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Dietary Intake of Pesticides Based on VegetableConsumption in Ismailia, Egypt. A Case StudyMohamed Tawfic Ahmed a , Sarah Greish a , Saad M Ismail a , Yahia Mosleh a , Naglaa MLoutfy a & Amina El Doussouki ba Plant Protection Department, Suez Canal University, Ismailia, Egyptb Department of Pathology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia,EgyptAccepted author version posted online: 26 Feb 2013.

To cite this article: Human and Ecological Risk Assessment: An International Journal (2013): Dietary Intake of PesticidesBased on Vegetable Consumption in Ismailia, Egypt. A Case Study, Human and Ecological Risk Assessment: An InternationalJournal, DOI: 10.1080/10807039.2013.775893

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Dietary Intake of Pesticides Based on Vegetable Consumption in Ismailia, Egypt. A Case

Study

Mohamed Tawfic Ahmed,1 Sarah Greish,

1 Saad M Ismail,

1 Yahia Mosleh,

1 Naglaa M

Loutfy,1 and Amina El Doussouki

2

1Plant Protection Department, Suez Canal University, Ismailia, Egypt;

2Department of

Pathology, Faculty of Veterinary Medicine, Suez Canal University, Ismailia, Egypt

Address correspondence to Mohamed Tawfic Ahmed, Plant Protection Department, Suez Canal

University, Ismailia, 41522 Egypt; E-mail: motawfic@tedata.net.eg

Running Head: Dietary Intake of Pesticides on Vegetables from Ismailia, Egypt

Received 2 January 2012; revised manuscript accepted 6 February 2013

ABSTRACT

The objective of this study was to assess pesticide residues in tomatoes, cucumbers,

peppers, strawberries, and potatoes collected from local markets in Ismailia, Egypt, and to assess

dietary intake and health risk implications of pesticide residues through food consumption.

Vegetable selection was based on their popularity and consumption. Selection of pesticides was

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based on their impact on humans, and on their heavy use. The majority of the analyzed samples

contained detectable levels of pesticides. Residues of some organophosphorus pesticides,

including malathion, ethion, and profenofos and some pyrethroid pesticides such as

fenpropathrin and cypermethrin were found in some samples at concentration equal to or

exceeding their European Union’s maximum residue limits (EU-MRLs). The fungicide

bupirimate detected in potato samples exceeded the EU-MRL by 1500%. Phentohate and

profenofos were the most frequently detected pesticides in 30 and 27% of analyzed samples,

respectively. Data were used to estimate the potential health risks associated with exposure to

these pesticides by ingestion of food. Estimated daily intakes (EDIs) of pesticides ranged from

0.03% to 40% of the acceptable daily intakes (ADIs), depending on pesticide concentration and

vegetable consumption. Overall, the EDIs of the different pesticides from vegetable consumption

are not considered a public health problem.

Key Words: pesticide residues, vegetables, estimated daily intake (EDI), acceptable daily intake

(ADI), Egypt.

INTRODUCTION

Egypt presently has a population of about 85 million. With the current annual rate of

2.5% population increase, its population is expected to reach 100 million by 2018, and the

balance between population growth and food production is becoming a daunting challenge

(Mansour 2004). Reliance on pest control chemicals in agriculture is likely to remain an

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essential component for increased food production. Even so, pesticide residues in foods might

have long-term health implications for humans’ health.

In Egypt, monitoring programs for pesticide residues in foodstuffs have been carried out,

mostly by the Central Laboratory of Residue Analysis of Pesticides and Heavy Metals in Food,

Ministry of Agriculture, Egypt (Dogheim et al. 1996a,b, 1999, 2001, 2002, 2004). Such

programs do not reflect the situation in the whole of Egypt, and they are not followed up by

evaluation of exposure levels and risks to humans (Anwar 2003).

The objectives of the current study were (a) to assess the residues of selected pesticides in

tomatoes, cucumbers, peppers, strawberries, and potatoes collected from local markets in

Ismailia, Egypt, and (b) to determine the current levels of exposure of the local population

associated with the consumption of these vegetables and any health implications. The region of

Ismailia was selected as it is one of the largest producers of fruits and vegetable crops in Egypt,

with much of its production exported to other governorates and countries.

The pesticides included in this study were profenofos, chloropyriphos, chloropyriphos

methyl, malathion, ethion, phentoate, fenpropathrin, lambda cyhalothrin, cypermethrin,

chlorfenapyr, metalaxyl, bupirimate, fenarimol, methomyl, and oxamyl. Selection was based on

the list of registered pesticides used in Egypt on fruits and vegetables and through interviews

with vegetable growers. Residues of pesticides pose a potential risks to humans’ health. Many

organophosphates (OPs) exert their toxic effects via oxidative stress mechanisms. This in turn

would lead to the generation of reactive oxygen species (ROS) and significant alterations in

antioxidants or ROS/RNS scavenging enzyme system (Sharma et al. 2005; Beuret et al. 2005).

OPs are also known to induce toxicity in mammals by inhibiting acetylcholinesterase (AChE),

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and the accumulation of acetylcholine and the subsequent activation of cholinergic muscarinic

and nicotinic receptors (Buyukokuroğlu et al. 2008).

The mode of exposure to OP insecticides includes the gastrointestinal, respiratory, and

dermal systems; the main targets of OP action are the central and peripheral nervous systems,

although many authors postulate that these compounds in both acute and chronic intoxication

disturb the redox processes, changing the activities of antioxidative enzymes and causing

enhancement of lipid peroxidation in many organs (Zhang and Lan 2004; Sharma et al. 2005;

Fortunato et al. 2006). There is some evidence that OPs may cause a lot of human body disorders.

Organs and systems that can be affected by these compounds are liver, kidney, muscles, immune

system, hematological system, and others (Teimouri et al. 2006). Similarly, synthetic pyrethroid

pesticides are potent nerve poisons with their toxicity impacting the axonic transmission of nerve

impulses. Pyrethroid insecticides are ion channel toxins that prolong neuronal excitation, but are

not directly cytotoxic. Pyrethroids show two basic poisoning syndromes. Type I pyrethroids

produce reflex hyperexcitability and fine tremor. Type II pyrethroids produce salivation,

hyperexcitability, choreoathetosis, and seizures. Both types produce potent sympathetic

activation (Ray and Forshaw 2000).

Residues of all targeted pesticides were detected in our study, with the exception of methomyl

and oxamyl.

METHODS AND MATERIALS

Sampling

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Vegetable samples were collected between March and May 2010. Fresh samples of

cucumbers, sweet peppers, potatoes, tomatoes, and strawberries were collected from six

locations: three major markets (Market-Elgomaa, Market-Elgomla, and Market-Elkhamies) and

three farms (Einghosein farm, Elmahsma farm 1, Elmahsma farm 2). Markets and farms were

selected to represent different parts of Ismailia city, with different supply lines, and also to

represent different societal and consumer classes. The selection of crops was based on their

popularity and high consumption rates at all community levels. Samples consisting of 2 kg of

each vegetable were transferred to the laboratory, thoroughly mixed, chopped into small pieces

then 100 g were picked at random and used for extraction, clean-up, and residue analysis.

Extraction

Pesticide residues were extracted using the method of Kadenezki et al. (1992). One

hundred g of chopped fruits were put into a 2-liter metal blender (model HGBSS, Waring,

Shelton, CT, USA), then 200 mL of acetone (for residue analysis, 99.99, Merck, Darmstadt,

Germany) was added, and the mixture was blended at high speed for 2 min. A 100-mL sample

of the mixture was collected and placed into a 500-mL separatory funnel, and 100-mL of

petroleum ether (99.9, bp 60-80, GC, Sigma–Aldrich, St. Louis, MO, USA) and 100-mL of

methylene chloride (98.0 % GC, Sigma–Aldrich) were added. The sample was shaken for 1 min

and the aqueous layer was transferred into a second 500-mL separatory funnel. The organic

layer of the first separatory funnel was dried by passing through 5 g of anhydrous sodium

sulphate (ACS reagent, 99% granular, Sigma–Aldrich). The aqueous phase was further extracted

with another 100 mL of methylene chloride and dried by passage through anhydrous sodium

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sulphate. The combined extracts were brought to near dryness using a rotary evaporator; the

residue re-dissolved in 0.5 mL of acetone, and kept in a deep freeze for further clean-up.

Clean-up

The extract was diluted with 10 mL of acetone and transferred to a 100-mL glass–

stoppered graduated cylinder using petroleum ether. The extract was then diluted to 100 mL

with petroleum ether, the flask was stoppered, and the solution was mixed thoroughly. The

solution was evaporated to near dryness using a rotary evaporator, then quantitatively transferred

on top of a Florisil column (PR grade, Fluka, Sigma–Aldrich 60 100 mesh). The column (20 x

1.2 cm) was prewashed with 25 mL of petroleum ether. Elution of the analytes from the column

was effected with three 200-mL portions each of mixtures of 6, 15, and 50% ethyl ether

(≥98.0%,, Sigma–Aldrich) in petroleum ether. Each fraction was collected separately in a 500-

mL flask, concentrated, and reduced to dryness, and diluted with 4 mL of hexane (≥99.0% GC,

Sigma–Aldrich) prior to gas chromatography determination.

Gas Chromatography Determination

Detection and quantification of pesticide residues were performed using a gas

chromatograph (GC) (model 5890A, Hewlett-Packard, Texas City, USA), equipped with an

electron capture detector (ECD) and nitrogen phosphorous detector (NPD). The ECD GC’s

temperature conditions were: detector temperature 300oC, injector temperature 225

oC. Two

different wide-bore capillary columns were used for analysis; the first column was coated with

ECD-tested Ultra 2 silicone (25 m x 0.32 mm i.d.,.,, film thickness 0.52 µm) (Agilent HP PAS-

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5); the second with ECD-tested 1701 silicone (25 m x 0.32 mm i.d.,.,,, film thickness 0.25 µm)

(Agilent HP PAS-1701). The temperature program was as follows: initial temperature, 90°C,

hold for 2 min, increasing to 150°C at 20°C min-1

, hold for 2 min, increasing to 220°C at 6°C

min-1

, hold for 15 min. Carrier gas flow rate (nitrogen) was 2.5 mL min-1

, make-up gas flow

(nitrogen) was 75–90 mL min-1

. The NPD was adjusted as follows: detector temperature was

280oC, injector temperature was 225

oC. Two different capillary columns were used. The first one

being a PAS-5 (cross-linked 5% phenyl-methyl-silicone) 30 m x 0.32 mm, film thickness 0.25

µm. The second column was DB–1701, with film thickness 0.25 µm, length, 25 m, column

i.d.,.,., 0.32 mm. Hydrogen flow rate was 3.5 ± 0.1 mL min-1

, air flow rate was 100–120 mL min-

1. Carrier gas: nitrogen, column head pressure was 75 kPa. Carrier gas + detector auxiliary gas

was 25 mL/min, septum purge was 5 mL/min, split vent 70 mL min-1

, splitless time: 0.7 min.

Quantification

A standard solution containing the targeted pesticides dissolved in hexane was injected

three times to ascertain the average retention time of each. Vegetable sample extracts were

injected and the pesticides identified according to their retention times. Standard solutions of

each pesticide were prepared and injected to establish the relationship between peak areas and

concentrations. Technical standards were obtained from the Central Agriculture Pesticides

Laboratory, Cairo, Egypt. The concentrations of the calibration levels were selected for each

pesticide according to the maximum residue limits. Good linearity was obtained in the range of

0.05 µg kg-1

to 5 µg kg-1

for the ECD, and from 0.07 µg kg-1

to about 5 µg kg-1

for the NPD.

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Quality Assurance Procedure

The criteria of quality assurance of the Codex committee were followed for quality

assurance. Calibration curves for the two detectors were made at levels of 10, 20, 50, 100, 250,

and 400 µg kg-1

. Calibration curves were generated by plotting the relative responses of analytes

(peak area of analyte/peak area of internal standard (IS), aldrin) to the relative concentration of

analytes (concentration of analyte/concentration of IS).

A constant amount of internal standard, 5 µg kg-1

, was contained in the aliquot of the

samples. The regression fit used for the calibration was the average response factor. Recovery

and reproducibility were evaluated by spiking pesticide standards to vegetable samples at levels

of 10, 50, and 200 µg kg-1

. The analysis was performed in replicates of four at each level. The

average recovery varied between 81–97 and 88–91 % for the ECD and NPD, respectively.

Estimation of the Daily Intake of Pesticides

The dietary intake of any particular pesticide residue in a given food is obtained by

multiplying the residue level in the food by the amount of that food consumed. Total intake of

the pesticide residue is then obtained by summing the intakes from all commodities containing

the residue of concern (WHO 1997). In the current study the dietary intakes of pesticides were

assessed by combining data of concentrations of pesticides found in different vegetables and the

daily amount of consumption of these vegetables. Food consumption data were collected using a

quantitative food frequency questionnaire structured by the National Cancer Institute of the USA

(Subar 2004). The questionnaire was translated into Arabic and some items were modified to fit

Egyptian food habits. A total of 250 adults from the Ismailia governorate participated.

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Volunteers, selected from a number of small villages in the vicinity of Ismailia city, were

approached when visiting the agricultural cooperation complex where growers obtain pesticides,

seeds, and other agricultural supplies used for crop production, or when visiting one of the main

medical centers. Volunteers were asked about their consent to take part in the current study and

only those who agreed were chosen. Information about Egyptian bodyweight average is meager

and not reliable. Seventy kg was used as average bodyweight based on data from the U.S.

Environmental Protection Agency (USEPA 1989). Pesticides’ estimated dietary intake was

calculated as follows:

Pesticide intake (mg/kg bw/day) = {pesticide residue (mg kg-1

)×consumption (kg/day)} ÷

bodyweight (kg).

RESULTS AND DISCUSSION

Pesticide Residues

In the present study, pesticide residues were determined in five vegetable crops:

tomatoes, cucumbers, sweet peppers, strawberries, and potatoes. The results and their European

Union (EU) EU-MRLs are presented in Table 1. All vegetable samples had detectable residues

of four to six pesticides. The most frequently detected pesticide in all samples was phenthoate,

detected in 33% of the samples.

For tomatoes, residues of three OP insecticides (malathion, ethion, and profenofos) and

two pyrethroid pesticides (fenpropathrin and lambda-cyhalothrin) were detected. In addition, the

pyrrole group insecticide with acaricidal activity, chlorfenapyr, was detected in tomato samples.

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Fenpropathrin, ethion, and profenofos residues in tomatoes exceeded their EU-MRL by 790%,

2700%, and 362%, respectively. For cucumbers, chlorpyrifos was the most frequently detected

pesticide, with residue levels ranging between 0.02 and 0.05 mg kg-1

, followed by the fungicide

metalaxyl detected at levels ranging between 0.16 and 0.18 mg kg-1

. The synthetic pyrethroid

insecticides cypermethrin, fenpropathrin, and lambda-cyhalothrin were also detected in

cucumber samples at residue levels of 0.2, 0.03, and 0.04 mg kg-1

, respectively. Fenpropathrin

residues detected in cucumber samples were three times higher than the EU-MRL. For sweet

peppers and strawberries, all pesticide residues did not exceed the EU-MRLs. For potatoes,

malathion, profenofos, and bupirimate residues exceeded their EU-MRL by 105%, 2960%, and

1500%, respectively.

Dogheim et al. (2002) and Abou-Arab (1999) reported higher residue levels of malathion

and profenofos in tomato samples collected from different locations in Egypt. Similarly, higher

residue levels of profenofos were reported in strawberry samples collected from eight Egyptian

local markets in six governorates including Ismailia (Dogheim et al. 1999, 2001, 2002). Pesticide

residue levels detected in this study are in agreement with the low residue levels reported by

Loutfy et al. (2008) for vegetable samples collected from the Ismailia governorate. Dogheim et

al. (2002) suggested that this low contamination level might be attributed to the relatively small

extent of pesticides used in Ismailia and the wide awareness and application of integrated pest

management (IPM) programs. On the other hand, many pesticides, including those banned in

Egypt, are still detected in various environmental segments such as groundwater, surface water,

fish, mussels, medicinal plants, soils, and sediments in Egypt (Tchounwou et al. 2002; El Nemr

and Abd-Allah 2004; Dogheim et al. 2004; Abdel-Halim et al. 2006).

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Daily Intake of Pesticides Based on Consumption of Vegetables

The ‘‘estimated daily intake” (EDI) was calculated and compared to the ‘‘acceptable

daily intake” (ADI) for all the detected pesticides. Shown in Table 2 are the average daily intake

values of pesticide residues and their corresponding ADI. The EDIs ranged from 0.0024 to 1.2

µg kg-1

bw/day depending on the pesticide concentration and vegetable consumption. The

highest absolute intakes via consuming a single commodity corresponded to profenofos,

phenthoate, ethion, and fenpropathrin with values of 1.2, 1.2, 0.27, and 0.26 µg kg-1

bw/day,

respectively. The highest absolute intakes via consuming more than one commodity

corresponded to profenofos and L-cyhalothrin, with values of 1.3 and 0.106 µg kg-1

bw per day,

respectively. In this study, the pesticides with higher contribution to the ADI are phenthoate

(around 40% of ADI), followed by ethion (13.5%), profenofos (4.6%), bupirimate (1.3%), and

fenpropathrin (1.1%), while the remaining pesticides provided less than 1% of the ADI.

The contribution to the ADI shows that all the intakes of pesticide residues are still within

acceptable limits. However, it should be emphasized that pesticide dietary intakes estimated in

this study have only considered exposures from selected vegetables and did not include other

food products or the rest of the vegetables consumed by the study’s participants. The present

study did not include drinking water or residential or occupational exposure. Information about

residential or occupational exposure to pesticides are not available but could be looked at in

future studies. Hence, the current estimates are not considered as total dietary exposure to

pesticides. It should also be borne in mind that the present study was conducted on vegetables

before they were washed, as washing is very likely to remove a considerable amount of pesticide

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residues. But in Egypt, especially at country side, fresh vegetables may be consumed without

washing or with minimal washing.

CONCLUSION

Results of the present study highlighted the presence of pesticide residues in vegetables

collected from local markets in Ismailia, Egypt. Results indicated that the concentration levels of

many of the detected pesticides equaled or exceeded their EU-MRLs, hence posing some

potential risks to consumers, especially to vulnerable groups such as children and elderly

consumers. These results also indicate that pesticide-use practices in the study area are far from

being sound practices and would need substantial effort to improve awareness, integrated pest

management, and good agriculture practices. On the other hand, EDIs recorded in the present

study showed a range of levels that posed no serious toxicity to vegetable consumers, although

the present study did not account for residues reaching consumers through water, either through

consumption or washing of consumed vegetables. In Egypt, regulations such as the safety period

that should follow pesticides’ application are not observed because of lack of awareness, and

weak follow-up. The present work highlights the importance of regular monitoring of pesticides

programs and the need to find a viable mechanism to enforce pesticides regulation, with special

reference to observing safety period in order to reduce pollution and to minimize health risks.

ACKNOWLEDGEMENT

The authors express their gratitude to two anonymous reviewers and HERA’s editor for

their contributions to this manuscript.

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WHO (World Health Organization). 1997. Guidelines for Predicting Dietary Intake of Pesticide

Residues (Revised) Global Environment Monitoring System – Food Contamination

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Monitoring and Assessment Programme (GEMS/Food) in collaboration with Codex

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Geneva, Switzerland

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Table 1. Average concentrations of pesticide residues in selected vegetables.

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Commodity Pesticide

contaminated

samples

No. %

Mean Residue

level mg kg-1

EU–MRL

mg kg-1

% Mean

Residue

Compared

with EU-

MRL

Fenpropathrin

3 25 0.08 ±0.01 0.01

790

L- Cyhalothrin

3 25 0.07 ±0.01 0.1

72

Ethion 3 25

0.27 ± 0.005 0.01 2700

Malathion

1 8.3 0.025 ± 0.005 0.5

5

Chlorfenapyr

2 16.6 0.03±0.01 0.05

60

Tomato

Profenofos

1 8.3 0.181±0.001 0.05

362

L- Cyhalothrin

1 8.3 0.04(± 0.001) 0.1

40

Cypermethrin

1 8.3 0.20(± 0.02) 0.2

100

Metalaxyl 2 16.6 0.17(± 0.01) 0.5 34

Chloropyrifos

3 25 0.03 (± 0.002) 0.05

60

Cucumber

Fenpropathrin

1 8.3 0.03(± 0.002) 0.01

300

Fenarimol 4 33

0.043(± 0.01) 0.5 8.5

Profenofos

2 16.6

0.047(± 0.003) 0.05

94

Chloropyrifos

1 8.3 0.02 (± 0.004) 0.5

4

Sweet

pepper

Chlorfenapyr

1 8.3 0.02(± 0.002) 0.05

40

Profenofos

3 25 0.035(± 0.003) 0.05

70

Chloropyrifos

2 16.6 0.022 (± 0.003) 0.2

10.75

L- Cyhalothrin

1 8.3 0.05(± 0.02) 0.5

10 Strawberry

Chloropyrifos –M

1 8.3 0.03 (± 0.01) 0.05

60

Malathion 1 8.3 0.021(±0.01) 0.02 105

Profenofos 2 16.6 1.48 (±0.05) 0.05 2960

Bupirimate

1 8.3

0.75(±0.02) 0.05

1500

Potato

Phenthoate 4 33 1.43 (±0.04) NA NA

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Table 2. Acceptable daily intake (ADI in µg /kg body weight/day), percentage of ADI and,

pesticide estimated daily intake based on vegetable consumption data in Ismailia, Egypt.*

Dietary intake (µg kg-1

b.w day-1

)

Pesticide

Tomat

o

Cucumb

er

Pepper

Strawberr

y

Potat

o

Total

ADI(µg /kg

bw/day) (source;

year)

%ADI

Bupirimate 0 0 0 0 0.64 0.64 30 (JECFA;

2006)

1.28

Chlorfenapyr

0.03 0 0.005 0 0 0.035 15 (ECCO 99) 0.23

Chloropyrifos

0 0.0257 0.005 0.0024 0 0.033 10 (JMPR; 2004) 0.33

Chloropyrifos

–M

0 0 0 0.0034 0 0.0034 10 (JMPR; 2004) 0.034

Cypermethrin

0 0.17 0 0 0 0.17

20 (JMPR; 2009) 0.85

Ethion 0.27 0 0 0 0 0.27 2 (JMPR; 1990) 13.5

Fenarimol 0 0 0.0106 0 0 0.0106 10 (JMPR; 1995) 0.106

Fenpropathrin 0.079 0.257 0 0 0 0.33 30 (JMPR; 2006) 1.12

L-

Cyhalothrin

0.072 0.0342 0 0 0 0.106 20 (JECFA;

2000)

0.5

Malathion 0 0 0 0 0 0.043 30 (JECFA;

2006)

0.14

Metalaxyl 0 0.145 0 0 0

0.145 80 (JMPR; 2004) 0.181

Phenthoate 0 0 0 0 1.2 1.2 3 (JMPR; 1984) 40

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Profenofos 0.181 0 0.0117 0.004 1.2 1.39 30 (JMPR; 2007) 4.6

*JMPR is the Joint FAO/WHO Meetings on Pesticide Residues; JECFA is the Joint FAO/WHO

Committee on Food Additives

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