Ethylene Oxide Keeps Raising It’s Head

White sesame frame isolated on black background. Top view, close-up. Often treated with ethylene oxide.
Copyright: photopaper

Ethylene oxide (EtO) is one of the most potent pesticides and antibacterial agents available for treating food and textile produce. There are however serious health and safety concerns over its use particularly as it can potentially cause cancer when ingested over long periods of time.

To be clear it does have other names such as its IUPAC names of oxirane, epoxyethane and oxacyclopropane. The CAS number is 75-21-8, its molecule formula is C2H4O and it has a molar mass of 44.052 g/mol.

The European Commission (including Switzerland and the UK) banned its use a number of decades ago over this issue, 1991 to be precise. It keeps regularly tuning up though as a presence in many different types of products, even fruit and vegetables, and other ingredients which have been disinfected with this gas. Ingredients used in the EU are not treated using EtO.  This pesticide is mainly found in products treated outside the EU.

Other countries do not have such qualms in its use and find it particularly effective as a treatment especially against insects and even Salmonella. Outside the EU, countries such as India regularly use ethylene oxide to fumigate raw ingredients like rice and sesame seeds. It is regularly used in Canada and the USA for a variety of purposes especially for the sterilizing of equipment.

Detecting its presence in foods is now so frequent that it is responsible for most of the recalls associated with a single substance throughout the EU and the United Kingdom. 

The Potency of Ethylene Oxide

Ethylene oxide is very effective at reducing if not eliminating microbial contamination of foods especially Clostridium botulinum, Salmonella and Escherichia coli. It severely reduces bacterial loads, destroys yeast and molds, viruses and spores, coliforms like E. coli and many other pathogens. It is also extremely effective against all types of insects. It has been a common practice of treatment in many countries for years. However, the gas is a carcinogen and mutagen. It causes irritation of the membranes and is an anaesthetic too. If it is used at too high a temperature it can damage sensitive plant materials such as herbs and spices.

Industrially, the gas is produced by oxidation of ethylene (ethene) over a silver catalyst. It is often abbreviated to EtO. It is a low molecular weight compound and has been a common intermediate in organic synthesis where it is valued for being able to add 2 carbon atoms and so extend an organic molecule.

The main inactivation mechanism of EtO is the alkylation reaction which adds alkyl groups to sulfhydryl, hydroxyl, amino, and carboxyl groups. This destroys the bacteria by denaturing functional proteins, DNA, and RNA structures. The disruption is so great that cell metabolism is completely destroyed.

EtO does not hang around very long. It dissipates readily from any food that is treated as much through reaction as through volatilization. It is often detected through the compounds it forms. These include reactions with chlorides and bromides to produce 2-chloroethanol (2-CE), 2-bromotheanol, 1,2-ethanediol and 2,2′-oxybis(ethanol). These compounds too have safety issues if not as tainting compounds.

Two EtO molecules can be converted to 1,4-dioxane which has potential carcinogenic behaviour. Acetaldehyde is formed when the EtO ring is broken. Inhalation of acetaldehyde produced long-term tissue injury with tumour development in the nasal region when the exposure level is above 750 ppm. The molecule, 2-chloroethanol (2-CE), has high toxicity, and it has been reported that 2-CE (92 mg kg−1, i.p.) can cause a 50% reduction in cerebral glutathione 6 hours after administration to mice.

As well as being colourless and flammable, it is highly reactive and can also cause explosions!

Applications

EtO is used as a raw material in large-scale chemical production. It is especially useful in the synthesis of ethylene glycol, polyethylene glycol, ethylene glycol ethers, ethanolamines and ethoxylates. 

EtO is used directly as a healthcare sterilant, especially for medical devices with plastics that cannot tolerate moisture or heat. This is its principal use.  It also has the role of a food fumigant because it successfully destroys so many microorganisms even spores and viruses. About 0.05% of the global production of EtO is used in these applications. The gas has a very high diffusivity with strong penetrating properties which makes it very effective with dry food commodities.

As a fumigant it is ideal for treating nuts and spices, oilseeds, dried fruits and vegetables, dried herbs and botanicals. In most cases, the products to be treated are contained in sacks, bags and boxes. They are placed in a chamber where the food is infused with EtO for up to 10 hours in some cases.

When it is used, the main dissipation pathway is through evaporation because of its high volatility and through reactions. Usually, excess EtO is removed from a treated food product by blowing air through the unit which helps in the removal of free ethylene oxide. There is a slower rate of loss if the foods are not aerated or are sealed in packaging soon after. The presence of 2-chloroethanol (ethylene chlorohydrin) is due to its formation in foods when chloride ions are present as in salted foods. This compound is less volatile and there is limited removal by aeration. It is the marker residue for EtO use. 

The Furore

The use of ethylene oxide has been banned in Europe since 1991. Although it has been found in thousands of foods and in some cases at levels a thousand times higher than the maximum residue limit allowed in the EU, it is still classified as only a potential ‘chronic risk’. The limits set by the EU are extremely stringent.

It was in September 2020 at the height of the COVID pandemic that Belgium first notified us of ethylene oxide’s unauthorised presence in batches of sesame seeds from India. Belgium reported this via the Rapid Alert System for Food and Feed (RASFF). The levels were between 0.1 and 10 mg/kg in some samples, the average value was 30 ppm but levels as high as 186 mg/kg were reported.

In October 2020, the EU Commission, and European Food Safety Authority (EFSA) held a food and feed crisis coordinators meeting. These countries called for extra vigilance on species and pepper.  An assessment by the National Institute for Public Health and the Environment (RIVM) and Wageningen Food Safety Research found it was “hardly possible” to eat safe quantities of bread, crackers, or cookies with sesame seeds containing ethylene oxide at a level of 10 mg/kg.

Since that time there have been thousands of items of foods with long shelf-lives that have had to be recalled. They include nearly everything from bagels and bread, biscuits, cereals, chocolate, crackers, ready made meals, food supplements and spices. There were 129 ethylene oxide incidents in the UK from April 2021 until March 2022 covering dietetic foods and food supplements. It is also commonly identified in food additives such as guar gum, locust bean gum, and xanthan gum. The xanthan gum came from Turkey.

In 2023, Madsen et al., (2023) reported on EtO and 2-CE in low-viscosity hydroxypropyl methylcellulose. This material is used in hard capsules.

The use in spices is important because many of these ingredients are processed, treated and then will be added to foods which do not undergo further processing.

Safety Issues

Most food authorities in the EU such as the Food Safety Authority of Ireland consider consumption of foods that are ‘contaminated’ with ethylene oxide does not pose an acute risk to health. If there is continued exposure over a significant period of time then it becomes a serious health issue.

In the EU, when it comes to foods, more recalls are possible because more and more pesticide treatments are being banned in the EU market.

Links to Cancer

The research into ethylene oxide and cancer has been established for some years. It was the Environmental Protection Agency in the USA that raised the possibility of prolonged contamination from foods. The EPA claimed that inhalation and ingestion of ethylene oxide was the biggest issue as a carcinogen. It is often present in smog and has been detected in many cities with severe pollution problems. It is also a contaminant in cigarette smoke.

The toxicity of the chemical is many fold but is defined by the IARC (International Agency for Research on Cancer) as a Group 1 carcinogen especially to humans. The USA’s EPA states it is carcinogenic to humans by the inhalation route of exposure and there is evidence supporting its mutagenicity. The European Union defines it as a category 1B mutagen, a 1B carcinogen and a 1B toxic compound for reproduction.

The compound is not all bad! It is still the most effective and safest sterilization method when handled properly. It is commonly used in the USA for the treatment of medical devices. At least 50% of all medical devices are sterilised this way which amounts to 20 billion medical devices annually. 

EU Regulations

The regulations in the EU are highly restrictive compared to the USA. Regulation (EC) No. 396/2005 defines the Maximum Residue Limit (MRL) for ethylene oxide as the sum of ethylene oxide and its metabolite 2- chloroethanol, in or on foods. This sum is expressed as ethylene oxide. The lowest *-MRL for “ethylene oxide” is 0.02 mg/kg (i.e. 0.01 mg/kg for ETO and 0.01 mg/kg for 2-chloroethanol). The legislation sets an MRL at the limit of quantification (LOQ) which is achievable in different commodities, so effectively meaning that it must not be detected in food.

Subsequently, the EU has also proposed separate maximum residual limits (MRLs) for ethylene oxide and its primary metabolite 2-chloroethanol in different food and agriculture commodity ranging from 0.02 to 0.1 mg/kg (Commission Regulation (EU) 2015/868).

The three MRLs (ppm or mg/kg) are set for three commodity groups:-

(1) MRL of 0.02 (mg/kg)  is set for fruits (fresh and frozen), vegetables (fresh and frozen) except herbs and edible flowers, for pulses, cereals, sugar plants and products of animal origin except for honey and other apiculture products.

(2) MRL of 0.05 (mg/kg) for tree nuts, oilseeds and oil fruits, herbs and edible flowers, honey and other apiculture products.

(3) MRL of 0.1 (mg/kg) for teas, coffees, herbal infusions, cocoa and carob, and for spices.  

Regulation (EU) 231/2012, lays down the specifications for food additives.  Ethylene oxide is not allowed to be used for sterilising purposes of food additives and sets limits for some additives involving it in the production process.  It specified an EtO limit of 0.2 mg/kg for additives that involved EtO in their prodiction, such as polyethylene glycol or polyoxyethylene sorbitans (polysorbate 20, 65 and 80). The figure is for free EtO only and does not involve the addition of 2-CE as a sum.

Issues however relating to food additives often arise. It was not clear how to handle food additives like gums which come from treated sources. An EU Commission communication arose on Locust bean gum (E410), guar gum (E412) and E415 (xanthan gum).

Any products on the EU market which incorporate Locust bean gum (E410) contaminated with ethylene residues above 0.1 mg/kg must be withdrawn from the market and recalled too.

EU Regulations on Food and Feed Additives 

Also, there must now be no residue above 0.1 mg/kg, irrespective of its origin, of ethylene oxide in all feed and food additives. The value of 0.1 mg/kg is the sum of EtO and 2-CE expressed as EtO and is the analytical LOQ which is applicable as the maximum limit for EtO.  This maximum limit was published in the Official Journal of the European Union on 11 August 2022. This regulation came into force on the 1st September 2022. It covers the food additives that are listed in Annexes II and III to the Regulation (EC) No. 1333/2008, including any mixtures of food additives. The change was devised for the purpose of managing this contamination incident. The ruling applies to all additives except those with an EtO specification defined in EU Regulation No. 231/2012 and includes calcium carbonate  used either as additive, as nutrient or as feed material.

Compound Foods

When it comes to compound foods and feeds (animal feeds) for which there is evidence that it was produced with a contaminated additive or feed material, has to be withdrawn from the market if EtO residues (EtO + 2-CE)are found above 0.02 mg/kg. This level was chosen because the recipe and processing factors might be unknown. If it is unknown whether a non-compliant raw material or ingredient has been used, so the MRL of 0.02 mg/kg is applied. If it is known that a non-compliant raw material or ingredient is used, then the end product is still regarded as not marketable and unsafe. The application is also stated for pet foods taking into account that pets too are affected by cancer due to longer lifetimes.

When it came to composite foods and food supplements, the EU Commission set stringent limits. Take instant noodles, without having any information on the use of a non-compliant ingredient, the MRL at the LOQ was set at 0.02* mg/kg. If there was evidence on the use of a non-compliant ingredient, it was to be withdrawn with recalls of the product from the marketplace and in the case of imports, rejection at the border.

Food Supplements

For food supplements, the EU required harmonization and consistency in the law, so the applicable MRL of 0.1* mg/kg was set for capsules using HPMC for example  in the production of food supplements.

Baby Foods

For foods for infants and toddlers, the EU states that where an additive is used for the production of a food for IYC and is contaminated with EtO at a level above 0.1* mg/kg, the final product must be withdrawn from the market and recalled from consumers, regardless of the EtO level in the final product. If EtO was used as an additive in compliance with the limit (<0.1* mg/kg) but leaves measurable residues in the final product (>0.01 mg/kg), then it should be withdrawn from the market or recalled from consumers. 

Commission Implementing Regulation (EU) 2020/1540, was the response to the September 9th alert from Belgium. Since 22 October 2020, sesame seeds originating from India must be tested for the presence of ethylene oxide prior to export to the EU. An official certificate must accompany all consignments of sesame seeds to show their compliance with pesticide EU MRLs. The additional restriction is 50% (i.e. half) of all batches of sesame seeds from India must be tested for pesticide residues. In formal terms, these are 50% EU entry official controls for pesticide residues including EtO on sesame seeds from India.

It was claimed by the Soil Association that Defra would not require importers to obtain ethylene oxide testing on product imported from India as of the 1st July 2022. Up to that time there was a mandatory requirement for testing imports of Indian organic products but now it may be viewed that the Indian organic certification process is now adequate.

The European Union Reference Laboratory for Single Residue Methods (EURL-SRM) published a comprehensive analytical observations report in December 2020 concerning EO and 2-CE .

USA and Canada Regulations

In the USA it is an approved fumigant according to the Code of Federal Regulations. Its use is covered under CFR 180.151 Ethylene oxide; Tolerances for residues. There are specific levels of presence for herbs and spices (group 19) which are all dried excluding basil, for liquorice and its roots, peppermint and spearmint tops, sesame seeds, vegetables and walnuts. 

In late 2019, Health Canada’s Pest Management Regulatory Agency proposed to establish maximum residue limits (MRLs) for ethylene oxide on dried vegetables and sesame seeds to permit the sale of foods containing such residues. It is an insecticide registered in Canada for use on whole or ground spices and processed natural seasonings.

In the USA and Canada, the two substances are now assessed as follows: the admissible maximum residue level for ethylene oxide allowed in the USA and in Canada for food is 7 mg/kg or ppm each (Fed. Reg., USA; Canada). For walnut, the maximum residue limit is 50 ppm.

For 2-chloroethanol, the MRL is 940 ppm irrespective of the food analysed. A conversion of 2-CE back to EtO is 514 mg/kg which is under 100-fold the MRL of 7 ppm set for EtO in its own right. That MRL for 2-CE is 10,000 times higher in the equivalent terms for EtO (as 514 ppm) than that set by the EU.

There are no Codex MRLs listed for ethylene oxide in or on any commodity.

The use of EtO is under review by the USA’s EPA. They have conducted a draft risk assessment of EtO for pesticide registration. 

Asian Regulations

The Taiwanese Food and Drug Administration (TFDA) recently suspended the distribution of Nongshim’s (South Korea) product Shin Ramyun Black Tofu Kimchi instant noodles in these countries on around the 31st January 2023 as reported on Yahoo (Yahoo! News 07/02/2023).  The TFDA found 0.075 mg/kg of ethylene oxide although the South Korean business stated this was actually 2-CE. However, 2-CE is still a proscribed chemical in Thailand. The limit in Taiwan is 0.02 ppm. 

The Filipino noodle brand Lucky Me! produced by Monde Nissin also suffered a similar fate being cited for unacceptable EtO levels by 10 countries in the European Union.

Testing Methods

Jensen (1988) reported a ‘simple’ and quick method of between 4 and 5 hours. In this analysis, ethylene oxide (EtO) and its reaction product ethylene chlorohydrin (ECH, 2-chloroethanol) are both measured by adding sodium hydroxide to the sample to convert ECH back to EtO. The EtO is distilled into dilute sulphuric acid containing sodium iodide which converts EtO to ethylene iodohydrin (2-IE). The iodohydrin is determined by gas chromatography with electron capture detection. The recovery of ECH was between 50 and 60%. It became the basis of the German official method § 64 LFGB, L53.00-1 (Gilsbach et al., 1999). The analysis of free EtO possible without the first conversion step.

A method of Aitkenhead and Vidnes (1988) used an extraction solvent for ECH based on an acetonitrile-methanol mixture. The ECH produced was detected suing capillary gas chromatography with an FID detector. The extraction recovery was 75%. 

Tateo and Bononi (2006) reported a method for detecting ethylene chlorohydrin which involved conversion of EtO to 2-CE and then analysis of the total 2-CE. This could then be converted to a measure of EtO. 

Nowadays, the routine methods involve direct analysis using headspace sampling i.e. headspace gas chromatography and gas chromatography coupled to mass spectroscopy (GC-MS). The headspace sampling can either be static or dynamic, or use SPME or a trap.

Any EO residues are measured by determining ethylene chlorohydrin (2-CE) (Bononi et al., 2014).

Most analytical systems have a detection limit of 0.05 mg/kg. The costs of analysis are around £200 (Sterling) per sample according to 2022 prices. 

The method using the analytical approach of QuEChERS and GC-MS/MS has been tried with ice cream to determine both EtO and 2-CE. It has a quantification limit (LoQ) of 0.01 mg/kg expressed as EtO. The recovery of the EtO in the ice cream matrix was over 85% (Bessaire et al., 2021). A similar approach has been used on oils and spices, noodles and food packaging (Nu et al., 2022).

The QuEChERS approach can rely on ready-to-use  extraction salts available from businesses such as Agilent Technologies. This mixture contains 4 g of magnesium sulphate, 1 g of sodium chloride, 1 g of sodium citrate, and 0.5 g of disodium citrate sesquihydrate, and dispersive Solid Phase Extraction salts  of d-SPE, containing 150 mg PSA, 150 mg C18EC, and 900 mg MgSO

Analysis is conducted at low temperatures because of the volatility of EO so ice baths are needed. Any diluting solutions are kept as cold as feasibly possible as are standard solutions.

Extraction of 2-CE is best performed using the European Norm EN 15662:2018 (QuEChERS-based procedure).  The method is the official version for general determination of pesticide residues using GC- and LC-based analysis. It relies on an initial acetonitrile extraction of the sample with partitioning. Any dry samples where the water content is below 80% will need the addition of water (10g) before the acetonitrile extraction. The QuEChERS approach is then used first with addition of magnesium sulfate, sodium chloride and buffering citrate salts. Its shaken intensively and centrifuged to cause a phase separation. Next, a portion or aliquot of the organic phase is cleaned-up using dispersive solid phase extraction cartidges (D-SPE; Phenomenex). This uses bulk absorbents and magnesium sulphate to remove residual water. The cleaning-up can use amino-sorbents such as PSA (primary secondary amine sorbent) and where needed graphitized carbon black (GCB) or octadecylsilane (ODS). The extracts are acidified by adding a small amount of formic acid to improve the storage stability of any base-sensitive pesticides. This final extract is suited to any GC- and LC- analysis. Typical columns include the C18 HPLC column (100 mm x 3 mm, 2.7μm) (Ascentis Express). An LC system such as the Shimadzu Nexera LC-30AD coupled to an IonDrive Turbo V Source (Sciex; Warrington, Cheshire, UK) is feasible.  A variety of detectors are mass selective, flame photometric detectors (FPD) and electron capture detector (ECD). Quantification is based on internal standards.

Toth et al., (2022) reported the generation of false positives using the European Standard Method.

A recent method (Madsen et al., 2023) proposes using solid phase microextraction (SPM) with GC/MS. This is an alternative to the European Council’s proposed generalised method for spices, seeds and capsules that uses QuEChERS, solid phase extraction (SPE) and GC-MS/MS. This article involved development of two methods specific for EtO and 2-CE. Both methods were highly specific and the limits of detection were  EtO 6.7 µg/kg and 2-CE 12 µg/kg.

Eurofins have developed their method which converts EtO to 2-IE and they analyse 2-IE and 2-CE. They claim it is very robust. They use gas chromatography-tandem mass spectrometry (GC-MS/MS) and there is separate reporting of both EtO and 2-CE residues as well as a sum. The LOQ/RL in mg/kg is 0.01 mg/kg.

The Current Requirements For Testing

In the United Kingdom, we may start to be seeing the divergence in regulations from the EU. From the 1st January 2022, DEFRA had asked that produces imported from India were to be tested for ethylene oxide because of the ongoing contamination issue. That expired on the 30th June 2002 and now products arriving in Great Britain do not need testing for this contaminant by the importer (Soil Association, 2022).

Maximum Limits (TBC)

Region Analyte Food Matrix MRL (mg/kg)
European Union ETO (sum of ETO and 2-CE expressed as ETO)
United States

In China, EtO is routinely used in the treatment of packaging. Gelatin capsule shells used in pharmaceutical applications are routinely treated in this manner. According to the ChP2020 (Chinese Pharmacopeia), the EtO residue should not exceed 0.0001% (1 ppm), and 2-CE residue should not exceed 0.002% (20 ppm) in gelatin capsule shells (Wang et al., 2022).

Ethylene Oxide In Feeds and Pet Foods

Feed is the generic term for foods used to feed animals such as poultry and livestock. In a recent EU memo (EU, Oct. 2021), it was stated there was no transfer of EO from feed to food of animal origin meaning that the presence of EO and any metabolites was not then being transferred via the meat into the food chain and posing a risk to consumers. Likewise there was no evidence of any serious animal health risk due to the presence of low levels of ethylene oxide and metabolites to the animals themselves.

When pets are considered, they are potentially exposed to EO for longer periods when food is contaminated with this pesticide. It appears that the carcinogenic properties of EO are a higher animal health risk for the longer lived pets than for food producing animals because of the former’s longevity.

When it comes to feed additives, the use of locust bean gum (E410) or other additive which is contaminated with EO above the LOQ of 0.1 mg/kg for feed is prohibited.

One additive that could fall foul of the ban is choline chloride because the presence of 2-CE is not through illegal use of EO. The production of choline chloride relies on using EO with hydrochloric acid. Choline chloride (75% purity) should be EO free and 2-CE can be present in levels from 10 to 55 mg/kg. A maximum level of ETO (sum of EO plus 2-CE) in choline chloride is 40 mg/kg relative to choline levels of 99% purity.

Alternatives

Alternative treatments include irradiation, cold plasma technology. One study showed that an ethylene oxide treatment compared favourably with irradiation of 4 or 8 kGy gamma (Farkas & Andrassy, 1988). The gas treatment was 800 g T gas per m3 at 22 ºC for 6 h. The species treated were  ground black pepper, ground paprika, onion powder and garlic powder and the water uptake of the latter two seasonings. A better gas may be chlorine dioxide which is now available for treating spices. It is also possible to use chlorine dioxide treatment.

Biomarkers For Ethylene Oxide Exposure

Haemoglobin adducts are good biomarkers and the main measure is 2-hydroxyethylvaline (HEV). The exposure pathways include  exogenous ethylene oxide, exogenous ethylene as well as endogenous ethylene oxide (Bailey et al., 1987; Kirman and Hays, 2017).

References

Aitkenhead, P., Vidnes, A., 1988. Simple and accurate method for determination of ethylene chlorohydrin in dried spices and condiments. J. Assoc. Off. Anal. Chem. 71, pp. 729–731

Ayoub, K., Harris, L., Thompson, B., 2002. Determination of low-level residual ethylene oxide by using solid-phase micro-extraction and gas chromatography. J. AOAC Int. 85 (6), pp. 1205–1209

Bailey, E.P. B. Farmer, and D. E. Shuker. (1987)Estimation of exposure to alkylating carcinogens by the GC-MS determination of adducts to hemoglobin and nucleic acid bases in urineArch. Toxicol. 60: pp. 18791. PMID: 3619640.

Bessaire, T., Stroheker, T., Eriksen, B., Mujahid, C., Hammel, Y. A., Varela, J., … & Stadler, R. H. (2021). Analysis of ethylene oxide in ice creams manufactured with contaminated carob bean gum (E410). Food Additives & Contaminants: Part A38(12), pp. 2116-2127.

Bononi, M., Quaglia, G., & Tateo, F. (2014). Identification of ethylene oxide in herbs, spices and other dried vegetables imported into Italy. Food Additives & Contaminants: Part A31(2), pp. 271-275 (Article).

Canada: https://pr-rp.hc-sc.gc.ca/mrl-lrm/index-eng.php

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Gilsbach, W., Weeren, R.D. (1999). Ringuntersuchungen zur Validierung einer gaschromatographischen Methode zur Bestimmung von Rückständen an Ethylenoxid und 2-Chloroethanol in Gewürzen aus Paprika und Chili, Dtsch. Lebensm. Rundsch. 95, pp. 83–90

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Madsen, R.B., Termansen, M., Mintert, M., Huettermann, C., Serr, B. (2022) Trace-level quantification of ethylene oxide and 2-chloroethanol in low-viscosity hydroxypropyl methylcellulose with solid phase microextraction and GC-MS, Food Additives & Contaminants: Part A, 39:12, pp. 1893-1905. (Article) 

Nu, D. N. N., Van Nhan, T., Duy, N. T., Kiet, L. T., & Van Dong, N. (2022). Determination of ethylene oxide and 2-chloroethanol in food by triple quadrupole GCMS/MS, combined with QuEChERS extraction. Vietnam Journal of Food Control5(3), pp. 310-322. (Article).

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yahoo!news (2023) (Article)

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