Rev Environ Health 2021; aop
Review Article
Ibrahim Issah*, John Arko-Mensah, Thomas P. Agyekum, Duah Dwomoh and Julius N. Fobil
Electronic waste exposure and DNA damage: a
systematic review and meta-analysis
https://doi.org/10.1515/reveh-2021-0074 comet assay biomarkers, 8-hydroxy-2′-deoxyguanosine
Received June 3, 2021; accepted October 17, 2021; (8-OHdG), telomere length, apoptosis rate were reported
published online October 29, 2021 using narrative synthesis.
Results: A total of 20 publications were included in this
Abstract
review, ofwhich seven studieswerewithin the occupational
Objectives: Inappropriate processing and disposal of setting, and the remaining 13 studies were ecological
electronic waste (e-waste) expose workers and surround- studies. The review found six biomarkers of DNA damage
ing populations to hazardous chemicals, including clas- (micronuclei, comets assay parameters (tail length, %
togens and aneugens. Recently, considerable literature tail DNA, tail moment, and olive tail moment), 8-OHdG,
has grown around e-waste recycling, associated chemical telomere length, apoptosis rate and chromosomal aberra-
exposures and intermediate health outcomes, including tions) which were assessed using seven different biological
DNA damage. Micronuclei (MN) frequency has beenwidely matrices (buccal cells, blood, umbilical cord blood,
used as a biomarker to investigate DNA damage in human placenta, urine and semen). Most studies showed elevated
populations exposed to genotoxic agents. We conducted a levels of DNA damage biomarkers among e-waste exposed
systematic review of published studies to assess DNA populations than in control populations. The most
damage in e-waste-exposed populations and performed a commonly used biomarkers were micronuclei frequency
meta-analysis to evaluate the association between e-waste (n=9) in peripheral blood lymphocytes or buccal cells and
exposure and DNA damage. 8-OHdG (n=7) in urine. The results of the meta-analysis
Methods: This systematic review with meta-analysis was showed that electronic waste recycling has contributed
conducted following the Preferred Reporting Items for to an increased risk of DNA damage measured using MN
Systematic Reviews and Meta-Analysis (PRISMA) state- frequency with a pooled estimate of the standardized mean
ment checklist. Articles published in English from January difference (SMD) of 2.30 (95% CI: 1.36, 3.24, p<0.001) based
2000 through December 2020 investigating the associa- on 865 participants.
tions between e-waste exposure and DNA damage were Conclusions: Taken together, evidence from this systematic
retrieved from the following three major databases: MED- review with meta-analysis suggest that occupational and
LINE, ProQuest, and Scopus. Studies that reported the use non-occupational exposure to e-waste processing is associ-
of MN assay as a biomarker of DNA damage were included ated with increased risk of DNA damage measured through
for meta-analysis. Studies that also reported other DNA MN assay and other types of DNA damage biomarkers.
damage biomarkers such as chromosomal aberrations, However, more studies from other developing countries in
Africa, Latin America, and South Asia are needed to confirm
and increase these results’ generalizability.
*Corresponding author: Ibrahim Issah, Department of Biological,
Environmental and Occupational Health Sciences, School of Public Keywords: biomarker; e-waste; genetic damage;
Health, University of Ghana, Legon-Accra, Ghana, micronucleus.
E-mail: ibrahimissah111@gmail.com
John Arko-Mensah, Thomas P. Agyekum and Julius N. Fobil,
Department of Biological, Environmental and Occupational Health
Sciences, School of Public Health, University of Ghana, Legon-Accra, Introduction
Ghana, E-mail: papaarko@yahoo.com (J. Arko-Mensah),
thomaspagyekum@gmail.com (T.P. Agyekum), jfobil@gmail.com The techniques used in the informal recycling of e-waste,
(J.N. Fobil). https://orcid.org/0000-0001-5498-5958 (T.P. Agyekum)
Duah Dwomoh, particularly in lower- and middle-income countriesDepartment of Biostatistics, School of Public Health,
University of Ghana, Legon-Accra, Ghana, (LMICs), are basic and primitive, with little or no regard for
E-mail: duahdwomoh@yahoo.com the health and safety of humans and the environment [1].
Open Access. © 2021 Ibrahim Issah et al., published by De Gruyter. This work is licensed under the Creative Commons Attribution 4.0
International License.
2 Issah et al.: E-waste and DNA damage
Recyclers often use basic tools such as a hammer, chisel Methods
and occasionally screwdrivers and spanners to dismantle
and separate the different components [2] and a longmetal This systematic review/meta-analysis was conducted
rod to rotate/flip burning items such as insulated wires and following the Preferred Reporting Items for Systematic
circuit boards of various sizes [3, 4]. These primitive recy- ReviewsandMeta-Analysis (PRISMA) statement checklist [17].
cling methods release multiple toxic pollutants into the
environment that exposes recyclers and surrounding
populations. Protocol and registration
Some of the chemicals released into the environment
during informal e-waste recycling, such as heavy metals A review protocol was developed and registered with the
and PAHs, are carcinogens [5]. Recent evidence from International prospective register of systematic reviews
developing countries suggests a higher concentration of (PROSPERO) with registration number CRD42020201149,
metals and organic compounds in e-waste recycling sites, and it is available from https://www.crd.york.ac.uk/
among e-waste workers and in people living near e-waste prospero/display_record.php?RecordID=201149.
sites than in the general population [6]. In addition, a
number of researchers have reported that high concen-
trations of heavy metals and organic pollutants from Eligibility criteria
e-waste recycling sites are associated with increased
cancer risks [1, 7–9]. This review focused on observational studies on human
Occupational and environmental exposure to geno- populations exposed to e-waste recycling. We included
toxic agents mainly through inhalation, ingestion, and studies that were original peer-reviewed publications,
dermal contact may damage DNA in a cell, which may be assessed e-waste exposure and biomarkers of DNA dam-
linked to the development of diseases [10–12]. Although age, and involved human populations, including women
studies have reported evidence of an association between and children. We excluded studies that were not original
crude e-waste disposal and DNA damage [13], to the best of (e.g., reviews, conference proceedings, letters to the editor,
our knowledge, there has not been any systematic syn- and abstracts) and did not report biomarkers of DNA
thesis of evidence linking specifically e-waste exposure to damage in human populations.
DNA damage in human populations as yet.
Recently, considerable literature has grown around
e-waste recycling, associated chemical exposures and Information sources and search strategy
intermediate health outcomes, including DNA damage
and cytogenetic alterations [14–16]. The use of biomarkers Articles published in English from January 2000, inves-
such as chromosomal aberrations (CA), micronuclei (MN) tigating the associations between e-waste exposure and
frequency, and comet assay parameters (tail length, tail biomarkers of DNA damage were retrieved through the
moment, etc.), which indicate biomarkers of early bio- following three major databases: MEDLINE (Academic
logical effects, may enable researchers to understand the Search Complete, CINAHL Complete, Education Research
mechanisms or pathways through which e-waste-related Complete, GreenFILE, Health Source: Nursing/Academic
chemicals influence their toxicity. In addition, these bio- Edition, Library, Information Science & Technology
markers may serve as targets for developing efficient Abstracts), ProQuest, and Scopus. The search terms
prevention strategies for workers and people living near used included the following keywords: (“electronic
e-waste sites with uncontrolled exposures and strengthen waste” OR “e-waste” OR “WEEE”) AND (“DNA damage”
regulation involving the safe disposal of e-waste in OR “chromosomal aberration” OR “DNA strand breaks”
general. OR “micronucl*” OR “Sister chromatid exchanges” OR
This systematic review was conducted to assess the “oxidative DNA damage” OR “genotox*” OR “oxidative
evidence of genetic alteration associated with e-waste stress”). Reference lists of selected articles were hand-
recycling as a penultimate step to analyzing DNA methyl- searched for relevant publications that were not captured
ation of long interspersed nucleotide element-1 (LINE-1) as by the electronic search. The search strategy and results of
a proxy for global DNA methylation among informal the various databases are presented in (Supplementary
e-waste recyclers. Table 1).
Issah et al.: E-waste and DNA damage 3
Study selection stage. After the title and abstract screening, a total of 685
articles were excluded, allowing 32 articles to advance to
The study selection was conducted in 2 phases. In phase 1, the full-text screening stage.
two reviewers independently screened titles and abstracts Out of the 32 full-text articles screened, 12 were
of publications retrieved from the electronic databases and excluded either because theywere not original articles (5),
hand searches. Publications that did notmeet the inclusion did not meet the inclusion criteria (3), were retracted
criteria were excluded. After phase 1 screening, 32 publi- articles (1) or shared the same population and outcome
cations advanced to phase 2 (see supplementary material), with another study already included (3) (Supplementary
full-text screening. In phase 2, the same reviewers inde- Table 2). A total of 20 publications were included in this
pendently examined the full-text publications for inclu- review, of which seven studies were within the occupa-
sion. Any discrepancies between reviewers were resolved tional setting, and the rest were ecological studies. Seven
by a third reviewer. Studies that were excluded at this stage of the 20 studies included in this systematic review were
are presented in Supplementary Table 2 with reasons. included in the meta-analysis.
Finally, a total of 20 publicationsmet the inclusion criteria.
Data extraction
Diagrammatic representation of study selection
The type of data extracted from each of the selected studies
The flowchart representing the process of study selection is was both qualitative and quantitative. The qualitative data
presented in Figure 1. In the initial search of three elec- include author and year of publication, details of study
tronic databases, a total of 822 articles were retrieved. design (exposure setting and population), the country
Duplicates of 106 were identified and removed, with a total where the study was conducted, and methods details
of 717 articles making it to the title and abstract screening (samples type, targeted chemicals, outcome measures).
Figure 1: PRISMA flow chart illustrating the
process of selecting the studies included in
the review.
4 Issah et al.: E-waste and DNA damage
The quantitative data extracted included the sample size between-study variability owing to differences in study
for each study, and the main findings expressed as means designs and interlaboratory reproducibility. The REML
and standard deviations if applicable (Table 2). Data assumes a normal distribution of the random study effect
extraction was performed by two reviewers. One reviewer sizes [22]. Forest plots were used to present the results of
extracted the data, and the second reviewer compared the the meta-analysis.
extracted data with the original report. To further explore heterogeneity between studies,
subgroup analyses were performed based on study setting,
i.e., whether studies were conducted among e-waste
Risk of bias (quality) assessment workers vs. non-e-waste workers (occupational) or studies
were conducted among residents of an e-waste exposed
The risk of bias (methodological quality) of each included town/village vs. residents in a neighbouring town/village
study was assessed using the modified version of the without e-waste exposure (ecological), and quality, (high
Newcastle-Ottawa Scale (NOS) for cross-sectional studies quality vs. low quality) as determined by the NOS for cross-
developed by Elyasi et al. [18] to ensure that the conclu- sectional studies. All statistical analyses were conducted
sions and findings of the reviews were based on the best using Stata version 16.1 (StataCorp LLC, College Station,
available evidence. The tool was adjusted to include TX, USA).
exposure assessment and a comparison group.
The score for each cross-sectional studywas calculated
based on four categories: group selection (three items), Results and discussion
comparability (two items), exposure measurement (one
item), and outcome measurement (one item). The items in Study characteristics
the first two categories, ’group selection’ and ’compara-
bility’, were awarded a maximum of two stars and one star
Design and site
for items in the remaining categories. The NOS score
ranged from 0 (lowest grade) to 10 (highest grade). Studies
All 20 studies included in this review were cross-sectional
that scored above themedianwere considered high quality
studies. The majority of the studies (15 of 20) were con-
[19], that is, >5 in this review. Two reviewers carried out the
ducted in China, and the remaining five studies were
risk of bias assessment. Any disagreementswere addressed
conducted in Nigeria [14], Palestine [23], Thailand [16],
by discussion between the two reviewers or by the inter-
Vietnam [15], and the Philippines [24].
vention of a third independent reviewer.
Populations studied
Statistical analysis
A total of seven out of the 20 studies included in the review
The effect size was calculated using standardized mean were conducted in occupational settings; the remaining 13
differences (SMD) since the studies were conducted in studies targeted people resident in e-waste exposed towns
different settings (ecological or occupational). Heteroge- (ecological studies). Only four of the ecological studies tar-
neity was determined using Cochran’s χ2 test and quanti- geted children [15, 25] and neonates [26, 27]; the remaining
fied using the I2 test. The null hypothesis for heterogeneity nine studies involved adult populations. A total of 17 of the
was that all studies share a common mean difference for 20 studies included a comparator group. The comparator
MN frequency. The I2 describes the percentage of differ- groups were mostly residents of non-e-waste recycling
ences across studies attributed to heterogeneity rather than towns with no history of e-waste exposure. Two of the
chance [20]. An I2 value of 25% is considered low hetero- occupational-related studies [28, 29] recruited age- and sex-
geneity, a value between 50 and 75% is moderate, and a matched farmers as control groups. The sample sizes of the
value above 75% is considered high heterogeneity [20]. studies included in this review ranged between 48 [30] and
The random effect meta-analysis model with restricted 377 [2]. The majority of the studies (16 of 20) had both male
maximum likelihood (REML) method [21] was used to and female participants, three studies had all-male partici-
calculate the overall SMD and its 95% confidence interval pants [28, 31, 32], and one study did not describe gender
(CI). The REML method performs well with a small number breakdown [23]. Tables 1 and 2 provide a summary of the
of studies and produces an unbiased estimate of the study characteristics of the included studies.
Issah et al.: E-waste and DNA damage 5
Table : Summary results of occupational studies including exposure groups, study location, samples used, and key findings.
Author Exposure Exposed group Country Samples Exposure Outcome Main findings
setting type
Alabi et al. [] Occupational Scavengers () Nigeria Blood, Pb, Ni, Cd, and Micronuclei, binucleated cells, Micronuclei: mean (. vs. ., p<.), binucle-
vs. control group buccal cells Cr pycnosis, condensed chromatin, ated cells: (. vs. ., p<.), pycnosis: (. vs.
() karyorrhesis, lobbed nuclei ., p<.), condensed chromatin: (. vs. .,
p<.), karyorrhesis: (. vs. ., p<.), lobbed
nuclei: (. vs. ., p<.).
Berame et al. [] Occupational E-waste recyclers Philippines Buccal cells NR Micronuclei frequency E-waste workers had increasedmicronuclei compared to
() vs. controls the control group.
()
Neitzel et al. [] Occupational Informal recycling Thailand Urine and Pb, Cd, Mn -hydroxy-′-deoxyguanosine Men who reported working > h/week had significantly
() blood (-OHdG) (p=.) higher levels of -OHdG compared to men
working ≤ h/week
Sheng et al. [] Occupational Informal recycling China Dust, hair, PCDD/Fs, -OHdG Pre- vs. postworkshift -OHdG: mean (range): .
() and urine PBDEs, and (.–.) vs. . (.–.) µmol/mol creat-
PCBs inine, p<..
Wang et al. [] Occupational Informal recycling China TSP, blood Pb, Cu, and Cd Micronuclei in binucleated cells Micronuclei, median (range): median ·% (·–·) vs.
() vs. controls and urine ·% (·–·), p<·.
() Positive correlation between blood lead andmicronuclei
in binucleated cells (r=·, p<·).
Wang et al. [] Occupational Informal recycling China Blood and PCBs, Pb, Cu Chromosomal aberration, Chromosomal aberration (%): (. vs. .), micro-
() vs. farmers semen Zn, Ca, Mg, Fe micronuclei, and DNA damage (DNA nuclei (%): (. vs. .), comet assay (greater DNA
() and Se TDNA%, T.M. and OTM) damage in exposed than in control group), pall<..
duration of exposure is associated with C.A., CBMN, and
DNA damage
Yuan et al. [] Occupational Informal recycling China Blood and PBDEs Micronuclei, -OHdG Micronuclei, median (range): 
() vs. farmers urine (–) vs. . (–.), p<., -OHdG, mean ± SD:
() . ± . vs. . ± . µmol/mol of creati-
nine, p=.. Working with e-waste is associated with
increased micronuclei frequencies OR, .; % CI
(–,.), p=.
Pb, lead; Cd, cadmium; Ni, nickel; Cr, chromium; Mn, manganese; Cu, copper; Zn, zinc; Ca, calcium; Mg, magnesium; Fe, iron; Se, selenium; Hg, mercury; PBDEs, polybrominated diphenyl ethers;
PCDD/F, polychlorinated dibenzo-p-dioxins and dibenzofurans; PCBs, polychlorinated biphenyls; OH-PAHs, hydroxylated polycyclic aromatic hydrocarbons; TSP, total suspended particles;
-OHdG, -hydroxy-′-deoxyguanosine; UCB, umbilical cord blood; DNA, deoxyribonucleic acid; TDNA%,% tail DNA; TM, tail moment; OTM, olive tail moment; CBMN, cytokinetic blockmicronuclei;
CA, chromosomal aberration; MNed BNC, micronucleated binucleated cells; NR, not reported; SD, standard deviation.
6 Issah et al.: E-waste and DNA damage
Table : Summary results of ecological studies, including exposure groups, study location, samples used, and key findings.
Author Exposure setting Exposed group Country Sample Exposure Outcome Main findings
type
Chen et al. Ecological: exposed town Population China Blood NR Micronucleated binucleated cells MNed BNC frequency: (median: .%, IQR: .–
[] vs. control town (n=) .%) vs. (median: .%, IQR: .–.%), p<.
 vs. 
He et al. [] Ecological: exposed town Population China Blood POPs ROS and micronucleus rate Micronucleus rate: (. ± .‰) vs.
vs. control town (n=) (. ± .‰), p<.
 vs. 
Khlaif et al. Ecological: exposed town Population Palestine Blood N.R. Total chromosome aberrations (CA), Total chromosome aberrations (CA): mean ± SD
[] vs. control town (n=) tail length relative to tail plus nucleus’ (. ± . vs. . ± ., p<.). Comet assay:
 vs.  length (TL/TL + NL) (TL/TL + NL) mean ± SD (. ± . vs.
. ± ., p<.)
Li et al. [] Ecological: proximity Population China Blood Ca, Cu, Fe, Micronucleus rate Micronucleus rate: (. vs. .%, p<.)
group vs. remote group (n=) Pb, Mg, Se,
 vs.  and Zn
Li et al. [] Ecological: exposed town Neonates China UCB Cr Comet assay (injury rate (tailing rate) Cell injury rate (%): . vs. ., p<., Length
vs. control town (n=) and the lengths of tail) of tails (%): . vs. ., p<.
 vs. 
Lin [] Ecological: exposed town Puerperae China Placenta Cd, Pb Placental telomere length Placental telomere length: negative correlation with
vs. two control towns ( (n=) placental Cd concentration (r=−., p=.).
and  km from the  vs. 
exposed town)
Liu et al. [] Ecological: exposed Population China Blood NR Chromosomal aberrations, micronu- CA rates (%): (. vs. ., p<.), micronuclear
towns vs. control towns (n=) cleus, DNA percentage in the comet tail rates (%): (. vs. ., p<.), comet assay
 vs.  (TDNA%), tail moment (TM), and olive (mean ± SD): TDNA% (. ± . vs. . ± .),
tail moment (OTM) TM (. ± . vs. . ± .), OTM (. ± .
vs. . ± .), pall<..
Lu et al. [] Ecological: exposed Population China Urine OH-PAHs -OHdG -OHdG, GMorder: e-waste area>rural reference>urban
towns vs. control towns (n=) reference (.>.>.). Positive association be-
 vs.  tween -OHdG and ∑OH-PAHs in e-waste partici-
pants (β=.; % CI: −., .; p<.)
Ngo et al. [] Ecological: exposed town Children (– Vietnam Blood Pb, Cd, Cr, Comet (tail length (µm), olive tail Comet assay: Tail length (. ± . vs.
vs. control town years) (n=) Ni, and As moment (µm), and %Tail DNA) . ± . µm, p<.), olive tail moment
 vs.  (. ± . vs. . ± . µm, p<.), Tail DNA
(. ± .% vs. . ± .%, p<.). Blood
arsenic correlated with Tail length (r=., p<.)
and Olive Tail Moment (r=., p<.)
Ni et al. [] Ecological: exposed town Neonates China UCB Pb, Cd, Cr, -OHdG UCB plasma -OHdG: (median: . vs.
vs. control town (n=) and Ni . ng/mL, p=.). -OHdG correlated with
 vs.  Cd (r=., p=.), Cr (r=., p=.), and
Ni (r=., p<.)
Issah et al.: E-waste and DNA damage 7
Narrative synthesis of study outcomes
Of the 20 studies included, six (6) biomarkers of DNA
damage (micronuclei, comets assay, 8-OHdG, telomere
length, apoptosis rate and chromosomal aberrations) were
measured in seven (7) different biological matrices (buccal
cells, blood, umbilical cord blood (UCB), placenta, urine
and semen) (Table 3). Telomere length (n=1) and apoptosis
rate (n=1) were the least biomarkers measured, while the
micronuclei frequency rate (n=9) was the most commonly
measured biomarker. Finally,whereas six studiesmeasured
more than one biomarker, the remaining 14 studies
measured one biomarker each. Most studies used blood
(n=9) and urine (n=7) as biological matrices in which DNA
damage was measured.
Micronuclei frequency
Micronuclei (MN) frequency has been widely used as a
biomarker to investigate DNA damage in human pop-
ulations exposed to genotoxic agents [39]. In this review,
nine studies [14, 24, 28–30, 33–35, 37] utilized MN fre-
quency rates as a biomarker of DNA damage associated
with e-waste exposure. Five out of the nine studies [14, 24,
28, 29, 33] targeted occupationally exposed groups, and the
remaining four were ecological studies. Almost all
the studies were conducted in China except for two
[14, 24], which were done in Nigeria and the Philippines,
respectively.
In the Nigerian study, Alabi et al. [14] evaluated
micronuclei frequency among teenage e-waste scavengers
in the Alaba International market, a major electronic waste
dumpsite in Lagos. The results show that the average MN in
exfoliated buccal cells in scavenging e-waste workers
(n=95) was significantly higher than that in the control
group (n=104) (168.04 vs. 3.23, p<0.001). Further analysis of
other cytogenic alterations, such as markers of cell prolif-
eration (cells with condensed chromatin and binucleated
chromatin) and parameters of cell death (pyconostic and
karyorrhective cells), were all significantly higher in the
Alaba group than in the control group (all p<0.01). Similarly,
Berame et al. [24] measured MN frequency in the buccal
epithelium of e-waste recyclers and controls in Payatas, the
Philippines. The results showed a significant increase in the
number of micronuclei in e-waste workers than controls
(p=0.00) [24].
All the studies conducted inChina reported consistently
higher MN in e-waste-exposed populations than in control
groups. Wang et al. [33] and Chen et al. [34] reported similar
results between e-waste-exposed populations and control
Table : (continued)
Author Exposure setting Exposed group Country Sample Exposure Outcome Main findings
type
Wang et al. [] Ecological: exposed Population China Blood and Cu, Fe -OHdG -OHdG in males (mean ± SD): (. ± . vs.
towns vs. control town (n=) urine . ± ., p<.) μmol/mol creatinine. Blood
 vs.  ferrous associated negatively with -OHdG
(β=−., p=.)
Xu et al. [] Ecological: exposed town Preschool chil- China Blood and Pb, Cd, and -OHdG -OHdG, median (range): . (.–.)
dren (n=) urine Hg ng/g creatinine. Higher Pb and Hg exposure are
associated with higher -OHdG
Yu et al. [] Ecological: exposed town Population China House PBDEs Tail DNA%, OTM, and apoptosis rate Comet assay (mean ± SD): tail DNA% (. ± .
vs. control town (n=) dust, and vs. . ± ., p<.), OTM (. ± . vs.
 vs.  semen . ± ., p<.)
TUNEL assay: apoptosis rate ( ±  vs.  ± ,
p=.)
Pb, lead; Cd, cadmium; Ni, nickel; Cr, chromium; Mn, manganese; Cu, copper; Zn, zinc; Ca, calcium; Mg, magnesium; Fe, iron; Se, selenium; Hg, mercury; PBDEs, polybrominated diphenyl ethers;
PCDD/F, polychlorinated dibenzo-p-dioxins and dibenzofurans; PCBs, polychlorinated biphenyls; OH-PAHs, hydroxylated polycyclic aromatic hydrocarbons; TSP, total suspended particles;
-OHdG, -Hydroxy-′-deoxyguanosine; UCB, umbilical cord blood; DNA, deoxyribonucleic acid; TDNA%,% tail DNA; TM, tail moment; OTM, olive tail moment; CBMN, cytokinetic blockmicronuclei;
CA, chromosomal aberration; MNed BNC, micronucleated binucleated cells; NR, not reported; SD, standard deviation.
8 Issah et al.: E-waste and DNA damage
Table: Summary of DNAdamagebiomarkers and samples used. Blue cells indicate biomarkers assessed in the study, and gray cells indicate
the type of sample used.
Sample DNA damage biomarkers
Publications EFBC Blood UCB Placenta Urine Semen MN CA Comets* -OHdG TL A.R.
Alabi et al. []
Chen et al. []
He et al. []
Khlaif et al. []
Li et al. []
Li et al. []
Lin []
Liu et al. []
Lu et al. []
Neitzel et al. []
Ngo et al. []
Ni et al. []
Sheng et al. []
Wang et al. []
Wang et al. []
Wang et al. []
Xu et al. []
Yu et al. []
Yuan et al. []
Berame et al. []
Total            
EFBC, exfoliated buccal cells; UCB, umbilical cord blood; MN, micronuclei; CA, chromosomal aberrations; -OHdG, -hydroxy-
′-deoxyguanosine; TL, telomere length; AR, apoptosis rate; *, comet assay (TDNA%, TM, and OTM).
groups. ThemedianMN frequencywas 4% inGuiyu e-waste Chromosomal aberrations
workers (n=48) compared to 1% in the control group (n=56)
(p<0.05) [33]. Similarly, Chen et al. [34] evaluated MN fre- Three studies examined the association between e-waste
quency in residents of an e-waste site and reported a higher exposure and DNA damage using chromosomal aberration
median MN frequency (4%) in the e-waste residents than in (CA) as a biomarker. All three studies showed significantly
the control group (1%), (p<0.01). higher CA frequency among the e-waste exposed group
In a study of male e-waste recyclers by Wang et al., a compared to the control groups. Wang et al. [28] examined
significant increase in the frequency ofMNwas observed in DNA damage in peripheral blood lymphocytes among
those with occupational exposures compared with those e-waste workers (n=146) and a control group (121) in China.
with no occupational exposures (26.30 vs. 4.52%, p<0.001). The results of this study showed that the total CA in the
In addition, e-waste workers were classified into exposure e-waste workers was approximately 5-fold higher than that
durations (≤3, 3–6, and >6 years) to investigate the rela- in the control group (8.01 vs. 1.8%, p<0.001). The duration
tionship between e-waste exposure andMN frequency. The of e-waste exposure was also positively correlated with CA.
results showed a significant positive association between However, no significant difference in CA was observed
MN and duration working with e-waste [28]. The results between smoking e-waste workers and nonsmoking
from earlier studies [29, 30, 35, 37] all demonstrated a workers (p>0.05). Similarly, according to Liu et al. [37],
strong and consistent association between e-waste expo- individuals (n=171) recruited from three e-waste polluted
sure and MN frequency rates. Overall, these studies villages in northern China had significantly increased
consistently indicated a link between e-waste exposure levels of total CA than those recruited (n=30) from a
andMN frequency in exfoliated buccal cells and peripheral neighbouring village with no e-waste exposure (5.50 vs.
blood lymphocytes (PBLs). 1.70%, p<0.001). The third study by Khlaif et al. [23] also
Issah et al.: E-waste and DNA damage 9
found a significant mean difference in total CA among the actively involved in e-waste processing with 121 adult
e-waste-exposed group compared to a control group in vegetable farmers who resided approximately 50 km away
Palestine (4.83 vs. 0.75%, p<0.001). with no history of e-waste exposure, Wang et al. [28]
reported the duration of exposure to be significantly posi-
Comet assay parameters tively associatedwith TDNA%and TMof both spermatozoa
and lymphocytes and showed that the e-waste workers
Six studies [15, 23, 26, 28, 31, 37] utilized the comet assay to were at increased risk of DNA damage compared to the
measure DNA damage associated with e-waste disposal. vegetable farmers.
One study [26] examined the tail injury rates and tail length
(TL) of neonates born in Guiyu, an e-waste polluted town, Oxidative DNA damage
compared to those born in Chaonan, with no history of
e-waste exposure. Tail injury rates and TL were observed to Oxidative DNA damage threatens genome stability and has
be significantlyhigher in theGuiyugroup than in the control been implicated in the pathogenesis of chronic diseases,
group (33.20 vs. 10.7, p<0.05) and (4.49 vs. 2.09, p<0.01), including cancers [40, 41]. 8-hydroxy-2′-deoxyguanosine
respectively. The measured umbilical cord blood chromium (8-OHdG) is the primary product of oxidative DNA damage
(UCB Cr) level, which was higher in the exposed neonates, and is used as a biomarker of genome stability associated
correlated positively with DNA damage parameters (tail with genotoxic exposure [42]. In this review, seven studies
injury rate and tail length). Similarly, in a recent study in [2, 16, 25, 27, 29, 32, 38] examined plasma or urine 8-OHdG
Vietnam, DNA damage in blood cells given as TL, olive tail as a biomarker of DNA damage associated with e-waste
moment (OTM) and% tail DNA (TDNA%) were measured in exposure.
children who resided in an e-waste polluted village and The results of these studies were contradictory. Three
children from a control village. The mean ± standard devi- studies [2, 27, 29] did not find a significant difference
ation TL, OTM, and TDNA% of 2.07 ± 0.41, 0.16 ± 0.04, and between the e-waste-exposed population and the control
2.67 ± 0.42 respectively, in the e-waste exposed children group. Ni et al. [27] did not find any significant difference in
were higher than those in children from a control village UCB plasma concentration of 8-OHdG in neonates born in
with 1.78 ± 0.59, 0.14 ± 0.03, and 2.22 ± 0.40 respectively Guiyu and those born in a control town (median: 162.9 vs.
(pall<0.001) [15]. 153.69 ng/mL, p=0.117). However, neonates whose mothers
Liu et al. [37] examined DNA damage in residents of engaged in e-waste recycling activities had higher UCB
e-waste processing sites in China. The results showed that plasma concentrations of 8-OHdG than neonates tomothers
the averages of TDNA% (4.27 vs. 1.18), TM (0.53 vs. 0.05), who were non-occupationally exposed (median: 179.77 vs.
and OTM (0.82 vs. 0.19) were significantly higher in the 159.00 ng/mL, p=0.028). In addition, blood Cd, Cr, and Ni
e-waste-exposed group than in the control group. Among were significantly positively associated with UCB plasma
the exposed group, females had a higher degree of DNA 8-OHdG concentration. In contrast, Wang et al. [2] found
damage than their male counterparts. Another study per- higher urinary 8-OHdG in the non-occupationally exposed
formed by Khlaif et al. [23] found significantly increased group than in the occupationally exposed group (mean
DNA damage parameters (tail and nucleus lengths) in an creatinine levels: 3.78 vs. 3.55 nmol/mol, p<0.01). Yuan et al.
e-waste-exposed population compared with controls in [29] also reported a statistically insignificant difference in
Palestine. urinary 8-OHdG among 23 e-waste workers and 26 farmers
Yu et al. [31] also examined TL and TDNA% in blood (mean creatinine levels: 69.04 vs. 229.97 μmol/mol,
lymphocytes of men recruited from e-waste dismantling p=0.200) in China.
areas in south China to assess semen quality associated Lu et al. [38] examined the urinary concentration of
with e-waste exposure. The results of this study showed 8-OHdG in people living in and around e-waste disman-
that the average TDNA% and OTM of 57.88 vs. 33.55, tling facilities (n=130) and in reference populations from
p<0.001 and 12.3 vs. 5.14, p<0.001 respectively, were rural (24) and urban (22) areas in China. They reported that
significantly higher in the exposed group (n=32) than in the urinary 8-OHdG concentrations were in the following or-
control group (n=25). The results indicate a higher risk of der: e-waste dismantling area (GM: 16.2 μg/g Cre)>rural
infertility in the e-waste-exposed group. Similarly, Wang reference area (GM: 12.3 μg/g Cre)>urban reference area
et al. [28] found significantly higher levels of DNA damage (GM: 11.6 μg/g Cre). Another study in Thailand found an
(represented by TDNA%, TM andOTM) in spermatozoa and association between the duration of e-waste exposure and
lymphocytes of e-waste-exposed men than in those of the urinary level 8-OHdG. The study found significantly higher
controls. Again, comparing 146 adult men directly and urinary 8-OHdG in men who worked ≥48 h/week than in
10 Issah et al.: E-waste and DNA damage
those who worked ≤48 h/week [16]. Similarly, Sheng et al. by Berame et al. [24], which did not report the mean and
[32] found a sharp increase in the urinary level 8-OHdG standard deviation (SD) values. Studies that reported me-
from the preworkshift (6.40 ± 1.64 μmol/mol) to the post- dians and interquartile range (IQR) or range [29, 33, 34]
workshift (24.55 ± 5.96 μmol/mol), p<0.05. The rise in were converted to means and SD using the formulas pro-
postworkshift urinary 8-OHdG levels was attributed to vided for different sample sizes by Wan et al. [43].
oxidative stress on workers during their work time pro- Despite high heterogeneity observed between studies
cessing e-waste. Xu et al. [25] also found elevated blood Pb (I2=95.81%), the meta-analysis showed a significantly
and Hg levels in preschool children living in e-waste- higher MN frequency among e-waste exposed population
exposed towns to be significantly associated with urinary than the control population with an overall SMD of 2.30
8-OHdG concentration. (95% CI: 1.36, 3.24, p-value<0.001) (Figure 2a). Potential
publication bias was not explored due to the limited
Telomere length number of studies (<10 studies) included in the meta-
analysis.
One study [36] examined 227 placentas of healthy puer- In a subgroup analysis considering only ecological
perae from Guiyu and 93 placentas from a control group to studies, four studies were included in the analysis. The
assess placenta telomere length associated with e-waste pooled estimate of the SMD was 1.68 (95% CI: 0.85, 2.51,
exposure. The results showed that placental Cd concen- p<0.001), with high variability between studies (I2=90.94%)
tration was negatively correlated with placental telomere (Figure 2b). Considering only studies conducted among
length (r=−0.138, p=0.013) and was observed to be corre- e-waste workers (occupational), only three studies were
lated in a dose-dependent manner. included in the analysis. The combined SMD showed that
e-waste recyclers had higher MN than controls (SMD: 3.09,
Apoptosis rate 95% CI: 1.53, 4.66, p<0.001) (Figure 2b). In a further sensi-
tivity analysis stratified by study quality, five studies
Regarding the apoptosis rate as a biomarker of DNA dam- adjudged “high quality” by the NOS confirmed that MN
age associated with e-waste exposure, Yu et al. [31] found a frequency was higher among the e-waste exposed group
significant increase in the apoptosis rate in spermatozoa of compared to the controls (MSD: 2.80, 95% CI: 1.79, 3.81,
residents of e-waste-exposed towns compared to a control p<0.001) (Figure 2c). Only two studies were considered “low
group (32 ± 19% vs. 20 ± 8%, p=0.037). quality” and did not show a significant difference in MN
frequency between the two groups (p=0.35).
Risk of bias (quality) assessment
Discussion
All studies included in this review were cross-sectional.
The risk assessment scores ranged between 3 and 7 To the best of our knowledge, this systematic review with
(maximum of 10). Of the 20 studies, 12 studies [2, 14, 15, meta-analysis is the first to specifically assess the risk of
26–31, 33, 36, 37] scored above themedian score of five and DNA damage associated with e-waste processing/disposal
were considered high quality. The appraisal details are in human populations. We identified and evaluated 20
summarized in Table 4. studies that investigated associations between e-waste
exposure and various biomarkers of DNA damage. Nine of
these studiesmeasuredDNAdamage byMNassay of which
Estimate of variance across studies and seven were deemed combinable for meta-analysis. The
pooled outcomes review provides ample evidence of the deleterious effects
of e-waste processing on DNA integrity, as evaluated
Nine out of the 20 included studies used Micronuclei (MN) through well-known DNA damage biomarker assays.
frequency assay to measure the risk of DNA damage Despite high heterogeneity between studies, the
associated with e-waste exposure. Seven of these studies overall SMD estimate showed higher MN frequency among
were included in the meta-analysis. One study [14], which the e-waste exposed group compared with the control
measuredMN in exfoliated buccal cells, was excluded from group with an effect size (SMD) of 2.30 (95% CI=1.36, 3.24).
the meta-analysis because it was considered an outlying Subgroup analysis by study setting revealed that workers
study that significantly affected the meta-analysis results. who directly recycle e-waste (occupational) had higher
The other excluded studywas conducted in the Philippines MN frequency (SMD: 3.09, 95% CI: 1.53, 4.66, p<0.001)
Issah et al.: E-waste and DNA damage 11
Table : Quality assessment of included studies based on the modified Newcastle–Ottawa Scale for cross-sectional studies.
Publication Sample selection criteria (four stars) Comparability (four stars) Exposure (one star) Outcome (one star) Total
( stars)
. Representativeness of . Sample size: . Non-respondents: a . Comparison group: . Subjects in outcome . Exposure ) Outcome mea-
sample: a **random; b a *justified and *comparability and a *described by au- groups comparable: a * measurements: a surements: a *vali-
*non-random; c selected satisfactory; b response rate satisfac- thors as geographi- study controls for most *exposure chem- dated methods
groups; d no description not justified tory; b comparability cally distinct; b *same important confounder; b ical(s) quantified; described; b no
and/or response rate community; c no com- *study controls for any b exposure chemicals description of
unsatisfactory; c no parison group additional confounder; c not reported methods.
description study did not control for
any confounder.
Alabi et al. b* b c a* b* a* b* a* a* /
[] (high)
Chen et al. b* b c a* a* b* b a* /
[] (low)
He et al. b* b c a* a* b* a* a* /
[] (high)
Khlaif et al. b* b c a* c b a* /
[] (low)
Li et al. [] b* b c a* b* c a* a* /
(low)
Li et al. [] b* b c a* a* b* a* a* /
(high)
Lin [] b* b c a* a* b* a* a* /
(high)
Liu et al. a** b c a* a* b* b a* /
[] (high)
Lu et al. [] b* b c a* c a* a* /
(low)
Neitzel b* b c c a* b* a* a* /
et al. [] (low)
Ngo et al. b* b c a* a* b* a* a* /
[] (high)
Ni et al. [] b* b c a* a* b* a* a* /
(high)
Sheng et al. a** b c c c a* a* /
[] (low)
Wang et al. a** b c a* a* b* a* a* /
[] (high)
Wang et al. b * b c a* a* b* a* a* /
[] (high)
Wang et al. b* b c a* a* b* a* a* /
[] (high)
12 Issah et al.: E-waste and DNA damage
compared to occupationally unexposed individuals (SMD:
1.68, 95% CI: 0.85, 2.51, p<0.001). A possible explanation
for these results might be that e-waste workers in the
informal sector are continuously involved inmultiple tasks
and work in the open using rudimentary tools with little or
no use of personal protective equipment [44, 45]. This
practice exposes the recyclers to higher levels of toxic
chemicals compared to the general population [46]. The
frequency of MN is generally used as a biomarker of effect
associated with exposure to genotoxic chemicals [47, 48].
Therefore, chronic exposure to these toxic chemicals may
result in some degree of DNA damage, as explained by the
increased levels ofMN in e-waste recyclers compared to the
non-occupational exposed group.
Even though all studies included in the meta-analysis
were conducted in China and had similar exposure pro-
files, substantial heterogeneity still existed. The high
variability between studies could be attributed to partici-
pant’s characteristics such as age, gender, diet, and
lifestyle factors (e.g., smoking, alcohol intake, and recre-
ational drugs) which may influence MN frequency in pe-
ripheral blood leukocytes (PBL) [49]. Except for the study
done by Li et al. [35], which did not control for any con-
founders, the remaining seven studies controlled for con-
founding by smoking and other important risk factors
through data collection and analysis. However, four
studies [28, 29, 33, 37] that controlled for confounding by
smoking did not provide quantitative data about smoking,
which could result in misleading conclusions when
comparing smokers and non-smokers [49]. Given the
causal role of MN in cancer development [50] and the evi-
dence of their increased levels shown in this review, MN
could be a primary biomarker for assessing DNA damage in
e-waste-exposed populations.
The review also found that other DNA damage bio-
markers, including chromosomal aberrations, tail length
(TL), percent tail DNA (TDNA%), tail moment (TM) and
8-OHdG showed a consistent higher frequency among the
e-waste exposed group than the controls. For instance,
three studies in this review assessed chromosomal aber-
rations (CAs) associatedwith e-waste exposure.Wang et al.
[28] demonstrated increased CA levels in the PBL of e-waste
workers compared to controls in China. Similarly, Liu et al.
[37] showed that individuals living in e-waste polluted
villages in northern China had higher CA levels than those
living in a neighbouring village with no e-waste exposure.
A similar study conducted in Palestine by Khlaif et al. [23]
reported increased CA levels in an e-waste-exposed pop-
ulation compared with controls. Induced chromosomal
aberrations are useful biomarkers of occupational and
environmental exposures to genotoxic agents and are
Table : (continued)
Publication Sample selection criteria (four stars) Comparability (four stars) Exposure (one star) Outcome (one star) Total
( stars)
. Representativeness of . Sample size: . Non-respondents: a . Comparison group: . Subjects in outcome . Exposure ) Outcome mea-
sample: a **random; b a *justified and *comparability and a *described by au- groups comparable: a * measurements: a surements: a *vali-
*non-random; c selected satisfactory; b response rate satisfac- thors as geographi- study controls for most *exposure chem- dated methods
groups; d no description not justified tory; b comparability cally distinct; b *same important confounder; b ical(s) quantified; described; b no
and/or response rate community; c no com- *study controls for any b exposure chemicals description of
unsatisfactory; c no parison group additional confounder; c not reported methods.
description study did not control for
any confounder.
Xu et al [] b* b c c a* b* a* a* /
(low)
Yu et al. b* b c a* a* b* a* a* /
[] (high)
Yuan et al. b* b c a* a* b* a* a* /
[] (high)
Berame b* b c a* a* b* b a* /
et al. [] (low)
Issah et al.: E-waste and DNA damage 13
Figure 2a: Standardized mean difference of micronuclei frequency for e-waste exposed population vs. control.
Figure 2b: Sub-group analysis by study setting.
predictive of future cancer risk [51, 52]. This review’s results Other studies have found increased frequencies of CA in
are consistent with a recent meta-analysis that concluded foundry workers [54] and farmers [55].
that occupational exposure to genotoxic agents such as Six studies adopted the comet assay (single-cell gel
benzene was associated with CA and MN frequencies [53]. electrophoresis assay) to assess DNA damage associated
14 Issah et al.: E-waste and DNA damage
Figure 2c: Sub-group analysis by study quality.
with e-waste disposal. Primary comet assay measure- such as metals and other persistent organic pollutants
ments, including tail length (TL) and a fraction of DNA in (POPs) are suggested to induce DNA damage through
the tail (% tail DNA), and derived indices, including tail direct interaction with the DNA [60]. The results of this
moment (TM) (tail length × % tail DNA) and olive tail review are similar to those reported by Villarini et al. [61]
moment (OTM) (the distance between the centres of gravity and Cayir et al. [62], where DNA damage measured by the
of the head and the tail along the x-axis of the comet assay was higher among welders exposed to mag-
comet × TDNA%) [56], were used to determine DNA dam- netics and farmers exposed to pesticides, respectively,
age levels associated with e-waste exposure. The comet than the general population.
assay is a versatile, economical, and fast technique that is Three of the seven studies [2, 27, 29] that examined
widely used in biomonitoring human exposure to muta- DNA damage using 8-OHdG did not find any significant
genic agents and is considered one of the most reliable differences between e-waste-exposed populations and the
biomarkers of early biological effects [57]. However, the reference populations. Several factors could account for
available literature does not consider the comet assay to be the lack of differences observed in these studies. First,
predictive of cancer risk [58]. Overall, all the studies Yuan et al. [29] recruited only 49 (23 exposed and 26 con-
reviewed demonstrated strong and consistent relation- trols) participants in their study. This small sample size
ships between e-waste exposure and DNA damage, repre- may lack the power to detect any differences between the
sented by TL, TDNA%, TM and OTM, as determined by the groups. In addition, the biological matrix used to measure
comet assay. These results may be explained by the fact 8-OHdG concentration could affect the results of these
that the majority of the studies were conducted in and studies. For instance, urine was widely used to measure
around Guiyu, China. Guiyu is noted for informal e-waste 8-OHdG in e-waste workers and controls. Although useful,
recycling and other industrial activities contributing urinary 8-OHdG is considered a less sensitive and accurate
significantly to environmental pollution [46, 59]. E-waste biomarker compared to peripheral blood leukocytes (PBL)
recyclers and residents may be exposed to high levels of 8-OHdG levels [63]. None of the studies in this review
potential clastogens and aneugens, whichmay damage the measured 8-OHdG in PBL, representing a long-term
DNA, as observed in this systematic review’s findings. response to oxidative stress and a more accurate measure
Genotoxic chemicals released during e-waste recycling of the body burden of DNA damage lesions [63]. However,
Issah et al.: E-waste and DNA damage 15
direct involvement in e-waste recycling was consistently integrated measure of exposure to the chemicals of inter-
associated with 8-OHdG levels. For example, neonates of est, their ability to escape detoxification (metabolic acti-
mothers who were directly involved in the processing of vation) and to be delivered to the target macromolecules in
e-waste had a significantly higher umbilical cord blood target tissues, and the efficiency of the body’s DNA repair
(UCB) plasma 8-OHdG than neonates whose mothers were pathways [64, 65].
non-occupationally exposed to e-waste [27]. This could be
attributed to the higher concentrations of metals detected
in mothers who recycle e-waste, as evidenced by 8-OHdG
been positively associated with Cd, Cr, and Ni concentra- Conclusions
tions (pall<0.05) [27]. In addition, Neitzel et al. [16] found a
significant association between increased work duration Despite the limitations outlined above, the evidence
and urinary 8-OHdG concentration, whiles Sheng et al. [32] from this study suggests that occupational and non-
observed a significant difference betweenpreworkshift and occupational exposures to e-waste are associated with an
postworkshift urinary levels of 8-OHdG in e-waste workers. increased risk of DNA damage measured through an MN
frequency and other wide range of DNA damage bio-
Limitations markers. Overall, sensitive, reliable and cost-efficient as-
says including comet, and micronuclei assays, were used
The current review is notwithout limitations. First, because to measure DNA damage. Therefore, the findings of these
most of the studies included in this review (75%) were studies suggest that chronic exposure to e-waste could be
conducted in China, results and conclusions may not be predictive of future cancer risk to people who directly
transferable to other populations. In addition, the current process e-waste and residents of e-waste polluted towns.
review cannot demonstrate a causal relationship between In addition, other DNA modifications, including epige-
e-waste exposure and DNA damage since all the studies netic markers such as DNA methylation, post-
included are cross-sectional. Future studies should translational histone modifications and miro RNA fre-
consider longitudinal studies that will allow researchers to quencies, should be considered in future investigations to
evaluate the causal relationships between e-waste expo- provide further elucidation on the mechanisms of e-waste
sure and DNA damage by assessing factors such as tem- induced health effects. We, therefore, propose to conduct
porality and dose-response relationships. a primary study at the Agbogbloshie e-waste recycling site
Second, most of the studies included suffered from in Accra, Ghana, to analyze DNA methylation of long
inadequate sample sizes and non-reporting of response interspersed nucleotide element-1 (LINE-1) as a proxy
rates and were limited to convenience samples. Only six for global DNA methylation among informal e-waste
studies out of the 20 studies had sample sizes >200. In recyclers. We also intend to apply robust statistical tech-
addition, only two studies randomly recruited participants, niques for estimating the health effects of multi-pollutant
and no study justified the sample sizes used or reported on mixtures to estimate DNA methylation associated with
the response rates. Future studies should consider robust the mixture of pollutants, which represent the reality of
methods that will enable the generalizability of study find- e-waste exposure than estimating the effect of one
ings by including sample size calculations and reporting chemical at a time.
participant’s response rates.
Third, to date, far too little attention has been paid to Research funding: This studywas financed by the½West
susceptible populations, such as neonates and children, Africa-Michigan CHARTER in GEO-Health with funding
with an increased risk of exposure due to extra exposure from the United States National Institutes of Health/
routes (breastfeeding and hand-to-mouth behaviour) and Fogarty International Center (US NIH/FIC) (paired grant
lower toxic elimination rates. Only four studies targeted no 1U2RTW010110-01/5U01TW010101) and Canada’s
neonates and children in this review. There is, therefore, the International Development Research Center (IDRC)
need to scale up research involving these groups of people (grant no. 108121-001).
since some of the chemicals released during e-waste recy- Author contributions: All authors have accepted respon-
cling are known neurodevelopmental toxicants. sibility for the entire content of this manuscript and
Finally, the use of urinary 8-OHdG concentration to approved its submission.
measure DNA damage may not provide an adequate mea- Competing interests: Authors state no conflict of interest.
sure of DNA damage. Future studies should consider Informed consent: Not applicable.
measuringDNA adducts from the blood,which provides an Ethical approval: Not applicable.
16 Issah et al.: E-waste and DNA damage
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