Dioxins and Dioxin-like Compounds in Foods and Feeds

Dioxins and dioxin-like compounds (DLC) are members of a group of chemical compounds that are described as persistent organic pollutants (POP). Some POP are highly toxic and carcinogenic, although their toxicity varies greatly.

The POP addressed in this information statement are:

• Polychlorinated dibenzo-p-dioxins (PCDD)
• Polychlorinated dibenzofurans (PCDF)
• Dioxin-like polychlorinated biphenyls (DL-PCB)

PCDD, PCDF and DL-PCB are three of the so-called ‘dirty dozen’ compounds identified as candidates for control and elimination after the institution of the Stockholm Convention on POP in 2001. They are collectively referred to as ‘dioxins’ within this information statement.

PCDD and PCDF are unintentional by-products of human activity, especially the combustion of chlorine-containing compounds.

PCB (including DL-PCB) are non-flammable and chemically stable with a high boiling point and electrical insulating properties. Consequently, although their production was abandoned in most countries in the 1970s, PCB were widely used in electrical, heat transfer and hydraulic equipment, and a variety of other applications.

Dioxins occur in the environment throughout the world and accumulate in the food chain, mainly in the fatty tissue of animals. Animal feeds and feed additives are major sources of contamination for food of animal origin, including eggs, meat, fish and milk. They are highly toxic and can compromise the reproductive, developmental and endocrine systems. Given their toxicity, levels of dioxins in feed and food are regulated in Europe, the USA and other countries. Consequently, reliable methods are required for the sampling and analysis of dioxins.

DL-PCB are a sub-group of the wider class of PCB which demonstrate a similar toxicity to PCDD and PCDF.

PCB are a group of organochlorine compounds that are non-flammable and chemically stable with a high boiling point and good electrical insulating properties. They are synthesised by the catalysed chlorination of biphenyl. Depending on the number of chlorine atoms (1–10), and their position in the two rings, 209 different congeners are possible. Figure 2 shows the structure of PCB and the numbering of the carbon atoms in the two rings.

Figure 2. Structure of PCB: Cly + Clx = 1-10.

In contrast to PCDD and PCDF, PCB had widespread use in numerous industrial applications, generally in the form of complex technical mixtures. They were produced with an estimated total world production of 1.2–1.5 million tonnes between 1929 and the end of the 1970s, when their production was abandoned in most countries, due to concerns about their toxicity and persistence in the environment and biota. Because of their physicochemical properties, PCB were widely used in a number of industrial and commercial applications. Technical PCB mixtures were mobile oils, viscous liquids or sticky resins, depending on the degree of chlorination (21–68% chlorine). Various commercial mixtures were produced with different trade names, such as Aroclor, Kanechlor, Declor and Clophen. PCB were used as insulating fluid in electrical transformers, and as heat exchange fluids. As a result of their widespread use, leakages, improper disposal practices and persistence, PCB also have a global distribution in the environment. Depending on the number and position of the chlorine atoms in the molecule, some of them are poorly degraded and, due to their lipophilic properties, are bioaccumulated in the food chain.

The PCB Elimination Network (PEN) develops and implements an awareness raising strategy, including videos, website, webinars and fact sheets, to ensure that PCB remain on the international agenda. It also supports PCB activities within the Basel, Rotterdam and Stockholm Conventions Conferences, and the United Nations Environment Assembly.

Dioxins in the food chain are of concern because of a number of adverse health effects that can occur at very low levels of exposure. Acute exposure at relatively high level can result in chloracne (a skin condition). Of perhaps greater concern are the chronic effects of low-level exposure, typically through the diet, which can cause reproductive, carcinogenic and other effects (Faqi et al, 1998; COC, 2001).

Toxic Equivalency Factors (TEF) and Toxic Equivalents (TEQ)

The most toxic dioxins are 2,3,7,8-TCDD and 1,2,3,7,8-PeCDD, which are given Toxic Equivalency Factors (TEF) of 1. All other dioxins are compared to these and given comparative TEF (see Table 1).

In order to compare the toxicity of a mixture of congeners, Toxic Equivalents (TEQ) based on the TEF of the individual congeners are calculated. This scheme assumes that the relevant PCDD, PCDF and DL-PCB bind to the intracellular aryl hydrocarbon receptor (AHR) and cause the same type of AHR-mediated biochemical and adverse effects. Another important requirement of the TEQ concept is the persistence and accumulation of the compounds in the body.  

To calculate the total TEQ value of a sample, the concentration of each congener is multiplied by its TEF and the products are then added together. The resulting TEQ value expresses the toxicity of PCDD, PCDF and DL-PCB in a complex sample relative to the two most toxic dioxins.

The TEQ value is calculated as follows: TEQ = ∑ [PCDD_i · TEF_i] + ∑ [PCDF_i · TEF_i] + ∑ [PCB_i · TEF_i].

The current TEF values were proposed by the World Health Organisation (WHO) in 2005 (van den Berg et al, 2006) and are termed WHO₂₀₀₅-TEF based on the year of the WHO expert meeting (Table 1).

Table 1. WHO Toxic equivalency factors (TEF) established in 2005 and compared with WHO TEF proposed in 2022 (DeVito et al, 2024).

The latest TEF values (WHO₂₀₂₂-TEF) were proposed by the World Health Organization (WHO) in 2022 following rigorous expert and statistical evaluation of an expanded set of studies of the congeners’ toxicological effects (DeVito et al, 2024). The WHO₂₀₂₂-TEF are listed in Table 1. They are expected to supersede the TEF derived in 2005.

Older analytical data generated before 2005 is generally reported as WHO₁₉₉₈-TEQ, I-TEQ or Nordic-TEQ. When interpreting TEQ results and evaluating, for example trends in the levels or exposure, it is important to know which TEF were used.

The most comprehensive estimates of dietary exposure have been provided by EFSA (EFSA, 2012, 2018). In their update of the monitoring of dioxins and PCB levels in food and feed (EFSA, 2012), a total of 13,797 samples were assessed for dioxins and DL-PCB and 19,181 samples for non-dioxin-like PCB (NDL-PCB). These samples were submitted between 1995 and 2010 by 26 European countries. At least one quantified congener of dioxins and DL-PCB was found in almost all samples, whereas at least one NDL-PCB indicator was quantified in 68.4 % of the feed and 82.6 % of the food samples. Eels and fish liver, and derived products, contained the highest average contamination levels of both dioxins and PCB. Depending on the population group, defined as the combination of age class and the respective survey, average exposure to dioxins and DL-PCB was estimated to be between 0.57 and 2.54 pg WHO2005-TEQ/kg bw per day, and the 95th percentile between 1.2 and 9.9 pg WHO2005-TEQ/kg bw per day. Average exposure to NDL-PCB indicators was estimated to be between 4.3 and 25.7 ng/kg bw per day and the 95th percentile between 7.8 and 53.7 ng/kg bw per day.  Fish, meat and dairy products appeared to be the highest contributing food groups to dietary exposure. Although the concentrations measured in foods are all extremely low in absolute terms, they are relatively high when compared with the various tolerable daily (or weekly or monthly) intake values that have been established by various organisations, including the WHO, in order to protect human health.

The TEF scheme does not currently cover other chemicals that have the same toxic mode of action, such as brominated and mixed halogenated analogues, and so may underestimate the true exposure to the totality of compounds that may contribute to this type of toxicity.

Global surveys of the occurrence of PCDD, PCDF and PCB in human milk have been performed by the WHO/UNEP (United Nations Environment Programme) since 1987. The three most recent surveys, from 2000 to 2010, have been reviewed (Van den Berg, 2016), and large global and regional differences were observed:

• levels of PCDD and PCDF were highest in India and some European and African countries. PCB levels were highest in East and West Europe,
• a temporal downward trend for PCDD, PCDF and PCB was indicated, and
• a risk-benefit assessment indicated that human milk levels of PCDD, PCDF and PCB were still significantly above those considered toxicologically safe. With respect to potential adverse health effects, a more dominant role of in utero exposure versus lactational exposure was indicated. If potential adverse effects were balanced against positive health aspects for (breastfed) infants, the advantages of breastfeeding far outweighed the possible disadvantages.

In the 2018 EFSA evaluation (EFSA, 2018), human chronic dietary exposure to PCDD, PCDF and DL-PCB was estimated using a data set containing:

• 19,965 food samples with all 29 congeners determined (17 PCDD/PCDFs and 12 DL-PCBs).
• 20,273 food samples with all 17 PCDD/PCDF congeners determined (including samples with the 29 congeners).
• 22,974 food samples with all 12 DL-PCB congeners determined (including samples with the 29 congeners).

An analysis of occurrence and consumption data from European countries indicated a mean total TEQ intake by Adolescents, Adults, Elderly and Very Elderly varied between 2.1 and 10.5 pg WHO2005-TEQ/kg bw/week. The P95 total TEQ intake for the same groups varied between 5.3 and 30.4 pg WHO2005-TEQ/kg bw/week. Both ranges imply a considerable exceedance of the TWI. Toddlers and Other Children showed a higher exposure than older age groups, and this was accounted for when deriving the TWI.

The main contributors to the mean dietary exposure, broken down by age group, were:

• Infants: Butter and Butter Oil (contributing 6.1-19.6%) and Fatty Fish (contributing 5.8-26.3%).
• Toddlers: Fatty Fish (contributing 5.9-13.9%), Cheese (contributing 5.9-21.8%) and Livestock Meat (contributing 7.7-16.2%).
• Other Children, Adolescents, Adults and Elderly: Fatty Fish (up to 56% contribution), Unspecified Fish Meat (up to 53.4% contribution), Cheese (up to 21.8% contribution) and Livestock Meat (up to 33.8% contribution).

There are several examples whereby food has become contaminated by dioxins and PCBs and many of these are discussed by Hoogenboom et al. (2015):

1. A nationwide survey of dioxins in foodstuffs in the USA, in the late 1990s, detected elevated levels of dioxins in some samples of poultry meats. Animal feed was implicated as the likely source of contamination, due to incorporation of ball clay (an anti-caking agent) in the production of the feeds. Control centred upon initially changing certain production practices to minimise the issue and subsequently in providing appropriate general advice, to the feed industry, regarding suitable monitoring to prevent repetition.
2. A programme of dioxin monitoring in foods, in Germany in the 1990s, initially showed a gradual decline which was followed by a gradual increase in milk, butter and meats. Investigation implicated contaminated citrus pulp (a feed ingredient for ruminants) being supplied from South America. Once again, changes in production practices of the feed material eliminated the issue. This particular incident affected other European countries, as well as Germany, which highlighted the international aspect of the situation, as well as emphasising the need for regularly analysing large numbers of food samples for dioxins in order to detect shifts in trends including seasonal variations.
3. An outbreak of illness in poultry, in Belgium in 1999, was traced to animal feed contaminated with dioxins in recycled fat used in its manufacture. Farms in France, Holland and Spain had also used the contaminated material for their livestock. Products from poultry and pigs were affected but not those from cattle. Farms were quarantined, and contaminated products destroyed. More than 30 countries temporarily banned certain food imports from Belgium, until the issue was resolved.
4. Ireland experienced trouble with elevated dioxin levels in some pork products in 2008. Again, contaminated animal feed was implicated. The cause of the contamination was thought to be fuel oil used in the drying of the affected feed.

In all these cases, issues were initially raised by the finding of elevated dioxin levels in food products during routine random testing.

In 2019, the environmental group International Pollutants Elimination Network (www.ipen.org) reported elevated levels of dioxins and PCBs in free-range chicken eggs in Tropodo, Indonesia. The nearby burning of plastic as fuel was the likely source of the contamination.

PCDD               polychlorinated dibenzo-p-dioxin

PCDF               polychlorinated dibenzofuran

PCB                 polychlorinated biphenyl

DL-PCB            dioxin-like PCB

NDL-PCB          non-dioxin-like PCB

POP                 persistent organic pollutant

EU-RL               European Union Reference Laboratory

NRL                  National Reference Laboratory

WHO                World Health Organisation

TEQ                  toxic equivalence

TEF                  toxic equivalency factor

TWI                  tolerable weekly intake

AHR                 aryl hydrocarbon receptor

GCMS              gas chromatography–mass spectrometry