1Institute of Wildlife Veterinary Research, Kodagu District, Karnataka, India
OPEN PEER REVIEW
REVIEWER STATUS
Abstract
As mobile phone usage is growing rapidly, there is a need for a comprehensive analysis of the literature to inform scientific debates about the adverse effects of mobile phone radiation on sperm quality traits. Therefore, we conducted a meta-analysis of the eligible published research studies on human males of reproductive age. Eleven studies were eligible for this analysis. Based on the meta-analysis, mobile phone use was significantly associated with deterioration in semen quality (Hedges’s g = -0.547; 95% CI: -0.713, -0.382; p < 0.001). The traits particularly affected adversely were sperm concentration, sperm morphology, sperm motility, proportion of non-progressive motile sperm (%), proportion of slow progressive motile sperm (%), and sperm viability. Direct exposure of spermatozoa to mobile phone radiation with in vitro study designs also significantly deteriorated the sperm quality (Hedges’s g = -2.233; 95% CI: -2.758, -1.708; p < 0.001), by reducing straight line velocity, fast progressive motility, Hypo-osmotic swelling (HOS) test score, major axis (µm), minor axis (µm), total sperm motility, perimeter (µm), area (µm2), average path velocity, curvilinear velocity, motile spermatozoa, and acrosome reacted spermatozoa (%). The strength of evidence for the different outcomes varied from very low to very high. The analysis shows that mobile phone use is possibly associated with a number of deleterious effects on the spermatozoa.
Almost 10% of men of reproductive age are estimated to be subfertile1. Owing to its complexity, even after identification of a plethora of underlying factors, etiology in almost half of the infertile subjects tested at fertility clinics remains obscure2. Hence, the list of the causes of male infertility is growing by the day with recent advances in fertility research3. Though advances in assisted reproduction technologies (ARTs), especially in the form of in vitro fertilization (IVF) and intracytoplasmic sperm injection (ICSI), have helped subfertile couples conceive offspring, it is feared that ARTs only bypasses the problem of subfertility and contributes towards hiding the underlying causes which have at times led to serious health problems in offspring4,5. Hence, identification of unknown aetiologies would help in prescription of specific preventive measures that will ultimately decrease the incidence of male infertility.
Most nations, especially developing countries, are witnessing an increase in the use of various radiation-emitting domestic-purpose devices that could cause mild to serious health problems based on the duration and intensity of usage6, and reduced fertility is now recognised as one such problem7. Wireless mobile phones are one of the most accepted devices with a tremendous increase in usage across the world in recent times8. Research into the impact of ionizing radiation on the development of various types of health disorders, especially cancers, has been well established9. Similarly, several studies have found an increase in the risk of developing some types of tumors after long-term exposure to non-ionizing radiation from mobile phones10. Research into the effects of mobile phone radiation on male fertility, though growing, is limited and inconclusive11,12. Recently, several case-control studies have reported results from a general population setting alongside a few studies from subfertile populations7,13–20. Like ionizing radiation, non-ionizing radiation is also expected to affect spermatozoa, though in subtle ways21. The aim of this meta-analysis was, therefore, to investigate the impact of mobile phone radiation on semen parameters in vitro as well as in vivo settings in men of reproductive age from both general and subfertile populations.
Material and methods
A systematic search of an electronic database was conducted to retrieve published studies on the impact of mobile phone radiation on semen parameters in adult men. The results have been reported according to the standards of the guidelines for meta-analysis of observational studies in epidemiology22. All English language research studies published up until January 2012 in scientific journals indexed in the searched databases were included for analysis.
Inclusion/exclusion criteria and outcomes of interest: The studies on human males of reproductive age reporting the effect of mobile phone radiation on any or all measures of semen volume, total sperm count, sperm concentration, sperm motility or sperm morphology were included. All the studies that did not satisfy the inclusion criteria were excluded.
Search strategy, data extraction and meta-analysis: Google Scholar and NLM’s PubMed database were searched for articles by using different combinations of 4 mobile phone related keywords [‘mobile phone’, ‘cellular phone’, ‘radiofrequency electromagnetic waves (RF-EMW)’, ‘radiation’] with 5 sperm quality related keywords (‘spermatozoa’, ‘semen’, ‘sperm concentration’, ‘sperm motility’, ‘sperm morphology’) Data from 11 eligible studies were extracted and separated into in vitro and in vivo categories.
Effect sizes were expressed as Hedges’s g23, separately for in vivo & in vitro studies using individual semen parameters as units of analysis (Supplementary Table 1). A random model was used to test and quantify effect size using ‘Comprehensive Meta-Analysis (v.2)’ trial version24. A random effect model was preferred over a fixed effect model in order to account for differences in both effect size and sampling error25.
Results
In vivo effects of mobile phone radiation
Our analysis shows that overall, mobile phone users had significant deterioration in semen quality (Hedges’s g = -0.547; 95% CI: -0.713, -0.382; p < 0.001). There was significant heterogeneity among effect sizes (Q = 475.985, p < 0.001), which suggest that some of the semen parameters may not be affected by mobile phone exposure. Hence, combined effect-size for each of the semen parameters were calculated separately (Table 1), and it was found that sperm concentration, sperm morphology, sperm motility, proportion of non-progressive motile sperm (%), proportion of slow progressive motile sperm (%), and sperm viability were deteriorated in individuals exposed to mobile phone radiation. By contrast, semen volume, liquefaction time, semen pH, proportion of rapid progressive motile sperm (%), and semen viscosity were not affected by mobile phone usage.
Table 1. Effect sizes of mobile phone radiation on sperm quality traits.
Sample size
Hedges’s g
p-value
In vivo studies
Semen volume
591
0.09774
0.29458
Sperm concentration
874
-0.66388
0.01858
Sperm morphology
746
-1.28325
0.00000
Sperm motility
1079
-0.81584
0.00102
Proportion of non-progressive motile sperm (%)
283
-0.16136
0.03396
Proportion of rapid progressive motile sperm (%)
283
-0.25708
0.09969
Proportion of slow progressive motile sperm (%)
283
-0.39031
0.00765
Liquefaction time (min)
321
-0.11449
0.28277
pH
321
-0.36681
0.05592
Sperm viability (%)
321
-1.13150
0.00220
Semen viscosity
321
-0.00924
0.93083
In vitro studies
Acrosome reaction (%)
24
-1.69939
0.00000
Sperm area (µm2)
24
-6.79952
0.00004
Average path velocity
20
-8.16777
0.00000
Curvilinear velocity
20
-10.37987
0.00000
DNA fragmentation
32
0.10182
0.68034
Fast progressive motility
49
-0.50794
0.01195
Hypo-osmotic swelling (HOS)
20
1.721867
0.000002
Major axis (µm)
24
-3.62708
0.01918
Minor axis (µm)
24
-7.4825
0.0361
Sperm motility
105
-2.82739
0.00118
Non motile spermatozoa
49
-0.61615
0.03275
Non progressive motility
49
0.04371
0.82612
Perimeter (µm)
24
-5.53132
0.01897
Progressive motility
12
-0.04606
0.90700
Reactive oxygen species (ROS)
36
-11.37087
0.33592
Slow progressive motility
49
-0.14543
0.67535
Sperm concentration
59
-0.02309
0.89887
Sperm zona binding
10
-0.68402
0.12153
Straight line velocity
20
-6.37614
0.00000
Total antioxidant capacity (TAC)
32
-0.25102
0.31138
Viability (%)
56
-2.75116
0.02543
Publication bias could potentially change the results of meta-analysis but analysis of funnel plot of precision by Hedges’s g using Dual and Tweedie’s trim-and-fill test26 did not change the overall effect size, suggesting little bias. Moreover, Rosenthal’s fail-safe N test27 revealed that 3964 missing studies with a mean Hedges’s g of 0 are required for the combined 2-tailed p-value to exceed 0.050. In other words, there need to be 99.1 missing studies for every observed study for the effect to be nullified.
In vitro effects of mobile phone radiation
Experimental exposure of spermatozoa isolated from healthy men of reproductive age to mobile phone radiation significantly affected sperm quality (Hedges’s g = -2.233; 95% CI: -2.758, -1.708; p < 0.001). There was significant heterogeneity among effect sizes (Q = 639.294, p<0.001), suggesting that similar to in vivo exposure, in vitro exposure may also not affect all the parameters of spermatozoa. Hence, combined effect-size for spermatozoa parameters were calculated separately (Table 1), and it was found that exposure to mobile phones significantly reduced straight line velocity, fast progressive motility, Hypo-osmotic swelling (HOS) test score, major axis (µm), minor axis (µm), total sperm motility, perimeter (µm), area (µm2), average path velocity, curvilinear velocity, motile spermatozoa, and acrosome reacted spermatozoa (%). By contrast, DNA fragmentation levels, non-progressive motility, total antioxidant capacity (TAC), progressive motility, reactive oxygen species (ROS) generation, slow progressive motility, sperm concentration, and sperm zona binding was not affected by mobile phone radiation.
A Funnel plot of precision by Hedges’s g using Dual and Tweedie’s trim-and-fill test did not change the overall effect size, suggesting little publication bias. Rosenthal’s fail-safe N test revealed that 3813 missing studies with a mean Hedges’s g of 0 are required for the combined 2-tailed p-value to exceed 0.050. In other words, there need to be 100.3 missing studies for every observed study for the effect to be nullified.
Discussion
This study was aimed to analyse the data assessing the risk of mobile phone radiation on male fertility. Our results suggest that mobile phone radiation has a tendency to significantly affect sperm quality. Based on the design of the analysed records, we divided studies into in vivo studies and in vitro studies. The effect size was significant in both the categories, suggesting that mobile phone radiation could severely compromise male fertility. This conclusion is robust, as a fail-safe test suggested that the results are not likely to be mediated by publication bias.
The number of worldwide mobile subscriptions grew from less than 1 billion in 2000 to over 6 billion in 20128, with more than half of these subscribers estimated to be children and young adults. Hence, it is very likely that in the coming decades, we could witness an increase in the incidence of male infertility due to mobile phone radiation exposure, similar to growing concerns over other hazards. Although the mechanism of cell phone radiation-mediated health defects is still obscure, it is proposed that their ability to produce heat, disrupt cell membranes, affect endothelial function, alter the blood-brain barrier, and modulate neuronal excitability have the potential to affect multiple physiological functions simultaneously28–30.
To our knowledge, this is the first meta-analysis of the effects of mobile phone radiations on various sperm quality parameters. Cellular phones have become integral part of everyday life, and newer versions of these are developed very rapidly these days. Hence, it is necessary to educate the users about the hazards of cell phones as well as test the newer versions like smartphones for health hazards.
Competing interests
No relevant competing interests were disclosed.
Grant information
The author(s) declared that no grants were involved in supporting this work.
Supplementary table
Supplementary Table 1. Effect sizes of sperm quality traits from the studies included in the analysis.
2. Matzuk MM, Lamb DJ: The biology of infertility: research advances and clinical challenges. Nat Med. 2008; 14(11): 1197–213. PubMed Abstract | Publisher Full Text
4. Davies MJ, Moore VM, Willson KJ, et al.: Reproductive technologies and the risk of birth defects. N Engl J Med. 2012; 366(19): 1803–13. PubMed Abstract | Publisher Full Text
5. Wen J, Jiang J, Ding C, et al.: Birth defects in children conceived by in vitro fertilization and intracytoplasmic sperm injection: a meta-analysis. Fertil Steril. 2012; 97(6): 1331–7.e1–4. PubMed Abstract | Publisher Full Text
6. Sage C, Carpenter D: BioInitiative Working G: BioInitiative report : a rationale for a biologically-based public exposure standard for electromagnetic fields (ELF and RF). [United States]: BioInitiative Working Group, 2007. Reference Source
7. Fejes I, Závaczki Z, Szöllosi J, et al.: Is there a relationship between cell phone use and semen quality? Arch Androl. 2005; 51(5): 385–93. PubMed Abstract | Publisher Full Text
8. World Bank. Information and Communication T, infoDev, World B. Maximizing mobile : 2012 information and communications for development. In. Washington, D.C.: World Bank: InfoDev. Reference Source
9. Ahlbom A, Green A, Kheifets L, et al.: Epidemiology of health effects of radiofrequency exposure. Environ Health Perspect. 2004; 112(17): 1741–54. PubMed Abstract | Publisher Full Text | Free Full Text
10. Myung SK, Ju W, McDonnell DD, et al.: Mobile phone use and risk of tumors: a meta-analysis. J Clin Oncol. 2009; 27(33): 5565–72. PubMed Abstract | Publisher Full Text
11. Agarwal A, Singh A, Hamada A, et al.: Cell phones and male infertility: a review of recent innovations in technology and consequences. Int Braz J Urol. 2011; 37(4): 432–54. PubMed Abstract
13. Wdowiak A, Wdowiak L, Wiktor H: Evaluation of the effect of using mobile phones on male fertility. Ann Agric Environ Med. 2007; 14(1): 169–72. PubMed Abstract
14. Agarwal A, Deepinder F, Sharma RK, et al.: Effect of cell phone usage on semen analysis in men attending infertility clinic: an observational study. Fertil Steril. 2008; 89(1): 124–8. PubMed Abstract | Publisher Full Text
15. Sajeda S, Al-Wattar YT: Effect of mobile phone usage on semen analysis in infertile men. Tikrit J Pharm Sci. 2011; 7(1): 77–82.
16. Erogul O, Oztas E, Yildirim I, et al.: Effects of electromagnetic radiation from a cellular phone on human sperm motility: an in vitro study. Arch Med Res. 2006; 37(7): 840–3. PubMed Abstract | Publisher Full Text
17. Falzone N, Huyser C, Fourie F, et al.: In vitro effect of pulsed 900 MHz GSM radiation on mitochondrial membrane potential and motility of human spermatozoa. Bioelectromagnetics. 2008; 29(4): 268–76. PubMed Abstract | Publisher Full Text
18. Ahmad L, Baig NM: Mobile Phone RF-EMW Exposure to Human Spermatozoa: An in vitro Study. Pakistan J Zool. 2011; 43(6): 1147–54. Reference Source
19. Dkhil MA, Danfour MA, Al-Quraishy S: Sperm function is affected by the electromagnetic radiation emitted by mobile phone. Afr J Microbiol Res. 2011; 5(27): 4896–900. Publisher Full Text
20. Agarwal A, Desai NR, Makker K, et al.: Effects of radiofrequency electromagnetic waves (RF-EMW) from cellular phones on human ejaculated semen: an in vitro pilot study. Fertil Steril. 2009; 92(4): 1318–25. PubMed Abstract | Publisher Full Text
21. Dasdag S, Ketani MA, Akdag Z, et al.: Whole-body microwave exposure emitted by cellular phones and testicular function of rats. Urol Res. 1999; 27(3): 219–23. PubMed Abstract
22. Stroup DF, Berlin JA, Morton SC, et al.: Meta-analysis of observational studies in epidemiology: a proposal for reporting. Meta-analysis Of Observational Studies in Epidemiology (MOOSE) group. JAMA. 2000; 283(15): 2008–12. PubMed Abstract | Publisher Full Text
24. Borenstein M, Hedges L, Higgins J, et al.: Comprehensive meta-analysis (Version 2) [Computer software]. Englewood, NJ BioStat, 2005.
25. Sutton AJ: Methods for meta-analysis in medical research. Chichester; New York: J. Wiley, 2000. Reference Source
26. Duval S, Tweedie R: A Nonparametric "Trim and Fill" Method of Accounting for Publication Bias in Meta-Analysis. J Am Statistical Assoc. 2000; 95(449): 89–98. Publisher Full Text
27. Orwin RG: A Fail-Safe N for Effect Size in Meta-Analysis. J Educational Statistics. 1983; 8(2): 157–59. Publisher Full Text
28. Straume A, Oftedal G, Johnsson A: Skin temperature increase caused by a mobile phone: a methodological infrared camera study. Bioelectromagnetics. 2005; 26(6): 510–9. PubMed Abstract | Publisher Full Text
29. Behari J: Biological responses of mobile phone frequency exposure. Indian J Exp Biol. 2010; 48(10): 959–81. PubMed Abstract
30. Juutilainen J, de Seze R: Biological effects of amplitude-modulated radiofrequency radiation. Scand J Work Environ Health. 1998; 24(4): 245–54. PubMed Abstract | Publisher Full Text
31. De Iuliis GN, Newey RJ, King BV, et al.: Mobile phone radiation induces reactive oxygen species production and DNA damage in human spermatozoa in vitro. PloS one. 2009; 4(7): e6446. PubMed Abstract | Publisher Full Text | Free Full Text
32. Falzone N, Huyser C, Becker P, et al.: The effect of pulsed 900-MHz GSM mobile phone radiation on the acrosome reaction, head morphometry and zona binding of human spermatozoa. Int J Androl. 2011; 34(1): 20–26. PubMed Abstract | Publisher Full Text
Dama MS and Bhat MN. Mobile phones affect multiple sperm quality traits: a meta-analysis [version 1; peer review: 2 approved, 1 approved with reservations] F1000Research 2013, 2:40 (https://doi.org/10.12688/f1000research.2-40.v1)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
track
receive updates on this article
Track an article to receive email alerts on any updates to this article.
Share
Open Peer Review
Current Reviewer Status: ?
Key to Reviewer Statuses VIEWHIDE
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
I confirm that I have read this submission and believe that I have an ... Continue reading
Competing Interests: No competing interests were disclosed.
I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.
NOTE: it is important to ensure the information in square brackets after the title is included in this citation.
Reviewer Report14 Mar 2013
Gary Klinefelter, Gamete and Early Embryo Biology Branch, Reproductive Toxicology Division, United States Environmental Protection Agency, Research Triangle Park, NC, USA
On the surface, the results seem quite striking with virtually any sperm endpoint one can imagine being significantly altered in the collective analysis of mobile phone studies compiled. However, upon looking at the data in the ... Continue reading
On the surface, the results seem quite striking with virtually any sperm endpoint one can imagine being significantly altered in the collective analysis of mobile phone studies compiled. However, upon looking at the data in the supplementary table, it is obvious that the relatively few studies compiled varied widely both in respect to endpoints measured and the sample size. As shown in Table 1, motility is the endpoint representing the greatest combined sample size for both in vivo and in vitro studies. Motility was measured in 4 out of 4 in vivo studies and 5 out of 7 in vitro studies. So motility ‘might’ be an endpoint that is repeatedly altered by cell phone exposure. The reason for ‘might’ is the lack of any reported exposure data in this study.
In summary, the small sample size and lack of exposure data significantly weaken the conclusions of this study.
Competing Interests: No competing interests were disclosed.
I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard, however I have significant reservations, as outlined above.
Madhukar Dama, Institute of Wildlife Veterinary Research, Kodagu District, Karnataka, India
02 Apr 2013
Author Response
We have studied the reviewer comments and would like to justify our results. Our analysis is showing that mobile phone radiations could affect many sperm parameters. This ... Continue readingWe have studied the reviewer comments and would like to justify our results. Our analysis is showing that mobile phone radiations could affect many sperm parameters. This could be due to interdependence of sperm parameters (Acta Eur Fertil. 1982;13(2):49-54). We also agree with the point that the number of studies is few and total sample size in in vitro studies is smaller. However, it must be noted that the sample size is weighted during meta-analysis, which nullifies the problems posed by smaller sample size studies. Apart from motility, other parameters like morphology, concentration, and viability are also significantly affected by in vivo exposure. Hence we have provided all the effect sizes individually along with p values and sample size. We hope that our points justify the reviewer comments.
We have studied the reviewer comments and would like to justify our results. Our analysis is showing that mobile phone radiations could affect many sperm parameters. This could be due to interdependence of sperm parameters (Acta Eur Fertil. 1982;13(2):49-54). We also agree with the point that the number of studies is few and total sample size in in vitro studies is smaller. However, it must be noted that the sample size is weighted during meta-analysis, which nullifies the problems posed by smaller sample size studies. Apart from motility, other parameters like morphology, concentration, and viability are also significantly affected by in vivo exposure. Hence we have provided all the effect sizes individually along with p values and sample size. We hope that our points justify the reviewer comments.
Madhukar Dama, Institute of Wildlife Veterinary Research, Kodagu District, Karnataka, India
02 Apr 2013
Author Response
We have studied the reviewer comments and would like to justify our results. Our analysis is showing that mobile phone radiations could affect many sperm parameters. This ... Continue readingWe have studied the reviewer comments and would like to justify our results. Our analysis is showing that mobile phone radiations could affect many sperm parameters. This could be due to interdependence of sperm parameters (Acta Eur Fertil. 1982;13(2):49-54). We also agree with the point that the number of studies is few and total sample size in in vitro studies is smaller. However, it must be noted that the sample size is weighted during meta-analysis, which nullifies the problems posed by smaller sample size studies. Apart from motility, other parameters like morphology, concentration, and viability are also significantly affected by in vivo exposure. Hence we have provided all the effect sizes individually along with p values and sample size. We hope that our points justify the reviewer comments.
We have studied the reviewer comments and would like to justify our results. Our analysis is showing that mobile phone radiations could affect many sperm parameters. This could be due to interdependence of sperm parameters (Acta Eur Fertil. 1982;13(2):49-54). We also agree with the point that the number of studies is few and total sample size in in vitro studies is smaller. However, it must be noted that the sample size is weighted during meta-analysis, which nullifies the problems posed by smaller sample size studies. Apart from motility, other parameters like morphology, concentration, and viability are also significantly affected by in vivo exposure. Hence we have provided all the effect sizes individually along with p values and sample size. We hope that our points justify the reviewer comments.
I confirm that I have read this submission and believe that I have an ... Continue reading
Competing Interests: No competing interests were disclosed.
I confirm that I have read this submission and believe that I have an appropriate level of expertise to confirm that it is of an acceptable scientific standard.
Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
Adjust parameters to alter display
View on desktop for interactive features
Includes Interactive Elements
View on desktop for interactive features
Competing Interests Policy
Provide sufficient details of any financial or non-financial competing interests to enable users to assess whether your comments might lead a reasonable person to question your impartiality. Consider the following examples, but note that this is not an exhaustive list:
Examples of 'Non-Financial Competing Interests'
Within the past 4 years, you have held joint grants, published or collaborated with any of the authors of the selected paper.
You have a close personal relationship (e.g. parent, spouse, sibling, or domestic partner) with any of the authors.
You are a close professional associate of any of the authors (e.g. scientific mentor, recent student).
You work at the same institute as any of the authors.
You hope/expect to benefit (e.g. favour or employment) as a result of your submission.
You are an Editor for the journal in which the article is published.
Examples of 'Financial Competing Interests'
You expect to receive, or in the past 4 years have received, any of the following from any commercial organisation that may gain financially from your submission: a salary, fees, funding, reimbursements.
You expect to receive, or in the past 4 years have received, shared grant support or other funding with any of the authors.
You hold, or are currently applying for, any patents or significant stocks/shares relating to the subject matter of the paper you are commenting on.
Stay Updated
Sign up for content alerts and receive a weekly or monthly email with all newly published articles
Comments on this article Comments (0)