International Journal of
Environmental Research
and Public Health
Article
Health Risks of Polybrominated Diphenyl Ethers
(PBDEs) and Metals at Informal Electronic Waste
Recycling Sites
Chimere May Ohajinwa 1, *, Peter M. van Bodegom 1 , Oladele Osibanjo 2 , Qing Xie 3 ,
Jingwen Chen 3 , Martina G. Vijver 1 and Willie J. G. M. Peijnenburg 1,4, *
1
2
3
4
*
Institute of Environmental Sciences (CML), Leiden University, P.O. Box 9518,
2300 RA Leiden, The Netherlands; p.m.van.bodegom@cml.leidenuniv.nl (P.M.v.B.);
vijver@cml.leidenuniv.nl (M.G.V.)
Department of Chemistry, University of Ibadan, Ibadan 200284, Nigeria; oosibanjo@yahoo.com
Key Laboratory of Industrial Ecology and Environmental Engineering (Ministry of Education), School of
Environmental Science and Technology, Dalian University of Technology, Dalian 116024, China;
qingxie@dlut.edu.cn (Q.X.); jwchen@dlut.edu.cn (J.C.)
Center for Safety of Substances and Products, National Institute of Public Health and the
Environment (RIVM), P.O. Box 1, 3721 Bilthoven, The Netherlands
Correspondence: chimeremayq@yahoo.co.uk or chimeremay@gmail.com (C.M.O.);
peijnenburg@cml.leidenuniv.nl (W.J.G.M.P.); Tel.: +31-(0)71-527-7434 (C.M.O.)
Received: 21 December 2018; Accepted: 8 March 2019; Published: 13 March 2019
Abstract: Concerns about the adverse public health consequences of informal electronic waste
(e-waste) recycling are increasing. This study adopted a cross-sectional study design to gain insights
into health risks (cancer and non-cancer risks) associated with exposure to e-waste chemicals among
informal e-waste workers via three main routes: Dermal contact, ingestion, and inhalation. The
e-waste chemicals (PBDE and metals) were measured in the dust and top soils at e-waste sites (burning,
dismantling, and repair sites). Adverse health risks were calculated using the EPA model developed
by the Environmental Protection Agency of the United States. The concentrations of the e-waste
chemicals and the health risks at the e-waste sites increased as the intensity of the e-waste recycling
activities increased: control sites < repair sites < dismantling sites < burning sites. Dermal contact
was the main route of exposure while exposure via inhalation was negligible for both carcinogenic
and non-carcinogenic risks. Cumulative health risks via all routes of exposure (inhalation, ingestion,
and dermal contact) exceeded the acceptable limits of both non-cancer effects and cancer risk at all
e-waste sites. This indicates that overall the e-waste workers are at the risk of adverse health effects.
Therefore, the importance of occupational safety programs and management regulations for e-waste
workers cannot be over emphasised.
Keywords: electronic waste; informal recycling; PBDEs; metals; soil; dust
1. Introduction
Information Communication Technology (ICT) has revolutionized our everyday life, consequently
causing an increasing demand for ICT. This growing importance of ICT coupled with rising
obsolescence due to rapid technological advancements, demand for the latest ICT, and decreasing
electrical electronic equipment (EEE) lifetime has led to a rapid increase in the volume of electrical
electronic equipment discarded, which is known as Waste Electrical Electronic Equipment (WEEE, also
known as e-waste) generated around the globe. e-Waste consists of electrical and electronic devices
including all separate components (such as wires, cables, batteries, and circuit boards), which are at
Int. J. Environ. Res. Public Health 2019, 16, 906; doi:10.3390/ijerph16060906
www.mdpi.com/journal/ijerph
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the end of their useful life [1,2]. e-Waste is one of the most complex waste streams because of the
wide variety of components, compositions, and rapidly changing product designs. It is also the fastest
growing municipal waste streams in the world.
The global estimate of e-waste generated in 2014 was 41.8 million metric tons, which increased
to 44.7 million metric tons in 2016, and 52 million metric tons are expected to be generated by
2021 [3]. Of the quantity generated, only about 20% of e-waste generated is properly collected and
recycled. About 80% of the e-waste generated globally is recycled in informal settings in developing
countries such as Nigeria, Ghana, Brazil, Mexico, China, India, Vietnam, and the Philippines [4,5].
The concern with e-waste is not only about the volumes generated but also about the unsafe methods
employed in recycling the electronics in developing countries, known as informal recycling. Informal
e-waste recycling is unregulated, unorganised and often overlooked [6–8]. It perpetuates due to a
lack of infrastructure for sound e-waste management, lax environmental laws/regulations, and weak
enforcement of existing national and international laws/regulations [9–12], such as the implementation
of extended producer responsibility schemes by manufacturers, which is already enforced in developed
countries [2,3]. Informal e-waste recycling involves the use of crude methods such as the undocumented
collection of e-waste from homes, workshops, dumpsites, sorting, manual dismantling, smelting, and
open burning. These activities are carried out without safety precautions. This leads to the release
of hazardous mixture chemicals into the environment. These practices have both environmental
and public health consequences. However, information on the potential cancer and non-cancer risks
associated with informal e-waste recycling is scarcely available in developing countries. Therefore,
abating the public health implications of unsafe e-waste recycling practices could be a challenge
without adequate information.
e-Waste contains a wide range of substances, some of which are economically valuable, and
some are hazardous. Some of the hazardous substances are compounds of potential concern (COPC),
which include metals, products of incomplete combustion (PICs), and/or reformation products. PICs
include any organic compound emitted during incomplete combustion, whereas reformation products
are organic compounds that are formed immediately after combustion, due to the interaction of
specific constituents. Some of the organic compounds are persistent organic pollutants (POPs) such
as brominated flame retardants (BFRs) like Polybrominated Diphenyl Ethers (PBDEs), non-dioxin
like Polychlorinated Biphenyls (PCBs), Polycyclic Aromatic Hydrocarbons (PAHs), Polychlorinated
Dibenzo-p-dioxins, and Furans (PCDD/Fs). These POPs, along with other organic compounds, may
pose significant implications for human health and environmental safety [6,7,13,14].
In this study, we considered PBDEs as a proxy for the cocktail of POPs emitted at informal e-waste
recycling sites. POPs like PBDEs are toxic, highly persistent in the environment, bio-accumulate in
food chains, and they have a high potential for long-range environmental transport. In addition, metals
from e-waste are non-biodegradable, they persist in the environment and can disturb the ecological
balance of the aquatic and the terrestrial environment, as well as affect human health. These chemicals
have been detected in humans and in increasing concentrations in various environmental matrixes,
including air, water, soil, sediment, animals, and foods in all regions of the world [15]. Evidence of
effects of exposure to informal e-waste recycling include injuries [8,16], infection of wounds, skin
and eye injuries and irritations, respiratory problems [17,18], and noise pollution, occupational stress,
among others [19]. There is also evidence on harmful effects of long-term exposure of humans and
wildlife, including effects on fetal/child development, impacts on thyroid and neurologic functions,
immunotoxicity, reproductive toxicity, and endocrine disruption with endpoints related to induction
of cancer [17]: See Table 1 for more information on health effects due to exposure to organic and
metal contaminants.
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Table 1. Evidence of health effects due to long-term exposure to persistent organic contaminants.
Chemical
Effects
Reference
PCDD/Fs
PBDEs
PATHs, PFOA
Cr, Mn, Ni
Pb, Cr, Cd, Ni
PCBs
Mn, Ni, Pb
Pb
As, Cd, Ni, Cr, Hg, Cu
Thyroid function
Thyroid function, Reproductive health, endocrine disruption
Reproductive health
Lung function
Reproductive health
Reproductive health, thyroid function
Growth
Mental health outcomes
Cancer, oxidative stress, DNA damage
[20]
[20–23]
[24,25]
[26]
[27–30]
[20,29]
[26,31,32]
[28,33]
[32,34]
PCDD/Fs: Polychlorinated Dibenzo-p-dioxins, and Furans; PBDEs: Polybrominated Diphenyl Ethers; PATHs:
Polycyclic Aromatic Hydrocarbons; PFOA: perfluorooctanoic acid; PCBs: Polychlorinated Biphenyls.
High concentrations of metals and PBDEs were found at and around informal e-waste recycling
sites [35–40]. Large quantities of e-waste are informally recycled in Nigeria using various recycling
activities such as repair, dismantling, and open burning [41]. Each of these activities may pose a
potential significant source of human exposure to pollutants (toxic metals and organic pollutants).
Human exposure could be through direct inhalation, ingestion, dermal contact, or via consumption
of contaminated food and water. Thus far, to our knowledge, no study has estimated the health
risks associated with informal e-waste recycling. Therefore, there is a need to estimate the health
risks associated with exposure to e-waste chemicals such as metals and PBDEs. The most evident
health-related issues are associated with direct occupational exposure. In addition to these apparent
occupational acute health issues, there might be some unforeseen threatening health issues in the long
run or even after the person has stopped working at e-waste sites. To provide an understanding of the
health risks to which various informal e-waste workers in Nigeria are exposed to, it was hypothesized
that the top soils and dusts samples from different informal e-waste sites may generate different levels
of risks depending on the pollutant concentrations.
Therefore, the objectives of this study were to assess non-cancer and cancer risks that are
attributable to metals and PBDEs in soils and dusts from different e-waste recycling sites. We estimated
the health risks of exposure to metals and PBDEs pollution, as present in top soils (0–10 cm) and various
dust samples (floor dust, and direct dust from electronics). We did this by calculating average daily
doses for workers exposed via inhalation, dermal contact, and oral ingestion. We consider exposure
to PBDEs and metals as a proxy for organic and inorganic chemicals respectively. Informal e-waste
workers are inadvertently exposed to both classes of chemicals at the same time. In this paper we
evaluated17 PBDE congeners: BDE-17, BDE-28, BDE-71, BDE-47, BDE-66, BDE-100, BDE-99, BDE-85,
BDE-154, BDE-138, BDE-183, BDE-190, BDE-208, BDE-206, and BDE-209, as well as 24 metals Ag, As,
Ba, Cd, Cr, Co, Cu, Fe, Ga, Ge, Hg, Mn, Ni, Pb, Se, Sn, Sb, Te, Ti, Ta, V, and Zn, at the various sites.
2. Methods
2.1. Study Locations and Designs
The methods employed in this study have been well detailed in our previous studies [8,16,35,36].
In brief, a cross-sectional study design was adopted to gain an understanding of the pollution levels
at the e-waste recycling sites in the three study locationsin Nigeria: Ibadan, Lagos, and Aba. In each
study location, a multi-stage random systematic sampling technique was used to select the sites. This
was to ensure representative inclusion of various e-waste recycling activities (burning, dismantling,
and repair) in the selected e-waste recycling areas. In Lagos, the selected sites were the Computer
village, Ikeja (6.593◦ N, 3.342◦ E), and Alaba international market Ojor (6.462◦ N, 3.191◦ E). In Ibadan,
the selected sites were Ogunpa (7.383◦ N, 3.887◦ E) and Queens Cinema areas (7.392◦ N, 3.883◦ E). In
Aba, the shopping center(5.105◦ N, 7.369◦ E) and Port-Harcourt Road/Cementary (5.104◦ N, 7.362◦ E)
and Jubilee road/St Michael’s Road (5.122◦ N, 7.379◦ E) were selected (Figure 1). Soil and dust samples
Int. J. Environ. Res. Public Health 2019, 16, 906
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were collected from the selected sites depending on the feasibility of collecting such samples. For
metal analysis, a total of 62 samples were collected from all the sites. The 62 samples consist of 23
top soil (0–10 cm depth), 31 floor dust, three roadside dust, and five direct dust samples collected
from the inside and outside of electronic devices were analyzed. For the PBDE analysis, a total of 56
samples consisting of 16 top soils (0–10 cm), 29 floor dust, 5 roadside dust, and 6 direct dust samples
collected from the inside and outside of electronic devices were analyzed: See Supplementary Figure
S1a,b. The difference in the number of samples analyzed for metals and PBDE is because there was
loss of samples, and some samples were below the detection limits due to strong matrix effects. See the
supplementary information for more details on the methods used for the analysis of metals and PBDEs.
Figure 1. Map of Nigeria showing the study locations.
2.2. Description of Recycling Activities and Likely Exposure Pathways
The recycling activities include collection, sorting, storage, washing, cleaning, dismantling, and
metal recovery through stripping of wires or open burning. Most e-waste recycling activities (especially
at dismantling and burning sites) are carried out outdoors, which involve manual dismantling
(disassembling) using hammer, machetes, or any tool that can help separate the parts. Open burning
leads to incomplete combustion and processed materials from the various e-waste activities are
dumped outside on bare ground (no vegetative cover on the ground). Most repair activities, which
involve soldering of various parts, take place indoors, but also sometimes outdoors, depending on the
settings of the work environment and the weather condition. These activities release large quantities
of hazardous substances without any emission control.
The workers work with minimal or no health or the environmental protection. The majority
(82%) of the workers work without the use of any personal protective equipment (PPE) such as gloves,
nose mask. Also most of them work in shorts, short-sleeved shirts, and slippers, exposing most
parts of their body [8,16]; also see Supplementary Figure S1d–f (photos of e-waste workers at the
sites). This means that they have multiple routes of exposure (directly and indirectly) to the e-waste
chemicals. The exposure routes are via ingestion, inhalation, or dermal contact. Informal e-waste
Int. J. Environ. Res. Public Health 2019, 16, 906
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recycling happens mostly in urban slums, usually with no official governance, regulations, and people
work mainly for economic benefits. Within the e-waste recycling vicinities, there are other (non-e-waste
recycling) informal businesses with workers having similar socio-demographic information like the
e-waste workers. In some locations there are water bodies less than 2 km away from the burning sites.
In addition, most residences use boreholes (ground water) and deep wells as a source of water, as
confirmed by Healya et al., 2017 [41]. Historically, from the responses of the e-waste workers and
residents around the e-waste recycling sites, e-waste recycling activities seem to be the most critical
activity that releases hazardous substances in the vicinity. Due to stricter enforcement of the e-waste
regulations by the National Environmental Standards and Regulations Enforcement Agency (NESREA),
Nigeria, the e-waste dumpsites/burning sites have been moved more than once at Alaba, Lagos. After
a while the new sites were crowded with both old and new in-coming workers (usually migrants
from northern Nigeria in search of greener pasture in the cities). As the migrants settle around the
dumpsites, the sites finally turn into small temporary unplanned residential communities. One major
concern is that current e-waste sites could be used for other activities in the future, which means that
the impact of the emissions from e-waste recycling could go beyond the e-waste workers. We recognize
that children around the e-waste recycling sites may be exposed to e-waste mixture chemicals, but in
this study, we focus on e-waste workers’ exposure to metals and PBDEs that are likely to be emitted
during e-waste recycling.
2.3. Health Risk Assessment
The potential health risks was assessed as the likelihood of adverse health effects resulting from
exposure of e-waste workers to e-waste chemicals (metals and PBDEs) over a specified time period.
The risks are commonly expressed in terms of the exceedance of the average daily dose (ADD). The
ADD is based on the magnitude, frequency, and duration of human exposure to chemicals (PBDEs
and metals in this study) in the environment. Information on the socio-demographic (age, weight,
height) and occupational characteristics were obtained from the e-waste workers, which were used
for the health risk estimates. The health risk of each of the metals, each of the PBDE congeners,
and ∑PBDEs is expressed in terms of either carcinogenic risks or non-carcinogenic health hazards.
Exposure to PBDEs and metals can occur via three main pathways: (a) Direct inhalation of vapor or
of atmospheric particulates through mouth and nose; (b) incidental ingestion of dust and top soils
due to their deposition on food or drinks or via hand-to-mouth activity, and (c) dermal absorption of
substances present in particles adhering to exposed skin [42]. The models used in this study to calculate
the exposure of humans to metals and PBDEs in dust and soil is based on the models developed by the
Environmental Protection Agency of the United States [43–46].
The average daily dose (ADD) (mg/kg/day) of a pollutant in soil and dust taken up via
ingestion, dermal contact, and inhalation, as exposure pathways wereestimated using Equations (1)–(3).
ADDingestion , ADDinhalation , and ADDdermal are the daily amounts of PBDEs and metals taken up
through ingestion, inhalation, and dermal contact (mg/kg/day), respectively. Median concentrations
of the pollutants were used in these calculations. Table 2 presents the sources of the values and factors
used for the health risk estimations and the meanings of the abbreviations.
ADDingestion = C ×
(1)
SA × AF × ABS × EF × ED
× CF
BW × AT
(2)
Cdust × Rinh × ET × EF × ED
× CF
PEF × BW × AT
(3)
ADDdermal = C ×
ADDinhalation =
Ring × EF × ED
× CF
BW × AT
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Table 2. Exposure parameters for adults (e-waste workers) with associated references.
Abbreviations
C (mg/g)
Ring (mg/day)
Rinh (m3 /day)
EF (days/year)
Work days
ED (years)
ET (hours/day)
BW (kg)
AT (days)
Age
SA
(cm2 )
AF (unitless)
ABS (unitless)
PEF (m3 /kg)
CF
Exposure Factors
Exposure Values
Median Concentration of the PBDE or
metals
Ingestion rate
inhalation rate
Exposure frequency
Average work days
Exposure duration
Exposure time in hours/day at work
Average body weight (279 workers)
Shown in Supplementary
Tables S1–S6
30 mg/day
20 m3 /day
313 days/year
6 days/week
24 years
9 h/day
67 kg
[47]
[45]
This study
This study
[45]
This study
This study
24 × 365 days
[45]
70 × 365 days
[45]
29 years
5700 cm2 (most of them do not use
any PPE)
0.2 mg/cm2 .day
0.1 (for semi-volatile compounds)
1.36 × 109 m3 /kg
10−6
available for four PBDE congeners
and 19 metals
–
–
Calculated and shown in
Supplementary Tables S7–S12
–
–
–
This study
Average time (ED × 365 days) for
non-carcinogens)
Average time (70 × 365 days) for
carcinogens
Median age of the workers
Skin surface area
IUR
Skin adherence factor
Dermal absorption factor
Particle emission factor
Conversion factor
reference dose via ingestion, inhalation,
and dermal contact
Reference concentration
Inhalation Unit Risk
ADD (mg/kg/day)
average daily dose
HQ (unitless)
HI
SF
Hazard quotient
Hazard index
Slope factor
RfDi (mg/kg/day)
RfC
(mg/m3 )
References
This study
[48]
[45]
[45]
[45]
[45]
[49]
[49]
[49]
This study
[49]
Cdust : Median Concentration of the PBDE or metals in dust.
Based on the ADDs, and the toxicity risk indices, the health risks for non-cancer hazards and
cancer risks) of the PBDEs and metals were estimated using Equations(4) and (5). The Hazard Quotient
(HQ) is used to calculate the non-carcinogenic risks based on reference daily dose (RfD or reference
concentrations (RfC) [50]. The RfD is the toxicity value used in evaluating the adverse health effects; is
an estimate of the allowable daily exposure to the human population [49]. Values for RfD and RfC were
available only for four PBDEs congeners (BDE-47, BDE-99, BDE-153, and BDE-209), and for 19 metals:
Ag, As, Ba, Cd, Cr, Co, Cu, Fe, Hg, Mn, Ni, Pb, Se, Sn, Sb, Ti, Ta, V, and Zn from USEPA 2011 [48] and
USEPA 2017 [50]. For further estimation of the potential cancer risks, only seven metals (Cr, Co, Ni,
As, Cd, Hg, and Pb) and one PBDE congener (BDE-209) toxicity values available [49]. A HQ value
below one indicates that there is an acceptable level of risk (indicating low probability of any adverse
effect), while HQ values exceeding one are indicative of unacceptable risks (higher than acceptable
probability of an adverse health effect). HQ values exceeding one are assumed to be of concern [50].
The HQ for each of the pollutants (PBDEs and metals) was calculated for ingestion, dermal contact,
and inhalation pathways, respectively.
Thecarcinogenic risk is the probability of an individual developing any type of cancer from the
lifetime exposure to carcinogenic chemicals. The health risk for carcinogen risk characterization is
based on the slope factor (SF) or the Inhalation Unit Risk (IUR). The slope factor (mg kg−1 day−1 )
is used in risk assessment to estimate the lifetime probability of an individual developing cancer
as a result of exposure to a particular carcinogen. A risk above 1 × 10−4 is generally considered
to be unacceptable, a risk below 1 × 10−6 is considered not to trigger any health effect, while risks
calculated to be in between 1 × 10−4 and 1 × 10−6 are within the acceptable limits. A risk of 1 ×10−6
Int. J. Environ. Res. Public Health 2019, 16, 906
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is interpreted as indicating that an individual has a one in 1,000,000 chance of developing cancer from
the exposure evaluated by [51–53].
Oral Hazard Quotient (HQing ) = ADD/RfD
Inhalation Hazard Quotient (HQinh ) = ADD/RfC
Dermal Hazard Quotient (HQder ) = ADD/(RfD × GIABS)
(4)
Carcinogenic risking = ADDing × SF
Carcinogenic riskinh = ADDinh × IUR
Carcinogenic riskder = ADDder × (SF × GIABS)
(5)
GIABS is the gastrointestinal absorption factor which was assumed to be equal to one (assuming
the total absorption of contaminants for all congeners) [48].
In addition, the Hazard Index (HI) is used to assess the potential of exposure to multiple chemicals
or multiple exposure routes at the sites to cause non-carcinogenic effects through different pathways.
The hazard index is equal to the sum of the HQ values for the individual chemicals. Since the workers
are exposed to multiple substances (both metals and PBDEs) within individual exposure pathways at
the same time, we estimated the total non-cancer hazard by summing up the HIs of metals and PBDEs
for each of the exposure routes [49]. We assume there are no interactions between PBDEs and metals.
2.4. Ethical Considerations
Ethical approval was obtained from the University of Ibadan/University College Hospital Ethical
Review Board (No. UI/EC/15/0096). Verbal and written consent of the workers was obtained at the
start of the interview, after explaining to the workers their full rights to refuse and to withdraw at
any time during the interview. To ensure that the participant remains anonymous each questionnaire
was coded with number identifiers. They were also assured that the data will not be used for other
purposes than for scientific reasons and for the development of safety promotion programs for the
sector. Permission to conduct the study was also obtained from the association of second-hand
electronics dealers at each study site. This study is a part of a bigger study.
3. Results
3.1. Descriptive Statistics of the PBDE and Metals
In the Supplementary Tables S1–S6, a summary of the medians of the various PBDE and metal
concentrations in soil and in dust samples at the various e-waste recycling sites is shown for each of
the three study locations. The general pattern of the PBDEs and metal distribution in top soil and dust
samples from the sites showed concentrations in this increasing order: Control sites < repair sites <
dismantling sites < burning sites. The concentrations of most of the PBDE and metals congeners at the
e-waste sites in the three locations exceeded the concentrations at the corresponding control sites.
3.2. Human Health Risk Assessment
3.2.1. Quantitative Estimation of Non-Carcinogenic Effects
The HI values for dermal exposure to metals and PBDEs combined, via soil and dust were greater
than one at all e-waste recycling sites (burning, dismantling, and repair sites), with metals contributing
the great majority of the risk.. This indicates that the concentrations at those sites exceeded the
threshold (safe) limit and the workers are at risk of developing non-cancer health effects via dermal
exposure, followed by ingestion of soil and dusts at the sites. In contrast, the non-carcinogenic risks via
inhalation were negligible. Dermal contact was shown to be the main route of exposure to both metals
and PBDEs and consequently poses a higher risk. Generally for the fourPBDEs, BDE-209 contributed
most to the health risk, followed by BDE-99 in Lagos and Ibadan, while Aba BDE-99 contributed
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the most, followed by BDE-153. Figures 2 and 3 present the hazard index (HI) of top soils and dust
for non-cancer risks via all exposure pathways at the e-waste sites for the three locations for PBDEs
and metals, respectively. See Supplementary Tables S13–S15 and Tables S16–S19 for more details,
Supplementary Table S20 shows the RfD, RfC, and GIABS used for the estimates.
Figure 2. Hazard index (HI) for non-cancer risk via ingestion and dermal contact of Polybrominated
Diphenyl Ethers (PBDEs) in soil and dust at various e-waste sites in three locations.
Figure 3. Hazard index (HI) for non-cancer risk of metal exposure via ingestion, inhalation, and dermal
contact of soil and dust at various e-waste sites in the three locations, showing that e-waste workers are
prone to non-cancer risks via dermal contact with metals in soils and dust, also via the ingestion of top
soils at burning sites in Lagos.
Combining the HIs for non-cancer risks of metals and PBDEs also revealed that the total HI
exceeded the acceptable (safe) limit for non-cancer hazards via dermal exposure at all sites in all
locations, and via ingestion of direct dust at repair sites in Ibadan and ingestion of top soils at burning
sites in Lagos (Figure 4 and Supplementary Table S17). The total HI is mainly influenced by the HI of
metals. We also considered the cumulative non-cancer effects by summing the risks from all exposure
routes. The cumulative non-cancer effects exceeded the accepatable limit at all sites in all locations, see
Figure 5.
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Figure 4. Total Hazard index (HI) for non-cancer risk via each exposure route of metal and
Polybrominated Diphenyl Ethers (PBDEs) in soil and dust at various e-waste sites in the three locations.
Figure 5. Cumulative Hazard index (HI) of all exposure routes for non-cancer risk of metal and PBDEs
in soil and dust at various e-waste sites in the three locations.
3.2.2. Quantitative Estimation of Risk of Developing Cancers
The cancer risk for BDE-209 via ingestion is within the range of 2.3 × 10−13 to 4.72 × 10−9 , and for
dermal uptake is between 3.2 × 10−10 to 6.6 ×10−6 . This indicates that the risks of developing cancer
−
−
via dermal contact, since the ranges are above the safe limit of 1 × 10−6 especially at the burning sites;
−
−
see Figure 6 and Supplementary Tables S21–S23 for more details. These findings indicate that exposure
−
of e-waste workers to PBDEs is potentially harmful to their health.
−
−
Only seven metals (Cr, Co, Ni,− As, Cd, Hg,− and Pb) had toxicity values available forthe estimation
of potential cancer risks via ingestion, inhalation, and dermal contact.
The HI for cancer risk through
−
metals via ingestion ranged from 8.7 × 10−6 to 1.5 × 10−4 , via the inhalation it ranged from 9.1 × 10−15
to 1.5 × 10−14 , andvia dermal contact it ranged from 7.0 × 10−4 to 1.2 × 10−1 , see Figure 7. For more
−
−
details on the results for each of the locations, see Supplementary Tables S24–S26. These results show
−
−
−
−
that exposure via inhalation induces risks that are below the acceptable (safe) limit, while exposure
via ingestion and dermal contact induces risks that exceeded
the acceptable
(safe) limits at all sites in
−
−
all locations.
These
findings
indicate
that
the
workers
are
most
at
risk
of
adverse
−
−
−
−non-cancer health
effects via dermal contact, followed by ingestion, while exposure via inhalation induces negligible
risks; dermal > ingestion > inhalation routes. Burning sites seem to be the most unsafe sites followed
by dismantling and repair sites. These findings indicate that exposure of e-waste workers to metals is
harmful to their health.
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Figure 6. Hazard index (HI) for cancer risk via ingestion and dermal contact of Polybrominated
Diphenyl Ethers (PBDEs) soil and dust at various e-waste sites in the three locations.
Figure 7. Hazard index (HI) for cancer risk via ingestion and dermal contact of metals in soil and dust
at various e-waste sites in the three locations.
Since the workers are exposed to multiple substances (both metals and PBDEs) at the same time
within individual exposure pathway, we estimated the total cancer risk by summing up the HIs of
metals and PBDEs for each of the exposure routes. The total HI is mostly influenced by the HI of metals.
The total HI shows that the exposure via ingestion and dermal contact of metals and PBDEs exceeded
the acceptable (safe) limit for cancer risks at all sites in all locations (Figure 8 and Supplementary
Table S27). We also considered it appropriate to sum risks from multiple exposure routes (i.e the
cumulative risk of exposure) (See Reference [49], Exhibit 8–1 to 8–3). Obviously, the cumulative cancer
risk also exceeded the acceptable (safe) limit at all sites in all locations, see Figure 9 and Supplementary
Table S28.
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Figure 8. Hazard index (HI) for cancer risk via each exposure route of metal and Polybrominated
Diphenyl Ethers (PBDEs) in soil and dust at various e-waste sites in the three locations.
Figure 9. Cumulative Hazard index (HI) of all exposure routes for cancer risk of metal and
Polybrominated Diphenyl Ethers (PBDEs) in soil and dust at various e-waste sites in the three locations.
4. Discussion
As far as we are aware, this is one of the few studies that estimated the cancer risks and non-cancer
hazards of exposure to PBDEs and metals in soil and dust samples from different informal e-waste
activity sites (burning, dismantling, and repair sites). The strength of this study is that we considered
three exposure pathways, different e-waste recycling activities, various environmental samples (top
soils and dusts) from different types of e-waste recycling and compared exposure in three different
cities in two different geopolitical zones in Nigeria. We estimated non-cancer effects, cancer risks,
and the assessed the cumulative effect of exposure to both PBDEs and metals via all exposure routes.
We also used some primary data on exposure parameters obtained from the respondents for the risk
estimation, instead of using default US EPA exposure parameters, which are commonly used in other
studies. In addition, we used epidemiological methods to select the target groups and sites to ensure
that the results obtained are a representative of the target groups and sites, and that the findings are
applicable to similar situations anywhere in the world. Focus on the three types of informal e-waste
recycling activities provided a comprehensive insight on the health risks for different groups of e-waste
workers. Workers are exposed to far more chemicals than the ones considered here. Therefore, this
study can be considered as being indicative of the risks due to both organic and inorganic chemicals.
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One limitation to this study is that there was no air sampling, which would have revealed deeper
understanding on the exposure level via inhalation.
The findings of this study as performed in Nigeria are likely to be representative for informal
e-waste recycling in developing countries that lack the resources for safe e-waste recycling. Increasing
amounts of electronic waste, unsafe recycling methods and disposal pose significant risks to the
environment and human health, therefore hindering sustained health. Understanding the implications
of scientific data related to informal e-waste recycling contributes towards the achievement of
Sustainable Development Goals (SDGs) related to environmental protection (Goals 6, 11, 12, and
14), health (Goal 3), and Goal 8 that focuses on employment and economic growth [54].
4.1. Health Risk Assessments
The concentrations of the PBDEs and metals considered in this study showed overall an increasing
trend of health risks at the sites as the intensity of the e-waste activities increased in this order: Control
sites < repair sites < dimantling sites < burning sites. This is similar to the findings of many studies
reviewed by Ni et al., 2013 [55]. This finding reveals that open burning of e-waste is the most risky
recycling activity. The risks associated with the high levels of e-waste chemicals and poor work
practices call for concern.
The health risk assessment shows the impact of the different metals and PBDE congeners via
viarious routes (ingestion, inhalation, and dermal contact). Overall, the magnitude of exposure to
non-cancer effects and cancer risks of PBDEs via the various routes is in this order: Dermal contact,
followed by ingestion of soil and dust at all the sites (burning, dismantling, and repair sites). The same
pattern of exposure risks are revealed for metal exposure: Dermal contact, followed by ingestion, while
exposure via inhalation is negligble (dermal contact > ingestion > inhalation). This finding is consistent
with a similar study on e-waste sites reported by Civan and Kara 2016 [56] and review studies by Song
et al., 2015 [57]. The health risk for the metals were much more pronouced than those for PBDEs.
The cumulative hazard index of PBDEs and metals via all exposure routes at all the e-waste sites
exceeded the acceptable (safe) limits by several orders of magnitude. Considering the exposure via the
different routes to both PBDEs and metals, the total risks calculated show that exposure via dermal
contact exceeds the acceptable limit for non-cancer effects in all locations at all sites with the burning
sites having the highest risks. Similarly, the total risks for ingestion and dermal contact exceeded the
acceptable limits for cancer risks in all locations at all sites with the burning sites having the highest
risks. For both non-cancer effects and cancer risks, dermal exposure is the main route of exposure.
In addition, the cumulative health risks via all routes of exposure (inhalation, ingestion, and dermal
contact) exceeded the acceptable limits of both non-cancer effects and cancer risk at all e-waste sites
and in all locations.
4.2. Implications for Health Risks
The risk assessment indicates that overall the e-waste workers are at the risk of adverse health
effects. Therefore, the occupational safety program for the e-waste workers, especially the use of
personal protective equipment (PPE), cannot be over emphasised. PPE such asappropriate work cloths,
as most of their body parts are exposed (see Supplementary Figure S1d–f). The majority (82%) of the
e-waste workers do not use any PPE, and one the reasons for not using PPE is discomfort. The workers
complained about the discomfort of using PPE at work, e.g., the gloves and thick coveralls because it
hinders productivity; with the gloves feel hot after some time and is difficult to pick up tiny screws,
and the coveralls are not convenient for the weather (hot and humid) in the tropics. This observation is
in accordance with a study on preferred product characteristics for PPE in tropical climates by World
Health Organization (WHO), in which the need for comfort is necessary for the increased use of PPE
and safety. In addition, a study by de Almeida et al., 2012 [58] highlighted the need for thermal comfort
of PPE to increase PPE usage by workers. The primary purpose of PPE is to prevent injury, but comfort
is also important because it can dramatically influence whether workers actually make proper use of it.
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Exposure of e-waste workers to PBDEs, metals, and other hazardous substances is even worse,
because, surprisingly, 88% of the workers are unaware that e-waste contains hazardous chemicals, and
70% do not think that the chemicals in e-waste can pose any health risk. In the study by Ohajinwa et al.,
2017a [8], the workers had a low health risk awareness level. This shows that informal workers often
appear to underestimate or deny the health risks associated with their jobs. This could be because
this job is a means of livelihood for them and they cannot escape from the risks easily. This is in
accordance with the theory of Cognitive Dissonance proposed by Festinger in 1957 in which he stated
that recognition of inconsistency will cause dissonance, and will motivate an individual to resolve the
dissonance by either change of beliefs, change of actions, or change of perception of action [59].
Ohajinwa et al., 2017 also reported a positive correlation between workers’ knowledge and
work practice. Therefore, improving e-waste workers’ knowledge on the health risks associated with
their daily jobs may decrease risky practices [8]. It is crucial that e-waste workers are educated on
the potential health risks peculiar to their jobs and the safety measures to be undertaken. It is also
important to note that non-e-waste workers, residents, and children around the e-waste sites are very
likely to also be at risk of adverse health effects from informal e-waste recycling as also pointed out by
References [15,56,57,60]. The other informal non-e-waste workers around the e-waste recycling vicinity
have similar socio-demographics and work conditions [61], hence they are likely to be exposed to
similar health risks like the e-waste workers. The high metal and PBDE concentrations at the e-waste
sites may also be an indirect source of pollution of surface and ground water and air, and could
consequently affect people farther away from the e-waste sites. It should therefore be noted explicitly
that the actual health risks would be higher than the risks calculated in this study. This indicates an
urgent need for more appropriate and effective policies, regulations, and strategies for enforcement
actions suitable for the informal sector.
We recommend:
•
•
•
•
•
That government and other formal institutions design effective occupational health and safety
(OSH) programs for the informal e-waste workers.
The enforcement of the policies and regulations. One effective way to enforce safety is for formal
institutions to work with the informal e-waste recycling associations to identify comfortable
PPE, and to communicate the health risks peculiar to informal e-waste recycling and the safety
measures to be undertaken. However, to effectively implement any OSH program in this sector, it
should be borne in mind that the approach must be situation specific. The approach may differ
depending on the type of job performed and location. In addition, enforcement agencies must not
be seen to be at cross-purposes with the informal e-waste sector, as it frequently appears because
informal associations have proved to operate efficiently without any formal support.
The ban of open burning of e-waste and other risky practices. If open burning of e-waste is
not banned, the effects will consequently affect those living far away from the recycling sites
through pollution of soil, air, underground water, and contamination of plants and foods. These
contaminants might even affect the unborn generation. One way to ensure such a ban is to
(a) devise appropriate alternative ways of e-waste recycling with caution to protect health and
environment, (b) bridge the communication gap between enforcement agencies and informal
e-waste workers, and (c) for the informal e-waste recycling associations to be made accountable
for safer practices.
More studies on air monitoring of the e-waste recycling sites, especially at the burning sites as fine
particles would not have been captured in the samples analyzed for this study. Air monitoring of
the site might reveal exposure via inhalation as a significant route of exposure.
The use of the hierarchical control method in the informal e-waste recycling sector(Figure 10).
Such controls are simple steps that will help to minimize exposure and health risks associated
with informal e-waste recycling, without impeding the workers’ source of livelihood. This will
not only protect the e-waste workers, but also protect people around the e-waste recycing sites.
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In our assessment, we assumed that there are no interactions of chemicals that increase toxic effects
to humans. Moreover, it is known that the toxicity of the chemicals also depends on other parameters
such as exposure time, dose, age, oxidation state, solubility, and properties of the environment among
others [62]. To address these uncertainties, we recommend further studies on biomonitoring of
informal e-waste workers. In addition, we could not assess exposure via inhalation of dust samples at
burning sites. Using respirable particles (dust samples) at burning sites is needed in future studies. We
recommend further toxicological studies to determine the cumulative toxicological effect associated
with exposure to multiple chemicals through different exposure pathways, because the additive
response method applied in this study might underestimate the potential for health effects. We also
recognize that we did not identify all compounds present in the emissions at the e-waste recycling
sites, including those in the new list of one of the most used intenational referencestandard guideline
values (SGVs) for environmental pollutants [63].
Figure 10. Hierachical control at the informal e-waste recycling sites; modified from OSHA 2016, [64].
5. Conclusions
Our study is one of few studies thatestimate the total non-cancer effects and cancer risksof e-waste
chemicals (organic and inorganic) that e-waste workers and people around the e-waste recycling
vicinity may be exposed to. The e-waste workers are prone to both adverse non-carcinogenic and
carcinogenic health risks. The magnitude of exposure showed that dermal contact is the most important
exposure route, followed by ingestion, while exposure via inhalation is the least important exposure
route. This is even more worrisome as previous studies revealed that e-waste workers have poor work
practices and low awareness of the health risks associated with their work. These sobering findings
call for the need for urgent action by both national and international govenments. There is a need
for more appropriate e-waste management regulations that consider maximum participation of the
informal e-waste workers to ensure a moresustainable improvement and development in this sector.
Supplementary Materials: The following are available online at http://www.mdpi.com/1660-4601/16/6/906/s1,
Table S1: Median PBDE concentrations (ng/kg) and Exeedance of soil and dusts across various e-waste sites in
Lagos, Table S2: Median metals concentrations (mg/kg) and Exeedance of soil and dusts across various e-waste
sites in Lagos, Table S3: Median PBDE concentrations (ng/kg) and Exeedance of soil and dusts across various
Int. J. Environ. Res. Public Health 2019, 16, 906
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e-waste sites in Ibadan, Table S4: Median metal concentrations (mg/kg) and Exeedance of soil and dusts across
various e-waste sites in Ibadan, Table S5: Median PBDE concentrations (ng/kg) and Exceedance of soil and dusts
across various e-waste sites in Aba, Table S6: Median metals concentrations (mg/kg) and Exceedance of soil and
dusts across various e-waste sites in Aba, Table S7: PBDEs: Estimation of Average Daily dose (ADD) via ingestion,
inhalation, and dermal uptake via soil and dust at various e-waste in Lagos; Table S8: PBDEs: Estimation of
Average Daily dose (ADD) via ingestion, inhalation, and dermal uptake via soil and dust at various e-waste sites
and in Ibadan; Table S9: PBDEs: Estimation of Average Daily dose (ADD) via ingestion, inhalation, and dermal
uptake via soil and dust at various e-waste sites and in Aba, Table S10: Metal: Estimation of Average Daily dose
(ADD) via ingestion, inhalation, and dermal uptake via soil and dust at various e-waste sites and in Lagos, Table
S11: Metal: Average Daily dose (ADD) via ingestion, inhalation, and dermal uptake via soil and dust at various
e-waste sites and in Ibadan; Table S12: Metal: Average Daily dose (ADD) via ingestion, inhalation, and dermal
uptake via soil and dust at various e-waste sites and in Aba, Table S13: Hazard Quotient (HQ) via ingestion,
inhalation, and dermal uptake via soil and dust at various e-waste sites and in Lagos, Table S14: Hazard Quotient
(HQ) via ingestion, inhalation, dermal uptake via soil and dust at various e-waste sites and in Ibadan, Table S15:
Hazard Quotient (HQ) via ingestion, inhalation, dermal uptake via soil and dust at various e-waste sites and in
Aba, Table S16: Oral Reference Dose (RfD), Inhalation Reference dose(RfC), gastrointestinal absorption factor
(GIABS) for metals, Table S17: Total HI Estimate for PBDEs and Metals for non-cancer Effects (log transformed
data), Table S18: Hazard Quotient (HQ) ingestion, inhalation, dermal in soil and dust at various e-waste sites and
in Lagos, Table S19: Hazard Quotient (HQ) ingestion, inhalation, dermal in soil and dust at various e-waste sites
in Ibadan, Table S20: Hazard Quotient (HQ) ingestion, inhalation, dermal in soil and dust at various e-waste sites
and in Aba, Table S21: Cancer risk of BDE-209 through ingestion, inhalation, dermal in soil and dust at various
e-waste sites and in Lagos, Table S22: Cancer risk of BDE-209 through ingestion, inhalation, dermal in soil and
dust at various e-waste In Ibadan, Table S23: Cancer risk of BDE-209 through ingestion, inhalation, dermal in
soil and dust at various e-waste sites and in Aba, Table S24: Cancer risk of metals through ingestion, inhalation,
dermal in soil and dust at various e-waste sites and in Lagos, Table S25: Cancer risk of metals through ingestion,
inhalation, dermal in soil and dust at various e-waste sites and in Ibadan, Table S26: Cancer risk of metals through
ingestion, inhalation, dermal in soil and dust at various e-waste sites and in Aba, Table S27: Total HI Estimate for
PBDEs and Metals for Cancer Risks (log transformed data), Table S28: Cumulative HI Estimate for PBDEs and
Metals for non-cancer effects and Cancer Risks (log transformed data); Figure S1: D–F: Photos of e-waste workers
at the e-waste recycling sites showing no use of PPE.
Author Contributions: This study is part of the Ph.D. research of C.M.O. C.M.O conceived the study, carried out
the literature review, developed the data collection and analyses plan, carried out data collection, sample collection
and preparation, analysed metals in the samples, analysed the data, drafted the manuscript and provided critical
revision to the manuscript. W.P., P.M.B., O.O.O. and M.V. are the supervisors and were involved in data collection
plan and revision of the manuscript. PMB was also involved in all stages of the write-up and critical revision of the
manuscript, contributed to the manuscript and data analyses. O.O.O. also contributed to the sample preparations
for PBDEs analysis. Q.X. and J.C. wrote the method for PBDE analysis and carried out the laboratory analysis of
PBDEs in China.
Funding: This research was funded by NUFFIC (Netherlands Universities Foundation for International
Cooperation).
Acknowledgments: Data for this paper was obtained within a research project supported by the Netherlands
Fellowship Program of NUFFIC (Netherlands Universities Foundation for International Cooperation), research
grant CF9420/2014 NFP-PhD.14/37. The authors acknowledge the various associations of second-hand electronics
dealers, the scrap dealer associations in each location for their cooperation and for allowing the soil and dust
samples to be collected from the work sites, the research assistants for helping with sample collection.
Conflicts of Interest: There is no conflict of interest. The founding sponsors had no role in the design of the study;
in the collection, analyses, or interpretation of data; in the writing of the manuscript, and in the decision to publish
the results”.
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