio (Emami et al. 2017), but they not detected in this study. Faraji et al. (2018) approved a QuEChERS-LC-MS/MS method for the concurrent determination of neonicotinoid pesticides in pistachio samples. They found all analytes 2 hours and 14 days after spraying in pistachios (Faraji et al. 2018). Acetamiprid and thiacloprid were detected in 27% of the pistachio samples whereas the other pesticides, including kresoxim methyl, permethrin, hexaconazole and buprofezin were not detected (Aydin &Ulvi 2019). According to vast literature review, no study detects kresoxim methyl, hexaconazole and buprofezin in samples and the current study is the first report of detection of these pesticides. The current study showed detected pesticides, including kresoxim methyl and buprofezin were above the MRL.

In the current study, there were no carcinogenic and non-carcinogenic risks in pistachio. This finding was observed for pistachio nuts as well (Arabameri et al. 2020).

Overall 85 pesticides were extracted by use of QuEChERS and investigated with UHPLC-MS/MS technique in apple and grapes in West Azerbaijan, Iran. Assessment of health risk showed that HI value for apple and grape consumption was less than 1 in adult and children and has no risk (Mahdavi et al. 2021). Among 16 investigated pesticides, 5 samples including acetamiprid, chlorpyrifos, diazinon, fenitrothion, and imidacloprid were detected in 28 date samples (Eslami et al. 2021). Diazinon content in 12 samples and imidacloprid in 1 sample was higher than MRL. The other residues was lower than MRLs. Results of risk assessment showed no risk for consumption of date fruits during lifetime (Eslami et al. 2021). Pelle et al. (2016) studied pesticides residues (malathion, pirimiphos methyl, chlorpyrifos methyl, and chlorpyrifos ethyl) in wheat samples and found that all samples had lower than MRL (Pelle et al. 2016). As the health risk assessment in these studies shows no risk for consumption but monitoring of pesticides in agricultural food are necessary. Overall, the results of this investigation would be helpful for the Iranian government regulations on the safe and proper application of pesticides in pistachio. Effective planning and management programs to operate out Good Agriculture Practices (GAP) (such as pre-harvest and safety intervals) by farmers and use authorized pesticides are recommended to control pesticide applications, especially in this case from detected pesticides only permethrin is recommended other pesticides like as kresoxim methyl, hexaconazole and buprofezin are not registered in control pistachio pests.

In current study, an approved method using a QuEChERS-UHPLC-MS/MS was developed to evaluate of 88 pesticides in 30 samples of fresh pistachio. HI in adults and children were 0.0002 and 0.0009 in fresh pistachio, respectively. Nonetheless, risk of carcinogen due to buprofezin, hexaconazole, kresoxim methyl and permethrin was 1.1E-9 and thousand times lower than 1.0E-6 of carcinogenic limit. Therefore, it seems that consuming fresh pistachios may not pose significant health risks in the short-term exposures and is not carcinogen. Due to detected some residues in some fresh pistachio samples seems required to implement control plans (e.g., GAP and/or IPM) to manage the proper application of these pesticide because Iranian pistachios are unique in terms of appearance and taste, in order to maintain their international position in world trade, it is very important to pay attention to the safety of this valuable food.

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Conflict of interest

The authors declare no conflict of interest relevant to this article.

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Authors contributions

Vahideh Mahdavi: Supervision, Investigation, Resources, Conceptualization, Risk Assessment, Methodology, Writing original draft; Tayebeh Zeinali and Parisa Sadighara: Sampling and analysis of pesticide, Data curation; Tayebeh Zeinali: Literature Searching, Writing & Editing; Sharaf S. Omar: Writing & Editing , Review & Editing ; Yadolah Fakhri: Supervision, Risk Assessment, Review & Editing

Acknowledgment

Iranian Research Institute of Plant Protection (IRIPP) is acknowledged for support of this study.

Funding

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Carcinogenic and Non-carcinogenic Risk Assessment Induced by Pesticide Residues in Fresh Pistachio in Iran Based on Monte Carlo Simulation

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Abstract

Figures

1. Introduction

2. Materials And Methods

2.1. Chemicals and reagents

2.2. Sample collection

2.2. Extraction and sample preparation

2.3. Ultra-high performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS)

2.4. Validation Evaluation

2.5. Health risk assessment

3. Results

3.1. Validation

3.2. Health Risk Assessment

3.2.1. Non-Carcinogenic risk

3.2.2. Carcinogenic risk

4. Discussion

5. Conclusion

Declarations

References

Supplementary Files

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