Abundance of diet derived polychlorinated dibenzo-p-and polychlorinated dibenzofurans in the bodies and nests of the hornet vespa velutina nigrithorax and risks to human health in south korea
Similar to Abundance of diet derived polychlorinated dibenzo-p-and polychlorinated dibenzofurans in the bodies and nests of the hornet vespa velutina nigrithorax and risks to human health in south korea
Evaluation of the Toxicity of Dioxins & Dioxin Like PCBs - A Health Risk Appr...v2zq
Similar to Abundance of diet derived polychlorinated dibenzo-p-and polychlorinated dibenzofurans in the bodies and nests of the hornet vespa velutina nigrithorax and risks to human health in south korea (20)
Abundance of diet derived polychlorinated dibenzo-p-and polychlorinated dibenzofurans in the bodies and nests of the hornet vespa velutina nigrithorax and risks to human health in south korea
2. 1. Introduction
Polychlorinated dibenzo-p-dioxins (PCDDs) and polychlorinated di-
benzofurans (PCDFs) are representative persistent organic pollutants
(POPs), which are widely distributed in the environment. They are man-
aged under the Stockholm Convention on Persistent Organic Pollutants
(Stockholm Convention). This large group of compounds, usually re-
ferred to collectively as “dioxins,” have caused great concern worldwide
because of their toxicity, persistence, bioaccumulation, multimedia fate,
and long-range transport properties (Stockholm Convention). They are
emitted from natural sources, such as wild fires (Shih et al., 2008), and
anthropogenic sources, such as municipal incineration (Schuhmacher
et al., 2013) and vehicle emissions (Laroo et al., 2012).
Based upon the properties mentioned above, PCDD/Fs are highly li-
pophilic and have long biological half-lives. According to the investiga-
tion of apparent half-lives of Dioxins base on the literature review,
1,2,3,4,7,8-HxCDD show the over 10 years of half-lives. Especially,
half-lives of adult was larger than those of infant (Milbrath et al.,
2009) Thus, after they are emitted into the environment from emissions
sources, they accumulate in organisms, especially in predators at the top
of the food chain via natural pathways. Accumulated PCDD/Fs in organ-
isms are highly toxic to humans, and they can affect human health via
dietary exposure. Therefore, many studies focus on investigating the
levels and patterns of PCDD/Fs in not only environmental media like
the soil (Domingo et al., 2015; Kimbrough et al., 2010; Shang et al.,
2013), atmosphere (Domingo et al., 2017; Domingo et al., 2015; Oh
et al., 2006), and water/sediment (Chang et al., 2016), but also in organ-
isms (Ball et al., 1989), food (Manning et al., 2017; Perello et al., 2015),
and the human body (Bilau et al., 2009; Schuhmacher et al., 2013). In
addition, many studies have reported a relationship between insects
and pollution. For example, bees or honey have been reported to be
one of the biomarkers for atmospheric pollution monitoring related to
heavy metals (Balestra et al., 1992; Hladun et al., 2016; Rashed et al.,
2009; Sanchez-Bayo and Goka, 2014) and pesticides (Heard et al.,
2017; Sanchez-Bayo and Goka, 2014). In addition, heavy metals and
pesticides were detected in earthworms (Shang et al., 2013), grasshop-
pers (Devkota and Schmidt, 2000), and edible insects (Poma et al.,
2017), indicating that emitted pollutants accumulate in organisms.
Based upon the studies of relationships between organisms and pollu-
tion, we focus here on the social wasp because of unique traditional cus-
toms in South Korea.
Emitted PCDD/Fs from industrial facilities were deposited into the
soil and water (Oh et al., 2006), and they can then accumulate in organ-
isms, such as social wasps, via natural pathways. Due to the ecological
behaviors of social wasps, such as foraging and the intake of foods, the
possibility of bioaccumulation of PCDD/Fs from environmental media
and the food chain is high if environmental media is polluted as a result
of anthropogenic activity.
Interestingly, social wasps have been used as ingredients in tradi-
tional liquor for a long time in South Korea because they are well-
known to promote human health as published in Donguibogam, Princi-
ples, and Practice of Eastern Medicine written by HeoJun in 1615 (Heo,
1615). According to the literature, the Vespid nest (Nidus Vespae) has
pharmacological efficacy for treating inflammatory conditions, viruses,
tumors, epilepsy, convulsions, and dental disease. In addition, although
not confirmed, some folk remedies indicate that there is a curative sub-
stance in the venom of adult and larvae saliva; therefore, many Koreans
make and drink a wasp liquor, which involves placing a wasp's nest (in-
cluding the living adults and larvae) into an alcohol. Recently, as interest
in human health has increased, studies of the efficacy of nests and larvae
saliva on human disease conditions have been performed (Guan et al.,
2012; Tsuchita et al., 1997; Xiao et al., 2007), and the demand for this
has been rapidly increasing.
Koreans have a high probability of dietary exposure to PCDD/Fs
through drinking traditional liquor made from polluted wasps and
nests. Normally, Decomposition of PCDD/Fs were required a high
temperature like over 500 K (over 200 °C) (Chen et al., 2012). Based
on this, we hypothesized that if PCDD/Fs were detected in social
wasps and they were used as ingredients in traditional liquor, this
might increase human health risks as a result of exposure to PCDD/Fs
because PCDD/Fs might be not decomposed.
The objective of this preliminary study was to investigate the levels
and patterns of PCDD/Fs in order to evaluate human health risks via in-
gestion of traditional South Korean liquor made from social wasps and
their nests.
2. Materials and methods
2.1. Target compounds and collection of samples
Target compounds of this study were the 17 PCDD/Fs (2378-TCDD,
12378-PeCDD, 123478-HxCDD, 123678-HxCDD, 123789-HxCDD,
1234678-HpCDD, OCDD, 2378-TCDF, 12378-PeCDF, 23478-PeCDF,
123478-HxCDF, 123678-HxCDF, 234678-HxCDF, 123789-HxCDF,
1234678-HpCDF, 1234789-HpCDF, and OCDF).
In order to investigate the levels and patterns of PCDD/Fs in wasps,
we selected the most common exotic hornet in South Korea as a test
subject, the yellow-legged hornet (Vespa velutina nigrithorax). The
yellow-legged hornet spread across the whole country after the first in-
vasion of Busan in South Korea in 2003 (Choi et al., 2013a; Choi et al.,
2013b; Kim et al., 2006). They have a very large colony, consisting of
about 5–10 combs and over 2000 individuals per nest (Choi et al.,
2012b; Perrard et al., 2009). The family Vespidae is a social insect (espe-
cially social wasps), which is divided into three castes that include the
queen, workers, and males. They undergo a complete metamorphosis
with four stages of development, including the egg, larva, pupa, and
adult (Wilson, 1971). This is indicating that feed and inhabitant cycle
between adult and larvae is different, and then accumulation and/or de-
tection of PCDD/Fs in social wasp's sample from polluted environmental
media could be shown different. The adults feed on carbohydrates, such
as nectar, the sap of oak trees, rotting sweet fruits, and honey. The adults
also attack various insects using their venomous sting and two strong
mandibles. Therefore, they are able to forage various insects, such as
grasshoppers, beetles, caterpillars, flies, honeybees, and other wasps.
They inhabit forests and rural and urban areas, and their density is
very high, especially in urban areas (Choi et al., 2012a; Choi and
Kwon, 2015). The food they capture are mostly masticated and then
fed to the larvae developing in their nests (Matsuura and Yamane,
1990). Nesting mainly occurs in open places, such as grasses, bushes,
branches, rocks, and eaves, as well as closed places, such as under-
ground, tree holes, and building walls. Nests are constructed of wood
pulp collected by the adults (Archer, 2012; Matsuura and Yamane,
1990) and the concentration of PCDD/Fs in nest can be interpreted as in-
habitant environmental pollution. Due to these reasons, collected
wasp's samples were divided to adult, larvae, and nest (Fig. 1).
The samples for this study were collected in November 2017 from
three sampling sites in South Korea: the Daegu metropolitan area, Mt.
Jiri (located in Kyoungnam province), and Mt. Palgong (located
Kyoungbuk province). Mt. Jiri and Mt. Palgong were rural area, thus
there is no anthropogenic emission sources such as industrial facilities
nearby sampling sites. In case of Daegu metropolitan, it is a representa-
tive complex city including dye industrial factories and heavy residen-
tial area over 2 million population (Statistics Korea). Fifteen total
samples were collected, and they were stored at −4 °C in order to eu-
thanize the wasps and preserve them for analysis.
2.2. Analysis and QA/QC
Four types of samples were collected: adults, larvae, combs in nests,
and envelopes in nests. They were freeze-dried and homogenized for a
chemical analysis of PCDD/Fs. Homogenized samples weighed approxi-
mately 15 g, and they were mixed with sodium sulfate. They were
1034 H.-O. Kwon et al. / Science of the Total Environment 654 (2019) 1033–1039
3. extracted using Soxhlet with hexane/dichloromethane (1:1 v/v) for
24 h, and then surrogate standards (EPA-1613LCS for PCDD/Fs,
Wellington Laboratories, Canada) were added to each sample before ex-
traction process. The extracted samples were evaporated and used in a
clean-up process, which involved elution with hexane on multi-layer
silica gel columns followed by a re-evaporation process. Internal stan-
dards (EPA-1613ISS and 68B-IS, Wellington Laboratories, Canada)
were added to GC vials prior to instrumental injection. Evaporated
final samples were analyzed using a spectrometer (GC/HRMS, Autospec
Premier™, Waters) with a DB5-MS column (50 m, 0.25-mm ID, 0.25-μm
film thickness). The injection volume of the final sample into the GC was
1 μL as a splitless mode.
For Quality Assurance vs Quality Control (QA/QC), instrumental de-
tection limits (IDL) were calculated by multiplying the standard devia-
tion by a factor of 3.14 based on seven replication analyses of
calibration standards (CS). These were regarded as the limits of detec-
tion (LOD), while concentrations below the LODs were considered
non-detects (NDs). The ranges of LOD for PCDDs (from 2378-TCDD to
OCDD) and PCDFs (from 2378-TCDF to OCDF) were 0.02–0.03 pg/μL
and 0.02–0.04 pg/μL, respectively. The recovery ratios of surrogate stan-
dards ranged from 77% to 110% for PCDD/Fs in all samples, and certified
reference materials (CRM) of fish tissue for organic contaminant analy-
sis (WMF-01, Wellington laboratories, Canada) were analyzed. The
measured values were within the acceptable range of CRM concentra-
tions, and the recovery of CRM was over 90%; therefore, we concluded
that the QA/QC was satisfactory.
2.3. Human health risk assessment
In order to evaluate the human health risk from PCDD/Fs associated
with drinking traditional liquor made from contaminated wasps, the
human health risk assessment was performed in accordance with sug-
gestions from the United States Environmental Protection Agency
(US-EPA) for hazard identification, dose responses, exposure assess-
ments, and the determination of risk (EPA, 2018). The human health
risk assessment for the dietary intake of PCDD/Fs via traditional liquor
made from polluted wasps was conducted based on the toxicity equiv-
alent concentrations (TEF) suggested by the World Health Organization
(WHO, 2000) and the tolerable daily intake (TDI) of PCDD in food ac-
cording to the following equation:
Risk ¼ Cp  FI=BWð Þ=TDIð Þ Â 100 ð1Þ
where risk is the human health risk (%), Cp is the concentration of
PCDD/Fs (pg WHO-TEQ/g) in social wasps, FI is the food intake (g/
day), BW is the body weight of exposer (kg), and TDI is the tolerable
daily intake of PCDD/Fs. In order to evaluate the potential human health
risks of dietary exposure, the daily intake of PCDD/Fs was calculated
based on two scenarios related to the handling of ND. According to the
ND data handling, human health risks can be changed, and then the re-
sult can lead to incorrect interpretations (Barghi et al., 2016). Therefore,
the application of a suitable method for addressing ND data is required,
and two scenarios, which considered the ND data to be zero and were
instrumental for detecting and handling ND data, were applied. The
WHO has suggested that the TDI for PCDD/Fs fall in the range of
1–4 pg WHO-TEQ/kg of body weight per day (WHO, 2000). The estima-
tion of food consumption was conducted based on a 2011 investigation
by the Nutrition and Health Survey in Korea. Traditional liquor made by
wasp is one of the type for traditional Korean liquor. Due to the no infor-
mation of daily consumption of liquor made by social wasp, 0.020 g/d
with a 0.010 g/d standard deviation of the daily consumption of tradi-
tional Korean liquor was used in order to calculate the risk (KRIDI,
2011), and the average body weight of a Korean was 62.8 kg (KRIDI,
2011). In order to calculate human health risk based on a probabilistic
approach using Monte Carlo simulations, the assumption of distribution
for each parameter is required based on parameter properties. Nor-
mally, the concentration of pollutants assumed a triangle distribution
based upon the inputted min, mean, and max concentration (Oracle,
2011). The cases of food intake and body weight were assumed to
have normal distributions because they do not change significantly,
and the TDI used was 4 pg WHO-TEQ/kg body weight/day as a constant
without any assumption. Any calculation result over 100% indicated a
harmful effect on human health as a result of dietary exposure to
PCDD/Fs. Meanwhile, a score below 100% indicated a non-harmful effect
on human health by PCDD/Fs. In addition, a probabilistic approach using
a Monte Carlo simulation was conducted in order to avoid any incorrect
interpretations of the results (Oracle, 2011; Schuhmacher et al., 2013),
and 10,000 simulation trials were performed.
3. Results and discussion
3.1. Congener concentration and patterns
Concentrations and patterns of each congener in the four sample
types of wasps collected in South Korea are presented (Fig. 2). Of the
17 PCDD/Fs congeners in the 15 samples, the most toxic congener
(2378-PCDD) was not detected in all samples. In the case of OCDD, it
was the most frequently detected in all but one sample, followed by
1234678-HpCDF and 123478-HxCDF. Abundant OCDD patterns in sam-
ples were not novel patterns in environmental media because there
have been many previous studies reporting this in such samples as the
soil (Rovira et al., 2010; Shang et al., 2013), air (Rovira et al., 2010),
and biological materials that include tern eggs (Zhou et al., 2017), fish
(Costopoulou et al., 2016), and breast milk (Schuhmacher et al., 2013).
The highest concentration among the 15 samples for 17 congeners
was OCDD 35.47 pg/g based on the dry weight from the envelope of a
nest harvested in Daegu. This concentration was over 30 times greater
than that of the lowest samples without non-detected samples. In addi-
tion, the highest mean and median concentrations of OCDD for the 15
samples were 9.16 and 3.61 pg/g based on dry weight, respectively.
The detection rate of OCDD was over 90%, and only one sample was
non-detectable. Even though the concentration of OCDD was high and
there was abundant congener, the highest TEQ concentration was
23478-PeCDF (0.27 pg WHO-TEQ/g dw), which was primarily due to
the low TEF of PCDD.
The order of the mean concentrations among the seventeen PCDD/Fs
included OCDF (13.82 pg/g), OCDD (9.16 pg/g), 1234678-HpCDD
(3.39 pg/g), 1234678-HpCDF (2.19 pg/g), and others. The highest
mean concentration was OCDF as 13.82 pg/g based on dry weight,
which was detected in only one sample. Thus, this was not a represen-
tative pattern. The order of the mean TEQ concentrations were 23478-
PeCDF (0.27 pg WHO-TEQ/g dw), 2378-TCDF, and 123789-HxCDF.
Fig. 1. Target species, Vespa velutina nigrithorax, and nest to investigate the levels and
patterns of PCDD/Fs at three sampling sites in South Korea.
1035H.-O. Kwon et al. / Science of the Total Environment 654 (2019) 1033–1039
4. Among the 17 congeners, the highest TEQ concentration was 23478-
PeCDF (0.71 pg WHO-TEQ/g dw), followed by 2378-TCDF and 123789
HxCDF.
Among the 17 PCDD/Fs congeners in all samples, OCDD was the
dominant congener (62%), followed by 1234678-HpCDF (11%) and
1234678-HpCDD (8%). In the case of the adult samples, only OCDD
was detected in one sample. 12478-PeCDF showed the most dominant
patterns in larvae (over 90%), combs (41%), and envelopes (49%), re-
spectively. These patterns did not display statistical significance due to
the lack of samples. Because the largest concentration was detected in
one sample, the whole pattern might be distorted. Thus, further studies
will consider these results, and abundant samples and congener pat-
terns will be discussed.
3.2. Concentrations and patterns of PCDD/Fs in samples
The concentrations of 17 PCDD/Fs in all samples is shown Table 1
and Fig. 3, presenting the concentrations (pg/g dw) and toxic equiva-
lents (pg WHO-TEQ/g dw) suggested by the WHO. In particular, TEF
has been used to evaluate the risks to humans and other mammals
(Van den Berg et al., 1998).
The concentrations of seven PCDD were from ND–42.23 pg/g dw
with a mean (9.68 pg/g dw) and median (3.29 pg/g dw) concentration,
which corresponded to 0.02 pg WHO-TEQ/g dw for a mean
concentration and 0.0010 pg WHO-TEQ/g dw for a median concentra-
tion, respectively. The range of PCDF was ND–20.71 pg/g dw with
4.03 pg/g dw of mean and 1.68 pg/g dw of median concentrations,
which corresponded to 0.24 pg WHO-TEQ/g dw of mean and 0.06 pg
WHO-TEQ/g dw of median concentrations, respectively. In total, the
concentration of PCDD detected was larger than that of PCDF. However,
comparative data for the TEQ concentrations of PCDD and PCDF showed
that concentrations of PCDF were larger than those of PCDD because of
the low TEF value of the detected PCDD congeners.
Concentrations of ∑17 PCDD/Fs ranged from ND to 54.77 pg/g dw
with a mean concentration of 13.70 pg/g dw and a median concentra-
tion of 5.18 pg/g dw, respectively. When assessing PCDD/Fs concentra-
tions in the WHO-TEF 2005, PCDD/Fs ranged from ND–1.45 pg WHO-
TEQ/g dw with a mean concentration of 0.25 pg WHO-TEQ/g dw and a
median concentration of 0.06 pg WHO-TEQ/g dw in 15 samples col-
lected in South Korea.
As a result of the comparative data for the concentrations of PCDD/Fs
in organism samples from different regions of the world, the average
levels of ∑17 PCDD/Fs in this study were compared to those of previous
studies. The levels of PCDD/Fs in social wasps were lower than those of
earthworm samples and soil samples from an E-waste dismantling area
in China (as much as 10 times less) (Shang et al., 2013). However, the
levels of PCDD/Fs in soil samples collected in Spain yielded similar re-
sults as this study (Rovira et al., 2010).
Fig. 2. Concentration and patterns for each of the 17 PCDD/Fs congeners in the four sample types (right) in wasps collected from South Korea. Fifteen (n = 15) samples were collected.
(a) The mean TEQ concentration of each congener and (b) patterns of each congener in all samples (left) versus four sample types (right).
1036 H.-O. Kwon et al. / Science of the Total Environment 654 (2019) 1033–1039
5. As a result of mean TEQ concentrations in four sample types that in-
cluded adults, larvae, combs, envelopes of nests, and combs in nests, the
highest mean concentration of ∑17 PCDD/Fs in the envelopes of nests
was 0.88 pg WHO-TEQ/g dw, followed by combs in nests (0.55 pg
WHO-TEQ/g dw), larvae (0.12 pg WHO-TEQ/g dw), and adults
(0.0005 pg WHO-TEQ/g dw). In total, the concentration of PCDD/Fs in
the nests were greatest in the 17 PCDD/Fs from larvae and adults be-
cause the nests consisted of wood pulp above the soil environment. In
addition, it seemed that the concentration of PCDD/Fs decreased in the
process of molting from larvae to adults (including the pupa stage).
The outcome, which was a high level of PCDD/Fs in the nest, was as-
sumed to be the reason.
Comparisons of ∑17 PCDD/Fs for all samples showed that the enve-
lopes of nests harvested from Daegu had high concentrations among the
15 samples, including 1.47 pg WHO-TEQ/g dw. This was followed by
combs in nests collected from Daegu (0.77 pg WHO-TEQ/g dw). As a re-
sult of comparing the concentrations at three sampling sites, Daegu
showed higher concentrations (0.99 pg WHO-TEQ/g dw) than those of
other sites (0.37 pg WHO-TEQ/g dw of Mt. Jiri and 0.20 pg WHO-TEQ/
g dw of Mt. Palgong). This was primarily due to the properties of the
sampling site in Daegu, which is a metropolitan city in South Korea.
Thus, there are many kinds of emissions sources of PCDD/Fs, such as in-
dustrial facilities (Oh et al., 2006; Onofrio et al., 2014) and vehicle emis-
sions (Laroo et al., 2012).
3.3. Human health risk assessment via dietary exposure
Using the probabilistic risk assessment based on the measured data
and literature data for Koreans, the human health risk from the intake of
traditional liquor made from polluted wasps of PCDD/Fs is presented
Fig. 4. Over 100% of the risk was indicated to have a harmful effect on
human health via exposure to PCDD/Fs. Meanwhile, a less than 100%
risk was interpreted to be a non-harmful effect. The deterministic ap-
proach showed that less than 30% of the possibility of daily intake of tra-
ditional liquor made from wasps was based on both scenarios related to
handling ND data.
Table 1
Results of each congener concentration (pg/g) and TEQ concentration (pg WHO-TEQ/g) based on the dry weight of 17 PCDD/Fs from four types of samples collected at three sampling sites
in South Korea (n = 15).
Congener TEF value Concentration (pg/g based on dry weight) TEQ concentration (pg WHO-TEQ/g dw dry weight)
Mean Median SD Mean Median SD
2378-TCDD 1 All ND All ND All ND All ND All ND All ND
12378-PeCDD 1 All ND All ND All ND All ND All ND All ND
123478-HxCDD 0.1 All ND All ND All ND All ND All ND All ND
123678-HxCDD 0.1 All ND All ND All ND All ND All ND All ND
123789-HxCDD 0.1 All ND All ND All ND All ND All ND All ND
1234678-HpCDD 0.01 3.3864 2.4410 1.9888 0.0339 0.0244 0.0199
OCDD 0.0003 9.1578 3.6051 11.0102 0.0027 0.0011 0.0033
2378-TCDF 0.1 0.8283 0.6171 0.6323 0.0828 0.0617 0.0632
12378-PeCDF 0.03 1.3279 1.3279 0.0109 0.0398 0.0398 0.0003
23478-PeCDF 0.3 0.8975 0.7028 0.7551 0.2693 0.2108 0.2265
123478-HxCDF 0.1 0.5833 0.3863 0.5070 0.0583 0.0386 0.0507
123678-HxCDF 0.1 0.6867 0.4742 0.3881 0.0687 0.0474 0.0388
234678-HxCDF 0.1 All ND All ND All ND All ND All ND All ND
123789-HxCDF 0.1 0.7113 0.4649 0.5215 0.0711 0.0465 0.0521
1234678-HpCDF 0.01 2.1929 1.4673 1.6374 0.0219 0.0147 0.0164
1234789-HpCDF 0.01 All ND All ND All ND All ND All ND All ND
OCDF 0.0003 13.8179 13.8179 All ND 0.0041 0.0041 All ND
∑17 PCDD/Fsa
13.7011 5.1830 16.0165 0.2524 0.0603 0.4026
a
Mean and median concentrations were calculated for each sample of ∑17 PCDD/Fs.
Fig. 3. Concentrations of ∑17 PCDD/Fs in wasps from different types of samples, including adults, larvae, comb in nest, and envelopes of nests at three sampling sites in South Korea.
1037H.-O. Kwon et al. / Science of the Total Environment 654 (2019) 1033–1039
6. In the case of the probabilistic approach using the Monte Carlo sim-
ulation, the concentration of PCDD/Fs was the greatest sensitive param-
eter (as much as more than 50% from sensitivity analysis). Thus, the
measured concentration in the wasp family was the most important pa-
rameter to evaluate human health risks. According to the ND data as a
zero and IDL, the risk level (%) ranged from 0% to 95% and 0% to 105%
in the case of zero and IDL. The result of 105%, which was considered
IDL for the ND data, indicated that there was a possibility for harmful ef-
fects on human health by PCDD/Fs in the worst-case situation. Despite
the less than 100% risk by the deterministic approach, the result of the
probabilistic interpretation showed the risk probability when Koreans
were exposed via intake of traditional liquor made from contaminated
wasps.
In previous studies, the estimation of the human health risk of PCDD/
Fs via dietary exposure was conducted on seafood (Costopoulou et al.,
2016; Manning et al., 2017; Shin et al., 2016), meat (Lee et al., 2016),
eggs (Van Overmeire et al., 2009), and offal (Fernandes et al., 2010).
The detection and investigation of PCDD/Fs in the food chain and food
are a scientific issue because food products from animal origins (such
as meat, fish, and dairy products) are the main contributors to dioxin in-
take. Seafood samples collected at Sydney Harbor were considered safe
for human consumption (Manning et al., 2017). However, farmed fish
produced in Greece (Costopoulou et al., 2016) and eggs from Belgium
(Van Overmeire et al., 2009) were shown to have a safe level. In the
case of South Korea, various fish species available at food markets
were reported to be safe (Shin et al., 2016). Likewise, the levels from
biota samples in this study showed variations due to the variety of con-
centrations related to the vicinity emission sources and consumption
habits.
In summary, the result of deterministic and probabilistic approaches
indicate that the human health risk for Koreans via dietary exposure
from traditional liquor made with polluted wasps is not at a dangerous
level. However, there is a potential risk from dietary exposure when the
concentration of PCDD/Fs increases due to air pollution or other envi-
ronmental changes. Therefore, continuous environmental monitoring
of the intake of polluted wasp in the diet is required. In addition, moni-
toring of not only PCDD/Fs, but also other kinds of pollutants (such as
heavy metals and/or pesticides) in wasp is necessary due to the unique
traditions of South Korea.
4. Conclusions
This preliminary study focused on investigating the concentration of
PCDD/Fs in social wasps, such as V. v. nigrithorax, from South Korea. The
detection of PCDD/Fs in social wasps is significant because this is evi-
dence of a relationship between environmental pollution and the or-
ganism. Thus, the investigation of the levels of pesticides, fungicides,
and heavy metals in social wasps is also required because those pollut-
ants have already been detected in honeybees. Social wasps are a pred-
ator of honeybee health, indicating that there is a possibility of
bioaccumulation via the food chain from honeybees to social wasps. In
addition, the source of PCDD/Fs in wasps and nests might be related to
the soil environment via dermal contact during nest-building and food
ingestion. However, there is no scientific evidence for this, and the up-
take or bioaccumulation of pollutants in organisms is a complex process
with environmental media and the organism itself. The health risk as-
sessment for Koreans based on the assumption of dietary exposure
from traditional liquor made from polluted wasps and nests was
deemed not dangerous. However, these results indicated that there is
a likely exposure pathway for PCDD/Fs due to the dietary customs in
South Korea. In addition, continuous monitoring of the levels and pat-
terns of environmental contaminants in wasps and nests is required in
order to evaluate the human health risks associated with the consump-
tion of traditional liquor made from contaminated wasps and nests.
References
Archer, M.E., 2012. Vespine Wasps of the World: Behaviour, Ecology & Taxonomy of the
Vespinae. Vol 4. Siri Scientific Press Monograph Series.
Balestra, V., Celli, G., Porrini, C., 1992. Bees, honey, larvae and pollen in biomonitoring of
atmospheric pollution. Aerobiologia 8, 122–126.
Ball, M., Päpke, O., Lis, Z.A., Scheunert, K.P.C.D.D., 1989. PCDF in mice and insects from var-
ious environments. Chemosphere 18, 759–765.
Barghi, M., Choi, S.D., Kwon, H.O., Lee, Y.S., Chang, Y.S., 2016. Influence of non-detect data-
handling on toxic equivalency quantities of PCDD/Fs and dioxin-like PCBs: a case
study of major fish species purchased in Korea. Environ. Pollut. 214, 532–538.
Bilau, M., De Henauw, S., Schroijen, C., Bruckers, L., Hond, E.D., Koppen, G., et al., 2009. The
relation between the estimated dietary intake of PCDD/Fs and levels in blood in a
Flemish population (50–65 years). Environ. Int. 35, 9–13.
Chang, H.-J., Lin, T.-F., Whang, L.-M., Wu, Y.-J., 2016. Congener profiles of polychlorinated
dibenzo-p-dioxins and polychlorinated dibenzofurans (PCDD/Fs) in sediment, water,
and fish at a soil contamination site in Taiwan. J. Environ. Sci. Health A 51, 251–261.
Chen, D.-Z., Hu, Y.-Y., Zhang, P.-F., 2012. Hydrothermal treatment of incineration fly ash
for PCDD/Fs decomposition: the effect of iron addition. Environ. Technol. 33,
2517–2523.
Choi, M.B., Kwon, O., 2015. Occurrence of hymenoptera (Wasps and bees) and their for-
aging in the Southwestern part of Jirisan National Park, South Korea. J. Ecol. Environ.
Sci. 38, 367–374.
Choi, M.B., Kim, J.K., Lee, J.W., 2012a. Increase trend of social hymenoptera (wasps and
honeybees) in urban areas, inferred from moving-out case by 119 rescue services
in Seoul of South Korea. Entomol. Res. 42, 308–319.
Choi, M.B., Martin, S.J., Lee, J.W., 2012b. Distribution, spread, and impact of the invasive
hornet Vespa velutina in South Korea. J. Asia Pac. Entomol. 15, 473–477.
Choi, M.B., Kim, J.K., Lee, J.W., 2013a. Checklist and distribution of Korean Vespidae
revisited (in Korean with English abstract). Korean J. Appl. Entomol. 52, 85–91.
0
20
40
60
80
100
0% 10% 20% 30% 40% 50% 60% 70% 80% 90% 100%
Risk(%)
ND=0 ND=IDL
Fig. 4. Results of the human health risks of PCDD/Fs via ingestion of traditional liquor made from Vespa velutina nigrithorax using a Monte Carlo simulation as a probabalistic approach.
1038 H.-O. Kwon et al. / Science of the Total Environment 654 (2019) 1033–1039
7. Choi, M.B., Lee, S.-A., Suk, H.Y., Lee, J.W., 2013b. Microsatellite variation in colonizing pop-
ulations of yellow-legged Asian hornet, Vespa velutina nigrithorax, in South Korea: ge-
netic variation of Vespa velutina. Entomol. Res. 43, 208–214.
Costopoulou, D., Vassiliadou, I., Leondiadis, L. PCDDs, 2016. PCDFs and PCBs in farmed fish
produced in Greece: levels and human population exposure assessment.
Chemosphere 146, 511–518.
Devkota, B., Schmidt, G.H., 2000. Accumulation of heavy metals in food plants and grass-
hoppers from the Taigetos Mountains, Greece. Agric. Ecosyst. Environ. 78, 85–91.
Domingo, J.L., Rovira, J., Vilavert, L., Nadal, M., Figueras, M.J., Schuhmacher, M., 2015.
Health risks for the population living in the vicinity of an integrated waste manage-
ment facility: screening environmental pollutants. Sci. Total Environ. 518-519,
363–370.
Domingo, J.L., Rovira, J., Nadal, M., Schuhmacher, M., 2017. High cancer risks by exposure
to PCDD/Fs in the neighborhood of an integrated waste management facility. Sci.
Total Environ. 607–608, 63–68.
EPA, 2018. United States Environmental Protection Agency (U.S EPA), 2018.
Fernandes, A., Mortimer, D., Rose, M., Gem, M., 2010. Dioxins (PCDD/Fs) and PCBs in offal:
occurrence and dietary exposure. Chemosphere 81, 536–540.
Guan, X., Zhou, Y., Liang, X., Xiao, J., He, L., Li, J., 2012. Effects of compounds found in Nidus
Vespae on the growth and cariogenic virulence factors of Streptococcus mutans.
Microbiol. Res. 167, 61–68.
Heard, M.S., Baas, J., Dorne, J.-L., Lahive, E., Robinson, A.G., Rortais, A., et al., 2017. Compar-
ative toxicity of pesticides and environmental contaminants in bees: are honey bees a
useful proxy for wild bee species. Sci. Total Environ. 578, 357–365.
Heo, J., 1615. Donguibogam, Principles and Practice of Eastern Medicine.
Hladun, K.R., Di, N., Liu, T.-X., Trumble, J.T., 2016. Metal contaminant accumulation in the
hive: consequences for whole-colony health and brood production in the honey bee
(Apis melliferaL.): impact of metal contaminants on honey bee health. Environ.
Toxicol. Chem. 35, 322–329.
Kim, J.-K., Choi, M., Moon, T.-Y., 2006. Occurrence of Vespa velutina Lepeletier from Korea,
and a revised key for Korean Vespa species (Hymenoptera: Vespidae): Vespa velutina
and revised key to Vespa from Korea. Entomol. Res. 36, 112–115.
Kimbrough, R.D., Krouskas, C.A., Leigh Carson, M., Long, T.F., Bevan, C., Tardiff, R.G., 2010.
Human uptake of persistent chemicals from contaminated soil: PCDD/Fs and PCBs.
Regul. Toxicol. Pharmacol. 57, 43–54.
KRIDI, 2011. Investigation on the Nutrition and Health Survey in Korea.
Laroo, C.A., Schenk, C.R., Sanchez, L.J., McDonald, J., Smith, P.L., 2012. Emissions of PCDD/
Fs, PCBs, and PAHs from legacy on-road heavy-duty diesel engines. Chemosphere 89,
1287–1294.
Lee, C.-C., Lin, H.-T., Kao, Y.-M., Chang, M.-H., Chen, H.-L., 2016. Temporal trend of
polychlorinated dibenzo-p-dioxin/polychlorinated dibenzofuran and dioxin like-
polychlorinated biphenyl concentrations in food from Taiwan markets during
2004–2012. J. Food Drug Anal. 24, 644–652.
Manning, T.M., Roach, A.C., Edge, K.J., Ferrell, D.J., 2017. Levels of PCDD/Fs and dioxin -like
PCBs in seafood from Sydney Harbour, Australia. Environ. Pollut. 224, 590–596.
Matsuura, M., Yamane, S., 1990. Biology of the Vespine Wasps. Springer-Verlag, Berlin
Heidelberg.
Milbrath, M.O.G., Wenger, Y., Chang, C.-W., Emond, C., Garabrant, D., Gillespie, B.W., et al.,
2009. Apparent half-lives of dioxins, furans, and polychlorinated biphenyls as a func-
tion of age, body fat, smoking status, and breast-feeding. Environ. Health Perspect.
117, 417–425.
Oh, J.-E., Choi, S.-D., Lee, S.-J., Chang, Y.-S., 2006. Influence of a municipal solid waste in-
cinerator on ambient air and soil PCDD/Fs levels. Chemosphere 64, 579–587.
Onofrio, M., Spataro, R., Botta, S., 2014. Deposition fluxes of PCDD/Fs in the area surround-
ing a steel plant in northwest Italy. Environ. Monit. Assess. 186, 3917–3929.
Oracle, 2011. Crystal ball User Guide.
Perello, G., Diaz-Ferrero, J., Llobet, J.M., Castell, V., Vicente, E., Nadal, M., et al., 2015.
Human exposure to PCDD/Fs and PCBs through consumption of fish and seafood in
Catalonia (Spain): temporal trend. Food Chem. Toxicol. 81, 28–33.
Perrard, A., Haxaire, J., Rowtais, A., Villemant, C., 2009. Observations on the colony activity
of the Asian hornet Vespa velutina Lepeletier 1836 (Hymenoptera: Vespidae:
Vespinae) in France. Annales de la Societe Entomologique de France 45, 119–127.
Poma, G., Cuykx, M., Amato, E., Calaprice, C., Focant, J.F., Covaci, A., 2017. Evaluation of
hazardous chemicals in edible insects and insect-based food intended for human con-
sumption. Food Chem. Toxicol. 100, 70–79.
Rashed, M.N., El-Haty, M.T.A., Mohamed, S.M., 2009. Bee honey as environmental indica-
tor for pollution with heavy metals. Toxicol. Environ. Chem. 91, 389–403.
Rovira, J., Mari, M., Nadal, M., Schuhmacher, M., Domingo, J.L., 2010. Environmental mon-
itoring of metals, PCDD/Fs and PCBs as a complementary tool of biological surveil-
lance to assess human health risks. Chemosphere 80, 1183–1189.
Sanchez-Bayo, F., Goka, K., 2014. Pesticide residues and bees – a risk assessment. PLoS
One 9, e94482.
Schuhmacher, M., Kiviranta, H., Ruokojarvi, P., Nadal, M., Domingo, J.L., 2013. Levels of
PCDD/Fs, PCBs and PBDEs in breast milk of women living in the vicinity of a hazard-
ous waste incinerator: assessment of the temporal trend. Chemosphere 93,
1533–1540.
Shang, H., Wang, P., Wang, T., Wang, Y., Zhang, H., Fu, J., et al., 2013. Bioaccumulation of
PCDD/Fs, PCBs and PBDEs by earthworms in field soils of an E-waste dismantling
area in China. Environ. Int. 54, 50–58.
Shih, S.-I., Lee, W.-J., Lin, L.-F., Huang, J.-Y., Su, J.-W., Chang-Chien, G.-P., 2008. Significance
of biomass open burning on the levels of polychlorinated dibenzo-p-dioxins and di-
benzofurans in the ambient air. J. Hazard. Mater. 153, 276–284.
Shin, E.S., Kim, J., Choi, S.D., Kang, Y.W., Chang, Y.S., 2016. Estimated dietary intake and
risk assessment of polychlorinated dibenzo-p-dioxins and dibenzofurans and
dioxin-like polychlorinated biphenyls from fish consumption in the Korean general
population. Chemosphere 146, 419–425.
Statistics Korea, d. Available at. http://kostat.go.kr, Accessed date: 25 October 2018.
Stockholom convention, 2015. Available at. http://chm.pops.int/, Accessed date: 5 August
2018.
Tsuchita, H., Shirai-Morishita, Y., Shimizu, T., Abe, T., 1997. Effects of a Vespa amino acid
mixture identical to hornet larval saliva on the blood biochemical indices of running
rats. Nutr. Res. 17, 999–1012.
Van den Berg, M., Birnbaum, L., Bosveld, A.T., Brunstrom, B., Cook, P., Feeley, M., et al.,
1998. Toxic equivalency factors (TEFs) for PCBs, PCDDs, PCDFs for humans and wild-
life. Environ. Health Perspect. 106, 775–792.
Van Overmeire, I., Waegeneers, N., Sioen, I., Bilau, M., De Henauw, S., Goeyens, L., et al.,
2009. PCDD/Fs and dioxin-like PCBs in home-produced eggs from Belgium: levels,
contamination sources and health risks. Sci. Total Environ. 407, 4419–4429.
WHO, 2000. Consultation on assessment of the health risk of dioxins; re-evaluation of the
tolerable daily intake (TDI): executive summary. Food Addit. Contam. 17, 223–240.
Wilson, E.O., 1971. The Insect Societies. Harvard University Press.
Xiao, J., Zuo, Y., Liu, Y., Li, J., Hao, Y., Zhou, X., 2007. Effects of Nidus Vespae extract and
chemical fractions on glucosyltransferases, adherence and biofilm formation of Strep-
tococcus mutans. Arch. Oral Biol. 52, 869–875.
Zhou, Y., Yin, G., Asplund, L., Stewart, K., Rantakokko, P., Bignert, A., et al., 2017. Human
exposure to PCDDs and their precursors from heron and tern eggs in the Yangtze
River Delta indicate PCP origin. Environ. Pollut. 225, 184–192.
1039H.-O. Kwon et al. / Science of the Total Environment 654 (2019) 1033–1039
