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Environmental Pollution 282 (2021) 116952

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Environmental Pollution
journal homepage: www.elsevier.com/locate/envpol

Review

Current progress on the effect of mobile phone radiation on sperm


quality: An updated systematic review and meta-analysis of human
and animal studies
Gang Yu a, 1, Zhiming Bai b, d, 1, Chao Song a, Qing Cheng b, Gang Wang b, Zeping Tang c,
Sixing Yang a, *
a
Department of Urology, Renmin Hospital of Wuhan University, Wuhan, China
b
Department of Urology, Affiliated Haikou Hospital of Xiangya Medical College, Central South University, Haikou, China
c
Guangdong Environmental Radiation Monitoring Center, Guangzhou, China
d
Haikou Center for Medical Synchrotron Radiation Research, Haikou People’s Hospital, Haikou, China

a r t i c l e i n f o a b s t r a c t

Article history: Potential suppression of fertility due to mobile phone radiation remains a focus of researchers. We
Received 3 June 2020 conducted meta-analyses on the effects of mobile phone radiation on sperm quality using recent evi-
Received in revised form dence and propose some perspectives on this issue. Using the MEDLINE/PubMed, Embase, WOS, CEN-
6 March 2021
TRAL, and ClinicalTrials.gov databases, we retrieved and screened studies published before December
Accepted 12 March 2021
Available online 30 March 2021
2020 on the effects of mobile phone use/mobile phone RF-EMR on sperm quality. Thirty-nine studies
were included. Data quality and general information of the studies were evaluated and recorded. Sperm
quality data (density, motility, viability, morphology, and DFI) were compiled for further analyses, and we
Keywords:
Mobile phone
conducted subgroup, sensitivity, and publication bias analyses. The pooled results of human cross-
RF-EMR. Male fertility sectional studies did not support an association of mobile phone use and a decline in sperm quality.
Sperm quality Different study areas contributed to the heterogeneity of the studies. In East Europe and West Asia,
Toxicity mobile phone use was correlated with a decline in sperm density and motility. Mobile phone RF-EMR
exposure could decrease the motility and viability of mature human sperm in vitro. The pooled results
of animal studies showed that mobile phone RF-EMR exposure could suppress sperm motility and
viability. Furthermore, it reduced sperm density in mice, in rats older than 10 weeks, and in rats
restrained during exposure. Differences regarding age, modeling method, exposure device, and exposure
time contributed to the heterogeneity of animal studies. Previous studies have extensively investigated
and demonstrated the adverse effects of mobile phone radiation on sperm. In the future, new stan-
dardized criteria should be applied to evaluate potential effects of mobile phone RF-EMR dosages.
Further sperm-related parameters at the functional and molecular levels as well as changes in biological
characteristics of germ cells should be evaluated. Moreover, the impact of mobile phone RF-EMR on
individual organs should also be examined.
© 2021 Elsevier Ltd. All rights reserved.

1. Introduction radio frequency electromagnetic radiation (RF-EMR; Belpomme


et al., 2018). The increasing popularity and use of mobile phones
Mobile phones produce a type of non-ionizing radiation termed have raised concerns on whether RF-EMR can affect male sperm
quality (Jalilian et al., 2019), and the current consensus in the
general public is that mobile phone RF-EMR is a major risk factor of
decreased sperm quality. However, the results of current research
Abbreviations: RF-EMR, radio frequency electromagnetic radiation; WOS, Web are contradictory, and whether mobile phone RF-EMR exposure
of Science; DFI, DNA fragmentation rate; CENTRAL, Cochrane Central Register of
decreases male sperm quality remains an unresolved issue in the
controlled trials.
* Corresponding author. scientific community. For instance, one study showed that sperm
E-mail address: drsixingyang@163.com (S. Yang). deformation rates in men increased with increasing mobile phone
1
The co-first authors: Gang Yu and Zhiming Bai.

https://doi.org/10.1016/j.envpol.2021.116952
0269-7491/© 2021 Elsevier Ltd. All rights reserved.
G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

usage time (Agarwal et al., 2008), whereas a different study found Epidemiology guidelines, and the guidelines for reporting animal
no such a correlation (Erogul et al., 2006). Mobile phone radiation research. We searched the MEDLINE/PubMed, EMBASE, Web of
was reported to suppress sperm motility and viability (Mailankot Science (WOS), Cochrane Central Register of Controlled Trials
et al., 2009; Ghanbari et al., 2013), whereas some different (CENTRAL) and ClinicalTrials.gov. databases for respective studies
studies suggested that this type of radiation didi not affect sperm on this topic.
density, motility, and viability in rodents (Dasdag et al., 2013; Trosic A mesh was applied to define the subject heading, which was
et al., 2013). In 2014, Liu et al. pooled the results of four cross- supplemented and simplified to achieve a more accurate literature
sectional studies, four human sperm in vitro studies, and four ani- retrieval. The search strategy in MEDLINE/PubMed was as follows:
mal studies and attempted to conduct a meta-analysis on the re- (“cell phone*"[Title/Abstract] OR “cellular phone*"[Title/Ab-
lationships of mobile phone use and sperm quality in terms of the stract]) OR “cellular telephone*"[Title/Abstract]) OR “mobile pho-
three aforementioned aspects (Liu et al., 2014). The results of this ne*"[Title/Abstract]) OR “mobile telephone*"[Title/Abstract]) OR
meta-analysis did not suggest that mobile phone usage was asso- “electromagnetic"[Title/Abstract]) AND ((“sperm*"[Title/Abstract]
ciated with changes in human sperm quality; however, direct OR “semen"[Title/Abstract]) OR “Seminal"[Title/Abstract]).
mobile phone RF-EMR exposure could reduce human sperm We searched for studies conducted before December 2020. The
motility and viability in vitro. Moreover, the results of animal ex- search strategies employed on the EMBASE and WOS databases are
periments suggested that mobile phone RF-EMR exposure could shown in Supplement 1. We also screened references in respective
decrease sperm density and motility (Liu et al., 2014). At approxi- articles to identify other potential studies.
mately the same time, Adams et al. conducted a meta-analysis on
human sperm quality, which included 10 studies (five cross- 2.2. Inclusion and exclusion criteria
sectional studies and five in vitro studies of human sperm) and
found that mobile phone RF-EMR exposure could affect human The inclusion criteria were as follows: 1. human cross-sectional
sperm motility and viability (when the results of the two afore- studies, human sperm studies in vitro (i.e., experiments were con-
mentioned study types were pooled; Adams et al., 2014). The ducted on ejected semen in vitro), and animal experiments on the
additional subgroup analysis conducted by Adams et al. using these relationships of mobile phone use/mobile phone EMR and sperm
limited studies only supported that mobile phone RF-EMR did not quality/semen quality; 2. associated studies with a control or
decrease sperm density in vitro (Adams et al., 2014). These previous comparison group; 3. associated studies with semen analysis/
studies pooled the findings of earlier studies, formulated some sperm quality analysis; 4. a specific absorption rate (SAR) of mobile
hypotheses, and revealed preliminarily relationships between phone RF-EMR below 2 W/kg for human sperm studies in vitro and
mobile phone RF-EMR exposure and male subfertility. However, animal studies.
owing to large differences in experimental conditions among the The exclusion criteria were as follows: 1. studies investigating
included studies, the meta-analyses by Liu et al. and Adams et al. the relationship of mobile phone base stations, radar EMR,
were highly heterogeneous in terms of results. Moreover, because extremely low EMR, wireless fidelity, mobile phone RF-EMR jam-
of the small number of studies available for analysis, further het- mers, and joint electromagnetic fields with male sperm quality; 2.
erogeneity analysis was limited. Thus, both research groups pro- studies investigating the effects of mobile phone RF-EMR exposure
posed that their preliminary conclusions should be further on pregnancy; 3. animal studies in vitro (i.e., studies on biological
examined and that their hypotheses should be further tested to changes in various germ cell lines such as GC2 and TM4, but lacking
elucidate the effects of mobile phone RF-EMR on male fertility. data on mature sperm quality); 4. studies containing data values
Taken together, additional data analyses are required to test the with incorrect decimal points; 5. studies in which the mean or
effects of mobile phone RF-EMR exposure on sperm quality. standard deviation could not be calculated based on the accessible
In the past six years, the rapid advancement of communication data; 6. special article types, including reviews, meta-analyses,
technology and the advent of 5G technology has led to increased comments, statements, and retracted articles.
cell phone use and subsequent higher exposure rates to associated
RF-EMR. Therefore, it is imperative to gain scientific understanding 2.3. Quality assessment
of the effect of mobile phone RF-EMR on male fertility (Choi et al.,
2018; Simko  and Mattsson 2019). Whether mobile phone RF-EMR We used the Joanna Briggs Institute Practical Application of
and other RF-EMR types emitted by wearable devices or the Clinical Evidence System (JBI) list to evaluate the included human
“Internet of Things” may exert reproductive toxicity has garnered cross-sectional studies (Laidsaar-Powell et al., 2019). We referred to
social attention and has attracted research interest. Many new the method proposed by Liu et al. and evaluated the quality of
studies using different experimental conditions have been pub- human sperm in vitro studies based on four parameters (Liu et al.,
lished, and we conducted a meta-analysis based on these studies to 2014): representativeness of subjects, type of the radiation expo-
examine the impact of mobile phone RF-EMR on sperm quality and sure device, comparability of the exposure and the control group,
to test some of the hypotheses proposed in previous studies. Our and representativeness of evaluation indices. The scoring system
analyses may elucidate the progress in the research on the rela- ranged from 0 (low quality) to 4 (high quality). We applied the
tionship of mobile phone use and male fertility. Furthermore, we Collaborative Approach to Meta-Analysis and Review of Animal
discuss personal views on the topic to provide suggestions for Data from Experimental Stroke (CAMARADES) list to evaluate ani-
future research. mal studies (Tong et al., 2019). Details are provided in Supplement
2.

2. Methods 2.4. Data extraction

2.1. Search strategies Basic information of the included studies was extracted ac-
cording to different study types. Data on sperm quality data
This meta-analysis was conducted according to the Preferred including sperm density, motility, viability, morphology, and DNA
Reporting Items for Systematic Reviews and Meta-Analyses fragmentation index (DFI) were pooled. Sperm quality data of rats
guidelines, the Meta-analyses of Observational Studies in and mice were pooled separately.
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G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

2.5. Statistical analyses 1073 studies were retrieved, and after screening, 137 studies
remained for full-text reading; of these, 98 studies were excluded,
Meta-analyses were performed using RevMan 5.3. Standardized and 39 studies were included, which comprised 5 human cross-
mean differences (SMD) and mean differences (MD) were used to sectional studies, 8 human sperm in vitro studies, and 26 animal
analyze sperm quality. Cochran’s Q test was applied to test het- studies (20 studies on rats and 6 studies on mice) for meta-
erogeneity, after which at P > 0.1, a fixed effects model was fitted, analyses. These 39 studies included results on sperm quality anal-
and at P  0.1, a random effects model was fitted. Heterogeneity is ysis of 2567 men of childbearing age (including 225 semen samples
represented by I2. Subgroup analyses were performed to analyze of men of childbearing age for sperm experiments in vitro) and 836
the origin of heterogeneity using RevMan 5.3. Regarding human epididymal semen samples of animals (583 rats and 253 mice). Full
cross-sectional studies, we performed a subgroup analysis based on texts of five studies could not be obtained even after contacting the
study area, exposure time, and evaluation method. For animal respective authors by e-mail. One study with a data value with an
studies, subgroup analyses were conducted with respect to animal incorrect decimal point mark and one study in which the standard
age (younger or older than 10 weeks), radiation exposure device deviation could not be calculated were excluded during screening;
(mobile phone or simulator), animal status during modeling despite inquiring with the respective authors by e-mail, no further
(restrained or unrestrained), and modeling time (short-term information was obtained.
exposure at < 140 h or long-term exposure at > 140 h).
A one-by-one exclusion method was applied to the sensitivity 3.2. Basic information
analysis. For parameters included in more than seven studies, we
applied a funnel chart, Egger’s test, and Begg’s test using Stata 16.0 The basic information of the included studies is shown in
to evaluate potential publication bias. Tables S1, S2, and S3.
Literature retrieval, quality assessment, and data extraction
were independently completed by two reviewers. If the opinions
3.3. Quality evaluation
were inconsistent, the reviewers consulted with each other or with
a third party.
As shown in Table 1, the JBI score of the human studies ranged
from 9 to 15, and only in one study was the JBI score below 10,
3. Results whereas in four studies, it was higher than 10. The JBI score for
human sperm in vitro studies ranged from 8 to 10; in one of these
3.1. Search results studies, the JBI score was 8, while in seven studies, the JBI score was
9. Regarding animal studies identified through the CAMARADES
A flow chart of the screening process is shown in Fig. 1. In total, list, the JBI scores of four studies were below 7, while those of 22

Fig. 1. Flow chart of the screening process.

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G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

Table 1
Quality evaluation of included studies.

Human study Score Human sperm study Score Animal study Score

Fejes(Fejes et al., 2005) 11 Erogul(Erogul et al., 2006) 9 Dasdag(Dasdag et al., 2003) 10


Agarwal(Agarwal et al., 2008) 11 Agarwal(Agarwal et al., 2009) 9 Yan(Yan et al., 2007) 10
Fejio(Feijo et al., 2011) 9 Ahmad(Ahmad and Baig 2011) 9 Ribeiro(Ribeiro et al., 2007) 12
Rago(Rago et al., 2013) 12 Dkhil(Dkhil et al., 2011) 9 Mailankot(Mailankot et al., 2009) 8
Yildirim(Yildirim et al., 2015) 12 Veerachari(Veerachari and Vasan 2012) 9 Lee(Lee et al., 2010) 8
Gorpinchenko(Gorpinchenko et al., 2014) 8 Imai(Imai et al., 2011) 6
Zalata(Zalata et al., 2015) 9 Nisbet(Nisbet et al., 2012) 6
Nakatani-Enomoto(Nakatani-Enomoto et al., 2016) 9 Ab Zayed(Zayed et al., 2012) 4
Trosic(Trosic et al., 2013) 8
Ghanbari(Ghanbari et al., 2013) 10
Shahin(Shahin et al., 2014) 12
Tas(Tas et al., 2014) 10
Liu(Liu et al., 2015) 12
Gohari(Gohari et al., 2017) 12
Oyewopo(Oyewopo et al., 2017) 10
Pandey(Pandey et al., 2017) 10
Almasiova(Alma siova
 et al., 2018) 12
Pandey(Pandey and Giri 2018) 10
Shahin(Shahin et al., 2018) 10
Narayanan(Narayanan et al., 2019) 8
Gautam(Gautam et al., 2019) 6
Yahyazadeh(Yahyazadeh and Altunkaynak 2019) 10
Shahin(Shahin et al., 2019) 10
Yu(Yu et al., 2020) 12
Vafaei(Vafaei et al., 2020) 10
Pardhiya(Pardhiya et al., 2020) 10

studies were higher than 7. 3.5.2. Sperm motility


As shown in Fig. 2B, the sperm motility analysis included five
studies (random model; MD ¼ 4.77 [-11.68, 2.15]; P ¼ 0.18;
3.4. Meta-analysis results I2 ¼ 87%; Q test P < 0.0001). Heterogeneity of the studies was high.
The subgroup analysis showed that I2 decreased to 0% (Q test
3.4.1. Research status P ¼ 0.65), P was 0.04 in the East Europe and West Asia group
Currently, relevant human epidemiological studies are still whereas in the America group, I2 was 95% (Q test P < 0.0001), P was
lacking. Studies have been predominantly conducted using animal 0.59. I2 decreased to 56% (Q test P ¼ 0.10), P was 0.56 in the forward
experiments, some of which used mobile phones, while others motility group, whereas I2 was 92% (Q test P ¼ 0.0003), and P was
used RF simulators to produce mobile phone RF-EMR. Only few 0.12 in the total motility group.
studies discussed effects of RF-EMR produced by 4G or 5G devices The sensitivity analysis showed that removing the study by
on reproductive functions, and considerable differences between Agarwal et al. reduced MD to 2.25 (6.55, 2.04), and I2 to 35% (Q
evaluation methods of the actual RF-EMR dosages in the exposure test P ¼ 0.20), P ¼ 0.30; the analysis results did not significantly
area were observed. Most studies assessed the effects of RF-EMR on change after removing other studies.
sperm density, motility, viability, and morphology, however, only
few investigated the effects of mobile phone RF-EMR exposure on 3.5.3. Sperm viability
reproduction through advanced sperm function tests, sperm DFI As is shown in Fig. 3A, the sperm viability analysis included two
test, and offspring quality tests. Almost all included studies inves- studies (random model; MD ¼ 4.91 [-23.53, 13.72]; P ¼ 0.61;
tigated the effects of whole-body RF-EMR exposure on male I2 ¼ 95%; Q test P < 0.0001).
fertility, and only few investigated the effects of local RF-EMR
exposure on certain reproductive organs. 3.5.4. Sperm morphology
As shown in Fig. 3B, the analysis of sperm morphology included
four studies (random model; MD ¼ 0.32 [-1.01, 0.37], P ¼ 0.36, and
3.5. Meta-analysis results of human cross-sectional studies I2 ¼ 91%; Q test P < 0.00001). The subgroup analysis showed that in
the East Europe and West Asia group, I2 was 0% (Q test P ¼ 0.87),
3.5.1. Sperm density and P ¼ 0.25, while in the America group, I2 was 97% (Q test
As shown in Fig. 2A, five studies were included for sperm den- P < 0.00001), and P ¼ 0.46.
sity analysis (random model; MD ¼ 1.21 [-15.14, 12.73]; P ¼ 0.87; The sensitivity analysis suggested that removing the study by
I2 ¼ 91%; Q test P < 0.001). Owing to the large heterogeneity of Agarwal et al. decreased the MD to 0.05 (0.17, 0.07), I2 to 0% (Q
studies, subgroup analyses were conducted, and the results showed test P ¼ 0.44), and P to 0.41. Removing other studies did not
that I2 decreased to 0% (Q test P ¼ 0.77), P was 0.0003 in the East significantly change the analysis results.
Europe and West Asia group, while in other regions I2 was 97% (Q
test P < 0.0001) and P was 0.98. 3.6. Meta-analysis results of human sperm studies
The sensitivity analysis showed that MD decreased to 7.99
(19.13, 3.15), I2 decreased to 79% (Q test P ¼ 0.003), and P 3.6.1. Total sperm motility, viability, and density
decreased to 0.16 after removing the Feijo’s study. The total effect As shown in Fig. 4, the total sperm motility analysis included
scale, I2, Q test P, and the statistical P-value did not significantly seven studies (fixed model; MD ¼ 3.56 [-5.11, 2.00];
change when other studies were removed. P < 0.00001; I2 ¼ 0%; Q test P ¼ 0.69). The sperm viability analysis
4
Fig. 2. Forest plot and subgroup analysis of sperm density (A) and motility (B) in human cross-sectional studies. The pooled results did not suggest that mobile phone use was
associated with a decline in sperm density in humans. Study area contributed to study heterogeneity in the analyses of sperm density and motility. The evaluation method
contributed to study heterogeneity regarding sperm motility analysis. Mobile phone use in East Europe and West Asia was associated with decreased sperm density and motility.

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G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

Fig. 3. Forest plot and subgroup analysis of sperm viability (A) and morphology (B) in human cross-sectional studies. The pooled results did not indicate that mobile phone use was
associated with decreased sperm viability and morphology in humans. The study area contributed to the study heterogeneity of sperm morphology.

included four studies (random model; MD ¼ 3.51 [-4.32, 2.70]; than 10 weeks, the P-value of pooled results changed to 0.03,
P < 0.00001; I2 ¼ 0%; Q test P ¼ 0.74). Three studies (random model) indicating statistical significance.
were included in the density analysis, (MD ¼ 1.07 [-8.34, 6.20]; The sensitivity analysis suggested that removing any study did
P ¼ 0.77; I2 ¼ 0%; Q test P ¼ 0.99). The sensitivity analysis of total not change the total effect scale, I2, Q test P, or the statistical P-value,
sperm motility, viability, and density showed that excluding any of suggesting robustness of the results. As shown in Figure S1A, the
the studies did not significantly affect the observed total effect funnel plot, Begg’s test (Pr ¼ 0.06), and Egger’s test (P ¼ 0.33) did
scale, I2, Q test P, and the statistical P-value. not suggest significant publication bias in these studies.

3.6.2. Sperm DFI


As is shown in Fig. 4D, the sperm DFI analysis included two 3.7.2. Sperm motility in rats
studies (random model; MD ¼ 1.30 [-0.57, 3.18]; P ¼ 0.17; I2 ¼ 94%; As shown in Figs. 5B and 11 studies (random model) were
Q test P < 0.0001). included in the analysis of sperm motility (SMD ¼ 0.83
[-1.41, 0.24]; P ¼ 0.005; I2 ¼ 80%; Q test P < 0.00001). As shown in
3.7. Meta-analysis results of animal studies Table 2, the subgroup analyses showed that study heterogeneity
(80%; Q test P < 0.00001) may be reduced in the restrained group
3.7.1. Sperm density in rats (0%; Q test P ¼ 0.82), in rats older than 10 weeks (28%; Q test
As is shown in Figs. 5A and 17 studies (random model) were P ¼ 0.22), and in the mobile phone group (56%; Q test P ¼ 0.08).
included in the analysis of epididymal sperm density (SMD ¼ 0.32 The sensitivity analysis showed that after removing the study by
[-0.64, 0.00]; P ¼ 0.05; I2 ¼ 58%; Q test P ¼ 0.001). The subgroup Ozlem et al. SMD was reduced to 1.00 (1.49, 0.52) and I2 was
analyses are shown in Table 2. Study heterogeneity (I2 ¼ 56%; Q test reduced to 66% (Q test P ¼ 0.002; P < 0.0001), whereas the analysis
P ¼ 0.003) was significantly reduced in the restrained group results were not significantly changed after removing other studies.
(I2 ¼ 28%; Q test P ¼ 0.22) and in the simulator group (I2 ¼ 40%; Q As shown in Figure S1B, the funnel plot, Begg’s test (Pr ¼ 0.06), and
test P ¼ 0.11). In addition, subgrouping by animal age did not Egger’s test (P ¼ 0.111) did not suggest significant publication bias
significantly affect study heterogeneity; however, in animals older in the included studies.
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G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

Fig. 4. Forest plot of sperm motility (A), viability (B), density (C), and DFI (D) in human studies in vitro. The pooled results supported the claim that mobile phone RF-EMR exposure
reduces total sperm motility and viability of human sperm in vitro.

3.7.3. Sperm viability in rats 3.7.4. Sperm morphology in rats


As shown in Fig. 5C, four studies (fixed model) were included in As is shown in Fig. 5D, seven studies (random model) were
the analysis of epididymal sperm viability (MD ¼ 8.20 [-10.33, included (SMD ¼ 0.37 [-1.12, 0.37]; P ¼ 0.33; I2 ¼ 79%; Q test
6.07]; P < 0.00001; I2 ¼ 0%; Q test P ¼ 0.57). The sensitivity analysis P < 0.00001). The subgroup analysis (Table 2) showed that I2
showed that excluding any study did not significantly change the decreased to 0% (Q test P ¼ 0.59), and the P-value changed to 0.01 in
observed total effect scale, I2, Q test P, or the statistical P-value. the mobile phone group. Sensitivity analysis showed that after

7
removing the studies by Nisbet et al. or Yahyazadeh and Altun-
kaynak, the SMD was reduced to 0.59 (1.25, 0.08) and 0.13
(0.70, 0.44), respectively, I2 was reduced to 67% (Q test P ¼ 0.01)
and 68% (Q test P ¼ 0.008), respectively, and P was 0.08 and 0.65,
respectively. Removing other studies did not significantly change
the pooled results. The funnel plots, Begg’s test (Pr ¼ 0.54), and
Egger’s test (P ¼ 0.48) did not suggest significant publication bias in
the included studies (Figure S1C).

3.7.5. Sperm density in mice


As shown in Fig. 5E, epididymal sperm density analysis included
six studies (random model; SMD ¼ 2.62 [-3.79, 1.44],
P < 0.00001; I2 ¼ 83%; Q test P ¼ 0.0001). A subgroup analysis
showed that there was no significant change in the analysis results
after grouping by modeling device, exposure time, or age. The
sensitivity analysis showed that removing any study did not
significantly change the observed total effect scale, I2, Q test P, and
the statistical P-value, suggesting robustness of the results.

4. Discussion

In the past six years, studies on the effects of mobile phone


radiation on sperm quality were mostly conducted using animal
experiments rather than human surveys. Consistent with the re-
sults of a meta-analysis from 2014 (Liu et al., 2014), the pooled
results of cross-sectional studies in our study did not suggest that
mobile phone use is associated with a decline in human sperm
quality. Current evidence from human sperm in vitro studies sup-
port the claim that mobile phone RF-EMR exposure can suppress
sperm mobility and viability. The meta-analysis by Liu et al. sug-
gested that mobile phone RF-EMR exposure can decrease sperm
density and motility in rats (Liu et al., 2014). Our pooled results
indicate that mobile phone RF-EMR exposure can reduce sperm
motility in rats but that it does not significantly decrease sperm
density (P ¼ 0.05); moreover, our pooled results also suggest that
mobile phone RF-EMR reduces sperm viability in rats, which has
not been shown previously. Despite considerable heterogeneity
among included human and animal studies, the large number of
studies enabled us to conduct subgroup analyses to further analyze
these heterogeneities caused by different experimental conditions.

4.1. Human cross-sectional studies

For the first time, our results suggest that differences in study
areas may cause heterogeneity when investigating sperm quality,
while the evaluation method contributed to heterogeneity of sperm
motility results. Analysis of sperm density, motility, and
morphology indicated that the respective studies in East Europe
and West Asia were less heterogeneous. The fact that study area
may be a source of heterogeneity may be due to differences in
ethnicities, habits, and research methods; moreover, statistical
fluke may not be ruled out, which should be considered in future
studies.
There are three particularly important aspects of the present
study. First, theoretically, if mobile phone use is associated with
reduced sperm quality, such correlations should become stronger
with increasing exposure time. Unfortunately, our present sub-
group analysis failed to show that duration of phone use affected
the pooled results or study heterogeneity, which may be attributed
to the recall bias in the epidemiological survey on mobile phone
use, which causes inaccuracy of survey results (Halgamuge et al.,
2020). Second, the sensitivity analysis suggested that the study Fig. 5. Forest plot of sperm density (A), motility (B), viability (C), and morphology (D)
by Feijo et al. significantly affected the pooled results, which may be in rat studies, and sperm density (E) in mouse studies. The pooled results suggested
that mobile phone RF-EMR exposure reduced sperm motility and viability in rats, and
due to the authors’ unique research method regarding mobile sperm density in mice.
phone use as they recorded only speaking time (Feijo et al., 2011),
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G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

Table 2
Subgroup analysis of sperm density, motility and morphological normality of rats.

Condition Subgroup n MD/SMD I2(P) Model P

Sperm density Modeling method


Before analysis 16 0.26[-0.59,0.06] 56%(0.003) Random 0.11
Activity-free 10 0.16[-0.61,0.29] 62%(0.005) 0.49
Activity-restricted 6 0.45[-0.84,-0.07] 28%(0.22) 0.02
Age
Before analysis 16 0.36[-0.69,-0.02] 59%(0.001) Random 0.04
>10 weeks 9 0.45[-0.87,-0.04] 52%(0.04) 0.03
<10 weeks 7 0.25[-0.82,0.31] 65%(0.009) 0.38
Exposure device
Before analysis 17 0.32[-0.64,0.00] 58%(0.001) Random 0.05
Mobile phone 9 0.54[-1.11,0.03] 64%(0.005) 0.06
Simulator 8 0.14[-0.48,0.20] 40%(0.11) 0.43
Sperm motility Modeling method
Before analysis 11 0.83 [-1.41, 0.24] 80%(<0. 00001) Random 0.005
Activity-free 8 0.95 [-1.85, 0.06] 85%(<0. 00001) 0.04
Activity-restricted 3 0.61 [-0.97, 0.25] 0%(0.82) 0.001
Age
Before analysis 10 0.70[-1.29, 0.12] 78%(<0.00001) Random 0.02
>10 weeks 6 0.79 [-1.23, 0.36] 28%(0.22) Random 0.0003
<10 weeks 4 0.49 [-1.83, 0.85] 89%(<0. 00001) 0.47
Exposure time
Before analysis 12 0.97[-1.57, 0.37] 81% Random 0.002
>140 h 5 0.45 [-1.36, 0.46] 87%(<0.00001) Random 0.34
<140 h 7 1.33 [-1.93, 0.73] 46%(0.09) <0.0001
Exposure device
Before analysis 11 0.83[-1.41, 0.24] 80%(<0.00001) Fixed 0.005
Mobile phone 4 0.91 [-1.66, 0.16] 56%(0.08) Random 0.02
Simulator 7 0.77 [-1.65, 0.11] 85%(<0.00001) 0.09
Sperm morphology normality Modeling method
Before analysis 7 0.37[-1.12, 0.37] 79%(<0. 0001) Random 0.33
Activity-free 3 0.27[-0.60, 1.15] 66%(0. 05) 0.54
Activity-restricted 4 0.98[-2.06, 0.10] 78%(0. 003) 0.08
Exposure device
Before analysis 7 0.37[-1.12, 0.37] 79%(<0. 0001) Random 0.33
Mobile phone 3 0.47[-0.83, 0.10] 0%(0.59) 0.01
Simulator 4 0.81[-2.41, 0.79] 88%(<0.0001) 0.32

whereas other researchers recorded the entire duration of mobile 4.2. Human sperm in vitro studies
phone use. The duration of mobile phone use is a broad concept
that includes speaking time, thus in the future, researchers should The pooled results of human sperm in vitro studies showed that
take measures to accurately record mobile phone usage to obtain mobile phone RF-EMR can affect mature sperm in vitro, leading to a
more reliable results. Third, in daily life, men who use their mobile decline in sperm motility and viability. These results suggest that
phones for prolonged periods of time are frequently highly pres- when performing in vitro sperm manipulation in reproductive
sured and have irregular lifestyles; therefore, they are more prone medicine, researchers should be attentive to the harmful effects of
to smoking, drinking, and other unhealthy habits which may affect EMR including mobile phone RF-EMR. However, present evidence
sperm quality (Toda et al., 2006; Zhang et al., 2016). Compared with may not directly support that carrying mobile phones in trouser
the effects of mobile phone use on reproductive functions, the ef- pockets adversely affects sperm quality in men, resulting in a
fects of these confounding factors on sperm quality would be decline in male fertility. The reason is that mature sperm are stored
considerably stronger. Without distinguishing these factors, intra- within the human body where they are shielded by several tissues
group differences in sperm quality would increase, resulting in such as the scrotal wall and the epididymal wall, and are protected
high heterogeneity in the analysis results. Therefore, further studies by semen components. After passing through these tissue walls, the
should consider the importance of using appropriate research and intensity of RF-EMR may have decreased sufficiently to not affect
statistical methods that can eliminate the influence of confounding mature sperm.
factors. In the MARHCS cohort study, Zhang et al. conducted The total number of studies included in the sperm DFI analysis
multivariate analyses using health data of 794 men of childbearing was small, and heterogeneity of the results was large. For this
age living in Chongqing, China, and after accounting for potential reason, even though the pooled results suggested that mobile
confounding factors such as smoking and drinking, extended phone radiation did not affect sperm DFI in vitro, further studies are
speaking time on mobile phones was found to be a risk factor for required to support this conclusion.
the decline in sperm concentrations (Zhang et al., 2016). Apart from
cross-sectional surveys, new ways of exploring the effects of mobile
phone use on male health should also be encouraged. For example, 4.3. Animal studies
Volkow et al. used positron emission tomography scanning tech-
nology to detect brain function changes in humans when talking on Over the past six years, the total number of animal studies on
mobile phones, and they found that 50 min mobile phone exposure the effects of mobile phone RF-EMR on sperm function has signif-
was associated with increased brain glucose metabolism in the icantly increased. Based on the pooled results, mobile phone RF-
region closest to the antenna (Volkow et al., 2011). EMR suppresses sperm motility and viability in rats and de-
creases sperm density in mice. For the first time, our subgroup
9
G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

analysis suggested decreased heterogeneity of the pooled results of investigating local exposure to certain reproductive organs is thus
rats which were restrained during radiation exposure, which may becoming increasingly important and necessary. Lastly, it should be
be attributed to the fact that restrained rats received more noted that some studies included in this meta-analysis were of low
consistent RF-EMR at larger doses than non-restrained rats. Further quality, and their research information was incomplete, which may
analyses showed that sperm density of restrained rats decreased have contributed to the high study heterogeneity and prevented in-
significantly, which differed from the conclusions of Liu et al. as depth analysis.
their results showed high heterogeneity (Liu et al., 2014).
Rats are sexually mature at 10e12 weeks of age, and environ- 4.4. Personal views
mental pollution can reduce sperm quality in immature or mature
rats via different mechanisms (Berndston 1977). Age may also be an In the present study, we did not perform a subgroup analysis of
important factor affecting the heterogeneity of rat studies, which SAR owing to inconsistencies in the calculation of SAR values of
has been shown in our analysis of sperm density and motility in rats reproductive organs in the reviewed studies. For many years, SAR
exposed to mobile phone RF-EMR. In addition, the results of the has been recognized as a key index for evaluating environmental
present study indicate that mobile phone RF-EMR causes a signif- safety of mobile phone RF-EMR (Chen and Wang 1994). However,
icant decrease in sperm density and motility in rats older than 10 the current safety threshold of SAR can only reflect the thermal
weeks, whereas in rats younger than 10 weeks, exposure to mobile effect of RF-EMR and does not account for non-thermal effects
phone RF-EMR at an immature stage does not exert such significant (Gaestel 2010). In addition, the calculation of SAR is based on a fixed
effects. These results may be explained by the low energy of mobile value of a human body model and does not consider the actual
phone RF-EMR and the strong recovery ability of immature rats. density, permeability, and dielectric constant of specific organs
Previously, Liu et al. hypothesized that exposure time and ra- affecting SAR values (Sallomi 2012). Moreover, SAR measurements
diation devices may be important factors affecting between-study are not standardized. According to a previous report (Davis 2010),
heterogeneity (Liu et al., 2014). The results of our study showed the SAR value of the same product varies substantially between
that exposure time contributed to heterogeneity when investi- measurements by different manufacturers. Thus, the current SAR
gating sperm motility in rats; however, heterogeneity was large in threshold may not be sufficiently safe to protect human health. The
the long-term exposure subgroup, which may be attributed to the academic community should identify other appropriate indices
considerable differences in exposure time between studies in this that are more suitable for health evaluation, and interdisciplinary
subgroup (the shortest and longest exposure durations were 168 h cooperations should be established to redefine the safe threshold of
and 1095 h, respectively). Our results also supported the claim that mobile phone RF-EMR dosages.
radiation device type is another important factor that affected Mobile phone RF-EMR is a low-energy electromagnetic radia-
heterogeneity when investigating sperm density, motility, and tion. The effects of this radiation on reproductive functions have
morphology in rats. However, some inconsistencies were observed been examined using some macro-indices such as sperm density,
in the results of the respective subgroup analyses. Compared with motility, and testicular morphology; however, normality of such
the mobile phone group, the simulator group was less heteroge- indices does not necessarily preclude adverse effects of mobile
neous regarding sperm density and was more heterogeneous phone RF-EMR on reproductive parameters. Further sperm-related
regarding motility and morphology. Generally, RF-EMR produced functional and molecular indices (especially at the genetic and
by simulators is theoretically more stable than that produced by epigenetic levels) should be investigated because macroscopic
mobile phones, thus heterogeneity in the simulator group should occurrence of a disease is frequently the result of cumulative
be lower. These inconsistencies may be explained by the results of changes in the microenvironment.
our sensitivity analysis, which showed that the simulator group Recently, low-dose toxins were suggested to alter the biological
included the study by Ozlem et al. which significantly increased characteristics of cells (Fernandez-Antoran et al., 2019). Based on
heterogeneity of the sperm motility analyses; in the morphology this, it is reasonable to assume that even though short-term or
analysis, the simulator group included studies by Nisbet et al. and intermittent mobile phone RF-EMR exposure is not strong enough
Yahyazadeh and Altunkaynak, which exerted substantial effects on to damage organs, it may affect biological characteristics of germ
the heterogeneity of pooled studies (Nisbet et al., 2012; Yahyazadeh cells, resulting in alterations of disease-resistance ability of the
and Altunkaynak, 2019). Unfortunately, our results cannot explain male reproductive system or, even more concerning, of offspring
how these studies increased the heterogeneity of the pooled health. Therefore, further research is needed to explore this issue in
results. depth.
Current animal studies have mostly investigated reproductive Even though effects of mobile phone RF-EMR exposure on male
effects of systemic exposure. As male reproductive ability is fertility have been studied extensively, progress in this field is slow,
affected by multiple tissues such as the hypothalamus, pituitary and respective studies are limited regarding research scope and
gland, and the testes (Ajayi et al., 2020), researchers only prelimi- depth. Further studies revealing the reproductive effects of mobile
narily explored whether mobile phone RF-EMR affects male phone RF-EMR are still of great practical importance because even
fertility via experiments with systemic exposure. However, they if mobile phone RF-EMR exerts only minor effects on the human
could not determine the main reproductive organ through which body and causes health problems in only a few permille of users, it
mobile phone RF-EMR exerts these effects. The National Institute of may still result in a global medical catastrophe (Falcioni et al., 2018).
Toxicology also proposed that investigating the effects of mobile With the development of model communication technology, the
phone RF-EMR on certain organs was important for further clari- presence of mobile phone RF-EMR in our lives will increase (Eeftens
fying the mechanism of mobile phone RF-EMR exposure on human et al., 2018; Havas 2017), and ignoring the problems caused by this
health when exploring the relationship between mobile phone RF- radiation may lead to a lack of relevant protective measures and
EMR exposure and cancer (NIEHS 2018). This perspective is also further decline in male fertility.
applicable regarding reproductive-toxicity research on mobile
phone RF-EMR. Moreover, the development of 5G, smart multi- 5. Conclusion
antenna, and beamforming technology may cause electromag-
netic field energy to concentrate in local space, resulting in a locally The results of our meta-analysis indicated that in East Europe
high electromagnetic field pattern in certain organs. Research and West Asia, mobile phone use is associated with a decline in
10
G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

human sperm density and motility. Mobile phone RF-EMR can electromagnetic waves(rf-emw) emitted by cellular phones impact semen pa-
rameters ofbrazilian men. Hum. Reprod. 26, i139ei140.
reduce motility and viability of mature human sperm in vitro, and it vaczki, Z., Szo
€ llo
}si, J., Kolosz
Fejes, I., Za ar, S., Daru, J., Kovacs, L., et al., 2005. Is there a
can also reduce sperm motility and viability in male animals and relationship between cell phone use and semen quality? Arch. Androl. 51,
decrease sperm density of sexually mature restrained rats. Some 385e393.
important factors that affect the results of animal experiments are Fernandez-Antoran, D., Piedrafita, G., Murai, K., Ong, S.H., Herms, A., Frezza, C., et al.,
2019. Outcompeting p53-mutant cells in the normal esophagus by redox
study setup and radiation device as well as age and exposure time. manipulation. Cell Stem Cell 25, 329e341 e326.
Our study is an extension of previous studies and has scientific Gaestel, M., 2010. Biological monitoring of non-thermal effects of mobile phone
value for future studies on effects of mobile phone RF-EMR asso- radiation: recent approaches and challenges. Biol. Rev. 85, 489e500.
Gautam, R., Singh, K.V., Nirala, J., Murmu, N.N., Meena, R., Rajamani, P., 2019.
ciated with sperm quality. Oxidative stress-mediated alterations on sperm parameters in male wistar rats
exposed to 3g mobile phone radiation. Andrologia 51, e13201.
Ghanbari, M., Mortazavi, S.B., Khavanin, A., Khazaei, M., 2013. The effects of cell
Declaration of competing interest phone waves (900 mhz-gsm band) on sperm parameters and total antioxidant
capacity in rats. International journal of fertility & sterility 7, 21.
The authors declare that they have no known competing Gohari, F.A., Saranjam, B., Asgari, M., Omidi, L., Ekrami, H., Moussavi-Najarkola, S.A.,
2017. An experimental study of the effects of combined exposure to microwave
financial interests or personal relationships that could have
and heat on gene expression and sperm parameters in mice. J. Hum. Reprod. Sci.
appeared to influence the work reported in this paper. 10, 128e134.
Gorpinchenko, I., Nikitin, O., Banyra, O., Shulyak, A., 2014. The influence of direct
mobile phone radiation on sperm quality. Central European journal of urology
Acknowledgements 67, 65.
Halgamuge, M.N., Skafidas, E., Davis, D., 2020. A meta-analysis of in vitro exposures
None. to weak radiofrequency radiation exposure from mobile phones (1990e2015).
Environ. Res. 109227.
Havas, M., 2017. When theory and observation collide: can non-ionizing radiation
Appendix A. Supplementary data cause cancer? Environ. Pollut. 221, 501e505.
Imai, N., Kawabe, M., Hikage, T., Nojima, T., Takahashi, S., Shirai, T., 2011. Effects on
rat testis of 1.95-ghz w-cdma for imt-2000 cellular phones. Syst. Biol. Reprod.
Supplementary data to this article can be found online at Med. 57, 204e209.
https://doi.org/10.1016/j.envpol.2021.116952. Jalilian, H., Eeftens, M., Ziaei, M., Ro €o
€sli, M., 2019. Public exposure to radiofrequency
electromagnetic fields in everyday microenvironments: an updated systematic
review for europe. Environ. Res. 176.
References Laidsaar-Powell, R., Konings, S., Rankin, N., Koczwara, B., Butow, P., 2019. A meta-
review of qualitative research on adult cancer survivors: current strengths and
Adams, J.A., Galloway, T.S., Mondal, D., Esteves, S.C., Mathews, F., 2014. Effect of evidence gaps. Journal of Cancer Survivorship 13.
mobile telephones on sperm quality: a systematic review and meta-analysis. Lee, H.J., Pack, J.K., Kim, T.H., Kim, N., Choi, S.Y., Lee, J.S., et al., 2010. The lack of
Environ. Int. 70, 106e112. histological changes of cdma cellular phone-based radio frequency on rat testis.
Agarwal, A., Deepinder, F., Sharma, R.K., Ranga, G., Li, J., 2008. Effect of cell phone Bioelectromagnetics 31, 528e534.
usage on semen analysis in men attending infertility clinic: an observational Liu, K., Li, Y., Zhang, G., Liu, J., Cao, J., Ao, L., et al., 2014. Association between mobile
study. Fertil. Steril. 89, 124e128. phone use and semen quality: a systemic review and meta-analysis. Andrology
Agarwal, A., Desai, N.R., Makker, K., Varghese, A., Mouradi, R., Sabanegh, E., et al., 2, 491e501.
2009. Effects of radiofrequency electromagnetic waves (rf-emw) from cellular Liu, Q., Si, T., Xu, X., Liang, F., Wang, L., Pan, S., 2015. Electromagnetic radiation at
phones on human ejaculated semen: an in vitro pilot study. Fertil. Steril. 92, 900 mhz induces sperm apoptosis through bcl-2, bax and caspase-3 signaling
1318e1325. pathways in rats. Reprod. Health 12, 65.
Ahmad, L., Baig, N.M., 2011. Mobile phone rf-emw exposure to human spermatozoa: Mailankot, M., Kunnath, A.P., Jayalekshmi, H., Koduru, B., Valsalan, R., 2009. Radio
an in vitro study. Pakistan J. Zool. 43. frequency electromagnetic radiation (rf-emr) from gsm (0.9/1.8ghz) mobile
Ajayi, A.F., Akhigbe, R.E., 2020. The physiology of male reproduction: impact of phones induces oxidative stress and reduces sperm motility in rats. Clinics 64,
drugs and their abuse on male fertility. Andrologia 52, e13672. 561e565.
Alma siova
, V., Holovsk 
a, K., Simaiov , V., Ben
a  ova
, K., Ra
cek, A., Racekova, E., et al., Nakatani-Enomoto, S., Okutsu, M., Suzuki, S., Suganuma, R., Groiss, S.J., Kadowaki, S.,
2018. The thermal effect of 2.45 ghz microwave radiation on rat testes. Acta Vet. et al., 2016. Effects of 1950 mhz w-cdma-like signal on human spermatozoa.
86, 413e419. Bioelectromagnetics 37, 373e381.
Belpomme, D., Hardell, L., Belyaev, I., Burgio, E., Carpenter, D.O., 2018. Thermal and Narayanan, S.N., Jetti, R., Kesari, K.K., Kumar, R.S., Nayak, S.B., Bhat, P.G., 2019.
non-thermal health effects of low intensity non-ionizing radiation: an inter- Radiofrequency electromagnetic radiation-induced behavioral changes and
national perspective. Environ. Pollut. 242, 643e658. their possible basis. Environ. Sci. Pollut. Control Ser. 1e18.
Berndston, W.E., 1977. Methods for quantifying mammalian spermatogenesis: a NIEHS, 2018. Cell Phone Radio Frequency Radiation Studies. https://
review. J. Anim. Sci. 44, 818e833. ntpniehsnihgov/results/areas/cellphones/.
Chen, H.-Y., Wang, H.-H., 1994. Current and sar induced in a human head model by Nisbet, H.O., Nisbet, C., Akar, A., Cevik, M., Karayigit, M.O., 2012. Effects of exposure
the electromagnetic fields irradiated from a cellular phone. IEEE Trans. Microw. to electromagnetic field (1.8/0.9 ghz) on testicular function and structure in
Theor. Tech. 42, 2249e2254. growing rats. Res. Vet. Sci. 93, 1001e1005.
Choi, J., Hwang, J.-H., Lim, H., Joo, H., Yang, H.-S., Lee, Y.-H., et al., 2018. Assessment Oyewopo, A., Olaniyi, S., Oyewopo, C., Jimoh, A., 2017. Radiofrequency electro-
of radiofrequency electromagnetic field exposure from personal measurements magnetic radiation from cell phone causes defective testicular function in male
considering the body shadowing effect in Korean children and parents. Sci. wistar rats. Andrologia 49, e12772.
Total Environ. 627, 1544e1551. Pandey, N., Giri, S., 2018. Melatonin attenuates radiofrequency radiation (900 mhz)-
Dasdag, S., Zulkuf Akdag, M., Aksen, F., Yilmaz, F., Bashan, M., Mutlu Dasdag, M., induced oxidative stress, DNA damage and cell cycle arrest in germ cells of male
et al., 2003. Whole body exposure of rats to microwaves emitted from a cell swiss albino mice. Toxicol. Ind. Health 34, 315e327.
phone does not affect the testes. Bioelectromagnetics 24, 182e188. Pandey, N., Giri, S., Das, S., Upadhaya, P., 2017. Radiofrequency radiation (900 mhz)-
Davis, D., 2010. Disconnect: the Truth about Cell Phone Radiation, what the Industry induced DNA damage and cell cycle arrest in testicular germ cells in swiss al-
Is Doing to Hide it, and How to Protect Your Family. Penguin. bino mice. Toxicol. Ind. Health 33, 373e384.
Dkhil, M., Danfour, M., Al-Quraishy, S., 2011. Sperm function is affected by the Pardhiya, S., Gaharwar, U.S., Gautam, R., Priyadarshini, E., Nirala, J.P., Rajamani, P.,
electromagnetic radiation emitted by mobile phone. Afr. J. Microbiol. Res. 5, 2020. Cumulative effects of manganese nanoparticle and radiofrequency radi-
4896e4900. ation in male wistar rats. Drug Chem. Toxicol. 1e13.
Eeftens, M., Struchen, B., Birks, L.E., Cardis, E., Estarlich, M., Fernandez, M.F., et al., Rago, R., Salacone, P., Caponecchia, L., Sebastianelli, A., Marcucci, I., Calogero, A.E.,
2018. Personal exposure to radio-frequency electromagnetic fields in europe: is et al., 2013. The semen quality of the mobile phone users. J. Endocrinol. Invest.
there a generation gap? Environ. Int. 121, 216e226. 36, 970e974.
Erogul, O., Oztas, E., Yildirim, I., Kir, T., Aydur, E., Komesli, G., et al., 2006. Effects of Ribeiro, E.P., Rhoden, E.L., Horn, M.M., Rhoden, C., Lima, L.P., Toniolo, L., 2007. Effects
electromagnetic radiation from a cellular phone on human sperm motility: an of subchronic exposure to radio frequency from a conventional cellular tele-
in vitro study. Arch. Med. Res. 37, 840e843. phone on testicular function in adult rats. J. Urol. 177, 395e399.
Falcioni, L., Bua, L., Tibaldi, E., Lauriola, M., De Angelis, L., Gnudi, F., et al., 2018. Sallomi, A.H., 2012. A theoretical approach for sar calculation in human head
Report of final results regarding brain and heart tumors in sprague-dawley rats exposed to rf signals. Journal of Engineering and Sustainable Development 16,
exposed from prenatal life until natural death to mobile phone radiofrequency 304e313.
field representative of a 1.8 ghz gsm base station environmental emission. Shahin, S., Mishra, V., Singh, S., Chaturvedi, C., 2014. 2.45-ghz microwave irradiation
Environ. Res. 165, 496e503. adversely affects reproductive function in male mouse, mus musculus by
Feijo, C., Verza Junior, S., Esteves, S.C., 2011. Lack of evidence that radiofrequency inducing oxidative and nitrosative stress. Free Radic. Res. 48, 511e525.

11
G. Yu, Z. Bai, C. Song et al. Environmental Pollution 282 (2021) 116952

Shahin, S., Singh, S.P., Chaturvedi, C.M., 2018. 1800 mhz mobile phone irradiation Veerachari, S.B., Vasan, S., 2012. Mobile phone electromagnetic waves and its effect
induced oxidative and nitrosative stress leads to p53 dependent bax mediated on human ejaculated semen: an in vitro study. Int. J. Infertil. Fetal Med. 3, 15e21.
testicular apoptosis in mice, mus musculus. J. Cell. Physiol. 233, 7253e7267. Volkow, N.D., Tomasi, D., Wang, G.-J., Vaska, P., Fowler, J.S., Telang, F., et al., 2011.
Shahin, N.N., El-Nabarawy, N.A., Gouda, A.S., Me garbane, B., 2019. The protective Effects of cell phone radiofrequency signal exposure on brain glucose meta-
role of spermine against male reproductive aberrations induced by exposure to bolism. Jama 305, 808e813.
electromagnetic fieldean experimental investigation in the rat. Toxicol. Appl. Yahyazadeh, A., Altunkaynak, B., 2019. Protective effects of luteolin on rat testis
Pharmacol. 370, 117e130. following exposure to 900 mhz electromagnetic field. Biotech. Histochem. 94,
Simko , M., Mattsson, M.-O., 2019. 5g wireless communication and health effectsda 298e307.
pragmatic review based on available studies regarding 6 to 100 ghz. Int. J. Yan, J.G., Agresti, M., Bruce, T., Yan, Y.H., Granlund, A., Matloub, H.S., 2007. Effects of
Environ. Res. Publ. Health 16, 3406. cellular phone emissions on sperm motility in rats. Fertil. Steril. 88, 957e964.
Tas, M., Dasdag, S., Akdag, M.Z., Cirit, U., Yegin, K., Seker, U., et al., 2014. Long-term Yildirim, M.E., Kaynar, M., Badem, H., Cavis, M., Karatas, O.F., Cimentepe, E., 2015.
effects of 900 mhz radiofrequency radiation emitted from mobile phone on What is harmful for male fertility: cell phone or the wireless internet? Kaoh-
testicular tissue and epididymal semen quality. Electromagn. Biol. Med. 33, siung J. Med. Sci. 31, 480e484.
216e222. Yu, G., Tang, Z., Chen, H., Chen, Z., Wang, L., Cao, H., et al., 2020. Long-term exposure
Toda, M., Monden, K., Kubo, K., Morimoto, K., 2006. Mobile phone dependence and to 4g smartphone radiofrequency electromagnetic radiation diminished male
health-related lifestyle of university students. SBP (Soc. Behav. Pers.): Int. J. 34, reproductive potential by directly disrupting spock3-mmp2-btb axis in the
1277e1284. testes of adult rats. Sci. Total Environ. 698, 133860.
Tong, Q., Zhu, P-c, Zhuang, Z., Deng, L-h, Wang, Y., 2019. Notoginsenoside r1 for Zalata, A., El-Samanoudy, A.Z., Shaalan, D., El-Baiomy, Y., Mostafa, T., 2015. In vitro
organs ischemia/reperfusion injury: a preclinical systematic review. Front. effect of cell phone radiation on motility, DNA fragmentation and clusterin gene
Pharmacol. 10. expression in human sperm. International journal of fertility & sterility 9, 129.
Trosic, I., Matausic-Pisl, M., Pavicic, I., Marjanovic, A.M., 2013. Histological and Zayed, F.A., Alfifi, Z., Mahmoud, A.A., 2012. Effect of electromagnetic waves on the
cytological examination of rat reproductive tissue after short-time intermittent frequency of micronucleated polychromatic erythrocytes and the sperm
radiofrequency exposure. Arh. Hig. Rada. Toksikol. 64, 513e519. morphology of rats (rattus norvegicus). Cytologia 77, 23e33.
Vafaei, S., Motejaded, F., Ebrahimzadeh-bideskan, A., 2020. Protective effect of Zhang, G., Yan, H., Chen, Q., Liu, K., Ling, X., Sun, L., et al., 2016. Effects of cell phone
crocin on electromagnetic field-induced testicular damage and heat shock use on semen parameters: results from the marhcs cohort study in chongqing,
protein A2 expression in male BALB/c mice. Iran J Basic Med Sci 23, 102e110. China. Environ. Int. 91, 116e121.

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