Brominated dioxins (PBDD/Fs) in free range chicken eggs from sites affected by plastic waste

Abstract

In this research, fifteen pooled samples of free-range chicken eggs (from 14 hot spots around the world) and two reference samples from supermarkets (see Table 1) were analyzed for PBDD/Fs. All egg samples were also analyzed for PCDD/Fs and dl PCBs by HRGC-HRMS.
Conclusion: This study demonstrated that sub-standard settings of e-waste plastic disposal and metal smelting plants are growing sources of PBDD/Fs releases to the environment in developing countries. PBDD/Fs are also shown to contribute significantly to overall dioxin toxicity of eggs. All the sources of these toxic substances and their precursors must be eliminated or strictly controlled at national, regional and global level.

Full text

BROMINATED DIOXINS (PBDD/Fs) IN FREE RANGE CHICKEN EGGS FROM SITES
AFFECTED BY PLASTIC WASTE
Teebthaisong A1, Saetang P1, Petrlik J2,3, Bell L2,4, Beeler B2, Jopkova M3, Ismawati Y5, Kuepouo G6,
Ochieng Ochola G7, Akortia E8
1 EARTH, Nonthaburi, Thailand, 11130, ateebt@gmail.com;
2 International Pollutants Elimination Network (IPEN), Gothenburg, Sweden, 40010;
3 Arnika – Toxics and Waste Programme, Prague, Czech Republic, CZ17000;
4 National Toxics Network (NTN), Perth, Australia, 6054;
5 Nexus3, Jakarta, Indonesia, 10110;
6 Centre de Recherche et d‘Education pour le Développement (CREPD), Yaoundé, Cameroon, 00000
7 Centre for Environmental Justice and Development (CEJAD), Nairobi, Kenya, 00100;
8 Ghana Atomic Energy Commission, Radiation Protection Institute, Accra, Ghana, 00233.
Introduction
Free-range chicken eggs are sensitive indicators of POPs contamination in soils/dust and represent an important
human exposure pathway1-3. As “active samplers” they can be used to reveal POPs contamination, particularly in
areas impacted by polychlorinated dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/Fs; “chlorinated
dioxins” in brief) and polychlorinated biphenyls (PCBs)4-8, as well as by brominated flame retardants (BFRs)9-12.
This study aims to investigate brominated dioxins in free range chicken eggs sampled at sites close to sub-
standard plastic waste disposal locations in developing countries.
Polybrominated dibenzo-p-dioxins and dibenzofurans (PBDD/Fs; “brominated dioxins” in brief) are known to be
byproducts of commercial PBDE mixtures since 198613. They were also found to be byproducts of some novel
BFRs like DBDPE14 or BTBPE15-16. PBDFs have also been found to be formed by sunlight exposure during
normal use, as well as during disposal/recycling processes of flame-retarded consumer products17. Some studies
found PBDD/Fs in copper metal recycling18, in the air around a waste incinerator plant19, around an open
burning site20, and, recently, in children’s toys21. PBDD/Fs have been found to exhibit similar toxicity and health
effects as their chlorinated analogues (PCDD/Fs)22-26. They can, for example, affect brain development, damage
the immune system and fetus, or induce carcinogenesis25. “Both groups of compounds show similar effects, such
as induction of aryl hydrocarbon hydroxylase (AHH)/EROD activity, and toxicity, such as induction of wasting
syndrome, thymic atrophy, and liver toxicity”23.
With the broad use of BFRs in many applications, the question has arisen about the presence of PBDD/Fs in the
food chain, as they are persistent and bioaccumulative and found in different environmental compartments25. The
WHO expert panel has concluded that PBDD/Fs and some dioxin-like polybrominated biphenyls (dl-PBBs) may
contribute significantly to daily human exposure to the total dioxin toxic equivalencies (TEQs)26. In general,
PBDD/Fs are less regulated than PCDD/Fs. For example, PBDD/Fs are not currently listed under the Stockholm
Convention27. There is littledata available on their presence in the environment compared to PCDD/Fs. Recent
studies in China, Japan, Taiwan or Vietnam demonstrate that PBDD/Fs are widely present in Asia28-31. IPEN and
Arnika recently found PBDD/Fs in consumer products from recycled e-waste plastic sold worldwide32.
There is also very little information about their presence in food and/or consumer products, and whether they
have direct impacts on human health, including in vulnerable groups such as children and women of childbearing
age, particularly in developing countries where regulations and standards to control PBDD/Fs in food or waste
incineration emissions are lacking.
Materials and methods
In this research, fifteen pooled samples of free-range chicken eggs (from 14 hot spots around the world) and two
reference samples from supermarkets (see Table 1) were analyzed for PBDD/Fs in the MAS laboratory,
Muenster, Germany. The accredited method MAS_PA002, ISO/IEC 17025:2005 was used to determine
PBDD/Fs. The basic steps of the analyses can be summarized as follows:
- Addition of 13C12-labelled PBDD/F internal standards to the sample extract
- Multi-step chromatographic clean-up of the extract
- Addition of 13C12-labelled PBDD/F - recovery standards
- HRGC/HRMS analysis
- Quantification via the internal labelled PBDD/F-standards (isotope dilution technique and internal
standard technique).
All egg samples were also analyzed for PCDD/Fs and dl PCBs by HRGC-HRMS at the laboratory of the State
Veterinary Institute in Prague, Czech Republic. Toxic equivalency factors from the 2005 World Health
Organization reevaluation of dioxins and dioxin-like toxicity26,33 were used for the calculation of levels in TEQs
so that the contribution of PBDD/Fs to overall dioxin toxicity of each sample is known.

Table 1: Overview of samples of chicken eggs
Country
Activity
Locality
Sample ID
Month/year
of sampling
n eggs in
sample
Fat
(%)
Belarus
Recycling, pre-recycling
Gatovo
Gatovo
06/2014
3
15.4
Cameroon
Dumpsite
Yaoundé - Etetak Q.
YA-3
08/2018
6
14.3
Gabon
Waste incineration
Nkoltang
GA-E-NKOL
11/2019
5
13.6
Gabon
Dumpsite
Libreville - Ozounge
GA-E-OZOU
11/2019
5
11.2
Ghana
Waste yards / e-waste site
Agbogbloshie
AGB-E
12/2018
4
14.7
Ghana
Ref
Accra (supermarket)
ACC-M-E
12/2018
6
8.8
China
Waste incineration
Wuhan
Wuhan 2
09/2014
3
12.5
China
Waste incineration
Wuhan
Wuhan 1
03/2014
6
15.5
China
Ref
Beijing
Control
10/2014
3
10.1
Indonesia
Waste yards / e-waste site
Tangerang
SEM-E-1
11/2019
3
16.2
Indonesia
Waste incineration
Tropodo
TROP-E-1
10/2019
6
13.9
Indonesia
Metallurgy
Kendalsari
KEN-E-1/19
11/2019
6
14.3
Kenya
Waste yards / e-waste site
Nairobi – Ngara m.
KE_002
01/2020
6
16
Mexico
Recycling, pre-recycling
Guadalajara
GUDAL-EGG1
04/2019
5
14
Philippines
Waste yard / e-waste site
Bagong Silang
PH-E-1-2
09/2019
2
13.8
Tanzania
Dumpsite
Pugu Kinyamwezi
TZ-PU-KI_EGG
01/2020
9
18.0
Thailand
Waste yards / e-waste site
Samut Sakhon
Samut Sakhon
02/2015
3
11.6
Results and discussion
Concentrations of PBDD/Fs and PCDD/Fs plus dl PCBs in pooled egg samples in this study are summarized in
Table 2. PBDD/Fs levels in eggs above LOQ are also presented in the graph at Picture 1.
Table 2 Results of analyses
Activity Locality Sample ID
PBDD/Fs
PCDD/Fs + dl PCBs
(pg TEQ g-1 fat)
RE/E-w
Guadalajara
GUADAL-EGG1
5.4
5.9
RE/ELVs
Gatovo
Gatovo
<LOQ
16
WY/E-w
Tangerang
SEM-E-1
6.9
72
WY/E-w
Bagong Silang
PH-E-1 and 2
11
20
WY/E-w
Samut Sakhon
Samut Sakhon
16
96
WY/E-w/ELVs
Accra – Agbogbloshie
AGB-E
300
856
WY/E-w
Nairobi - Ngara market
KE_002
8.5
502
WI
Tropodo
TROP-E-1
0.33
172
WI
Wuhan
Wuhan 2
<LOQ
13
WI
Wuhan
Wuhan 1
27
16
WI
Nkoltang (MedWI)
GA-E-NKOL
< LOQ
15
DU
Yaoundé-Etetak Quart.
YA-3
0.17
13
DU
Libreville – Ozounge
GA-E-OZOU
2.0
21
DU
Pugu Kinyamwezi
TZ-PU-KI_EGG
3.0
35
ME
Kendalsari
KEN-E-1/19
0.57
60
Ref
Beijing (supermarket)
Beijing (superm.)
<LOQ
0.48
Ref
Acrra –supermarket
ACC-M-E
< LOQ
0.56
RE – recycling and pre-recycling; E-w – electronic waste; ELVs – end of life vehicles; WY – waste yards; WI –
waste incineration; DU – dumpsite; ME – metallurgy; Ref – reference sample; LOQ = 1.4 - 3.8 pg TEQ g-1 fat
The highest level of PBDD/Fs were measured in eggs from Agbogbloshie, an e-waste and ELVs scrapyard
followed by eggs from the vicinity of waste incinerators in Wuhan (27 pg TEQ g-1 fat). The observed high
PBDD/Fs levels in eggs from Samut Sakhon (16 pg g-1 fat), Bagong Silang (11 pg g-1 fat), Tangerang (7 pg g-1
fat) and Guadalajara (5 pg g-1 fat) can be explained by e-waste plastics being dismantled or shredded and/or
openly burned at some of these sites. PBDD/Fs are already present in e-waste plastics as by-products in
BFRs34,21, and they are also released as unintentionally produced chemicals formed as a result of burning plastics
treated with BFRs. The level of 300 pg TEQ g-1 fat from Agboglboshie is the highest ever measured level of
PBDD/Fs in eggs globally. A previous study reported a level of 62 pg TEQ g-1 dw in soil sample near the eggs
sampling site in Agboglboshie35.
The eggs from Wuhan had higher levels of TEQs originating from PBDD/Fs compared to PCDD/Fs and dl-
PCBs. The level of PBDD/Fs in TEQs concentration was equal to the sum of PCDD/Fs in eggs from

Guadalajara, the site where e-waste plastic is recycled into new products. High levels of PBDEs and novel-BFRs
of 31 and 379 ng g-1 respectively, were measured in the recycled plastic produced at this site36. E-waste plastic is
shredded at this site that might explain the potential pollution of the soil or dust with PBDD/Fs that are
subsequently ingested by free range chickens.
Two samples from supermarkets in Accra, Ghana and Beijing, China and three pooled free-range eggs from
Gatovo, Belarus, Wuhan 2, China and Nkoltang, Gabon had levels below the laboratory limit of quantitation
(LOQ).
A report from Ireland showed levels of 0.244 – 0.415 pg TEQ g-1 fat of PBDD/Fs in eggs37. That is two orders of
magnitude lower than the levels measured in free-range chicken egg samples from Wuhan or Samut Sakhon, and
three orders of magnitude lower than in the samples from Agbogbloshie. However, the levels of PBDD/Fs in egg
samples from Tropodo, Yaoundé – Etetak Q., and Kendalsari are similar to those measured in Ireland. It seems
that lower levels of PBDD/Fs were generated in the vicinity of aluminum smelters (Kendalsari, Indonesia)
and/or dumpsites in one of the African cities where dumping and burning of BFRs containing wastes was
probably not involved to such an extent as, for example, at e-waste sites or larger dumpsites. Low levels of
PBDD/Fs in eggs from Tropodo are hard to explain as very high levels of PBDEs were found in the same sample
coming from an area affected by burning plastic waste as fuel in tofu factories38-39.
Figure 1 Levels of PBDD/Fs measured in the samples
In the parallel research, we monitored also other POPs, including PCDD/Fs and dl-PCBs (see the results in Table
2) for comparison with levels of PBDD/Fs. Part of the research included calculation of dietary intake of selected
POPs through consumption of free-range chicken eggs. In some cases, brominated dioxins contribute
significantly to the total TEQ levels in the egg samples and at the same time to the dioxin exposure of the human
body, in particular for the egg samples from sites affected by e-waste23, because those plastics have originally
been treated with BFRs. This is mainly the case for the samples from Agbogbloshie, Wuhan, Tangerang, Samut
Sakhon, Bagong Silang, and Guadalajara.

Conclusion
This study demonstrated that sub-standard settings of e-waste plastic disposal and metal smelting plants are
growing sources of PBDD/Fs releases to the environment in developing countries. PBDD/Fs are also shown to
contribute significantly to overall dioxin toxicity of eggs. All the sources of these toxic substances and their
precursors must be eliminated or strictly controlled at national, regional and global level.
Acknowledgements
This study was conducted as a part of the following projects: “Increasing Transparency in Industrial Pollution
Management through Citizen Science and EIA System Enhancement” financed by EU AID (EuropeAid
2017/389-531), and co-financed by the Transition programme of the Czech Ministry of Foreign Affairs, Global
Greengrants Fund, and Thai Health Foundation. It is also part of a larger study focused on plastic waste
financially supported by Swedish government through IPEN.
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