|Year : 2018 | Volume
| Issue : 2 | Page : 87-92
Sperm counts in Asian men: Reviewing the trend of past 50 years
Pallav Sengupta PhD 1, Sulagna Dutta1, Maiza Binti Tusimin2, Tulay Irez3, Elzbieta Krajewska-Kulak4
1 Department of Physiology, Faculty of Medicine, MAHSA University, Malaysia
2 Department of Obstetrics and Gynaecology, Faculty of Medicine and Health Sciences, University Putra Malaysia, Malaysia
3 Department of Histology and Embryology, Medical Faculty, Biruni University, Istanbul, Turkey
4 Department of Integrated Medical Care, Faculty of Health Sciences, Medical University of Bialystok, Bialystok, Poland
|Date of Submission||13-Dec-2017|
|Date of Decision||27-Dec-2017|
|Date of Acceptance||10-Jan-2018|
|Date of Web Publication||21-Mar-2018|
Department of Physiology, Faculty of Medicine, MAHSA University
Source of Support: None, Conflict of Interest: None
Objective: To reveal the trend in alterations of sperm counts in Asian men over the past 50 years. Methods: This study reviewed all the published reports to unveil the specific pattern of alterations of sperm concentrations in Asian men from 1965 till 2015. The time-related changes in sperm concentration were studied using linear regression analyses. Results: The present study elucidated the trend using the reports from Carlsen et al (1965-1990) and non-Carlsen studies published until 2015, on fertile Asian men. In the reports of Carlsen et al, no overall declining trend in Asian men (r = 0.509, P = 0.760) was observed during this tenure, but non- Carsen reports showed a significant time-dependent decline of sperm concentration (r = -0.754, P = 0.005) in Asian men. This present review also showed a mild time-dependant decline in sperm concentration (-0.44×106/mL/year, 95% CI: -0.65 to -0.23; r = -0.473, P = 0.040) which accounted for an overall 22.17% decrease in past 50 years. Conclusions: This study brings to the forefront that sperm concentration among Asian men follows a mild declining trend over the period of 50 years, and further studies addressing the causes of this decline are required.
Keywords: Asian men, Semen quality, Sperm concentration, Sperm count
|How to cite this article:|
Sengupta P, Dutta S, Tusimin MB, Irez T, Krajewska-Kulak E. Sperm counts in Asian men: Reviewing the trend of past 50 years. Asian Pac J Reprod 2018;7:87-92
|How to cite this URL:|
Sengupta P, Dutta S, Tusimin MB, Irez T, Krajewska-Kulak E. Sperm counts in Asian men: Reviewing the trend of past 50 years. Asian Pac J Reprod [serial online] 2018 [cited 2019 Aug 17];7:87-92. Available from: http://www.apjr.net/text.asp?2018/7/2/87/228018
| 1. Introduction|| |
The declining trend of semen quality over past few decades is one of the most concerned issues of men's health. This not only reflects upon male reproductive health but also indicates a threat to the mankind and upcoming generations as a whole. In 1974, Nelson and Bunge brought this alarming trend to the forefront for the first time. Then in 1992, in a report of 61 studies, Carlsen et al found a global diminution in sperm counts by about 50% between 1938 and 1990. In that study, they recorded significant declines in sperm count in the United States, Europe, and Australia with no such trend in non-Western countries. After this report, in 1997 Swan et al published a study where they reanalysed 56 studies confirming a significant deterioration in sperm density in the United States and Europe only. Further in 2000, in an analysis of 101 studies, Swan et al had established the decline of sperm concentration in the phase of 1934 to 1996. Subsequently in 2013, Rolland et al reported 32% diminution in sperm count between 1989 and 2005. A plentiful retrospective evaluations of laboratory semen records have indicated a decrease in semen quality as reported from Belgium, Canada, Finland, France, Greece, Norway, Scotland, the USA, and the UK, while no variations have been reported from regions such as Denmark, Israel and Australia. But, this is still unconvincing considering the global temporal trends.
The above discussed studies have helped to construct a portrait of the global trend of sperm concentration as well as the drift which research had been following to put forth such information. But whenever the orientation of the trend of sperm concentration among Asian men population comes to the forefront, it remains barely answerable as only a trivial number of such studies have been performed in non-Western countries including Asia. The first document regarding altered sperm concentration of Asian population after 1965 was put forth by Bhushan et al in 1978. During 1965-1977, there was no study recounting altering sperm concentration in Asian men, however, after 1978, several research articles began to emerge with retrospective analysis of sperm concentration. The first duration analysis was published by Benshushan et al in 1997 reporting semen quality of 188 subjects for the duration of 1980- 1995. Followed by this report, Zhang et al in 1999 reported semen quality of 9 292 Chinese fertile men for the duration of 1983- 1996, the report by Almagor et al in 2003 included 2 638 males from Jerusalem from the couples who attended infertility clinic for intrauterine insemination for the period of 1990-2000, Liang et al in 2008 reported semen quality of fertile 5 834 Chinese men for the duration of 1980-2005, the report by Haimov-Kochman et al in 2012 included the semen quality of 2 182 young, healthy, fertile Israeli men for the duration of 1995-2009 and very recently Huang et al in 2017 reported semen quality of 30 636 fertile Chinese men for the duration of 2001-2015. In the report of Huang et al, they have indicated a decline of sperm concentration from 68×106/mL to 47x106/mL is past 15 years.
Thus, from these scanty and scattered studies regarding Asian trend of sperm count, it can be perceived that it has become crucial on scientific as well as social perspectives to have clear information regarding the trend of altering sperm count among Asian men. Thus, the objective of this report is to build-up a considerable idea concerning the trend in alterations of sperm concentration in fertile Asian men by picking all the available reports, of Carlsen et al (for studies before 1990) and non-Carlsen new studies (post-1990), over 50 years, moulding them in sequential pattern.
| 2. Methods and materials|| |
Research articles on fertile men published in English-language from 1965 to 2015 had been considered. The data of Carlsen et al. i.e. reports from 1965 to 1990 and non-Carlsen new studies (post-1990, until 2015) were included. The study opted randomized selection criteria for reports on sperm concentration, with predefined standards for inclusion and exclusion, as follows: (1) Non-Carlsen studies between 1990 and 2015 were identified in electronic databases including Medline, National Library of Medicine, Bathesda, MD with the Medical Subject Headings key words: semen quality, sperm concentration, sperm count, sperm density and semen analysis; (2) Relevant literatures on variations of the sperm concentration were retrieved; (3) Studies involving fertile men aged between 17 and 55 years were considered; (4) Data of the infertile patients were excluded; (5) Studies with sample size (n) of less than five (n<5) were excluded. Following Meta-analyses of Observational Studies in Epidemiology guidelines and Preferred Reporting Items for Systematic Reviews and Meta-analyses checklist, the present study extracted the data using the above mentioned electronic databases. The present study recorded a total of 38 studies published between 1965 and 2015 regarding semen quality in Asian men from the above-mentioned databases. From these reports, a total of 27 studies were excluded: (1) with infertile men (n=6); (2) not dealing with sperm count (n=6); (3) in non-English language (n=2); (4) with less sample size (n=7); (5) interval studies recorded alteration in sperm count (n=6, [17,20-24]). In addition, two studies, from Carlsen et al were included. Thus, the present review was based on 13 Asian studies published between 1965 and 2015. In each case, the outcome of the report for sperm concentration was evaluated. The review applied univariate and multivariate linear regression analyses by weighted least squares method (for sample size) considering the entire data, and on studies from Carlsen et al and non-Carlsen separately. Statistical significance of trends, if any, was recorded.
| 3. Results|| |
The outcome of the 13 studies on alterations of sperm concentration in Asian men over the past 50 years was represented in [Table 1] [19,28-39]. Most of the reports were grounded upon andrology laboratories (48.85%), and others included epidemiological studies (38.56%) and data from healthy sperm donors (15.39%). Among the 13 published research studies discussed in this review article from 1965 to 2015, most were executed in India, China and Japan. Most of the studies had sample size of less than 500 men (61.54%) and four studies included sample size more than 1 000 men (30.76%). About 84.61% of these reports had data about age of the subjects; 92.30% had depicted significant decrease in sperm concentration from 1965 to 2015.
|Table 1: Studies on changes of sperm concentrations in Asia (1965-2015).|
Click here to view
Separate evaluation of Carlsen and non-Carlsen studies by univariate linear regression there was no significant change in Carlsen data from 1965-1995 among Asian men (r = 0.509, P = 0.760), but non-Carlsen data revealed a significant decline with time (r = -0.754, P = 0.005) [Figure 1]A. The study identified a timedependent declining trend in sperm concentration of -0.44 ×106/mL/ year (95% CI: -0.65 to -0.23; r = -0.473, P = 0.040) which accounted for an overall 22.17% decrease in mean sperm concentration in past 50 years [Figure 1]B.
|Figure 1: Sperm count.|
(A) Sperm count in Asian men in Carlsen and Non-Carlsen studies; (B) Trend sperm count with time in past 50 years. Bubble size corresponds to the number of men in the study.
Click here to view
[Figure 2] was describing the alterations in past five decades with the present World Health Organization (WHO) cut-off value of sperm concentration. It revealed that despite being higher than the WHO range, this declining trend should be considered as a matter of concern of fertility among Asian men.
|Figure 2: Changes in sperm concentrations ( ×106/mL) from 1965 to 2015 shown as box-and-Whisker plots.|
Click here to view
| 4. Discussion|| |
Review of the data of these studies suggests that the sperm concentration of Asian men is showing a mild declining trend in past 50 years, i.e., 1965-2015. It is also similar with the trends in regional findings from India,,,, China,, Israel, and Japan,. Carlsen et al reported the trend in all continents up to 1992, but there were very few studies on Asian population in that report within our selected range. These reports were not describing any significant trend in sperm concentration decline among Asian men. But while reviewing the non-Carlsen reports up to 2015, which were much higher in numbers, a very significant decline was observed. Most of these reports came up from India, China and Japan. Other studies, conducted in Thailand, Saudi Arabia, and Korea, also reported the same trend. Only one study from Israel failed to demonstrate a time-related decline in semen quality.
A very recent study on Chinese fertile men has shown that their sperm concentration has been decreasing over past 15 years. It declined from 68×106/mL to 47×106/mL from 2001 to 2015. One more very recent large-scale cross-sectional update on sperm concentrations of Japanese men, Iwamoto et al in 2013 reported a severe decline in sperm concentration in almost all provinces in Japan, including Sapporo, Osaka, Kanazawa and Fukuoka. They also reported that the present mean sperm concentration of Japanese was 18×106/mL which was very near to WHO reference value of 2010 (15×106/mL). Recently, one of the reports indicated a significant worldwide reduction in sperm concentration between 1980 and 2015 from 91.65 ×106/mL to 39.34 x106/mL (r = -0.313, P = 0.000 2). It has reflected almost 57% decline in sperm count worldwide from 1980. It also showed that recruitment of larger population for this type of study has been increased predominantly after 1995, which is also found in this study. The present study also reported declining trend of sperm count in Europe and Africa, which suggested the biologically meaningful declining trend in global sperm counts. Conversely, a recent review from Cocuzza and Esteves revealed that evidences of confirmation of global decline in semen parameters are not enough. Inquisitively, some analyses put forth that semen quality has neither declined nor remained steady, while slightly increased in the recent years,. Nonetheless, follow-up studies are essential to inspect whether the mentioned observation is an actual phenomenon or completely random variation. The possible causes of the decreasing sperm concentration were also mentioned. The increased frequency of abnormalities in male reproductive may reflect adverse effects of environmental or lifestyle factors, like occupational and environmental exposures, sexually transmitted diseases and medications,,,. These factors play a key role in determining reproductive health and can influence fertility. Spanning the last few decades, progressive changes have been observed in aspects of diet, lifestyle and environment owing to which incident of male infertility has reportedly enhanced. Lifestyle factors such as alcohol intake, tobacco smoking, smokeless tobacco chewing, use of some modern electronic gadget etc. have heavily adverse effect on general health. These may interfere with spermatogenesis, spermiogenesis, sperm motility, integrity of sperm DNA and chromatin, hormonal regulation or by decreasing the fertilizing capability of spermatozoa. In previous reports, the root causes of this trend in declining semen quality were also indicated, highlighting on the effects of several lifestyle factors on male reproductive health,,,. In 2006 Iwamoto et al specified that the low level of sperm concentration in fertile Japanese men may be the consequence of modifications in lifestyle or environmental factors. They also indicated the likelihood of ethnic differences owing to genetic variation or combinations.
The expansions and demanding agricultural and industrial activities worldwide, together with environmental abuse, are risk to the health of entire population. Recently, the effect of pollutants and occupational factors on reproductive health has been a matter of debate. Undeniably, environmental pollutants such as pesticides, lead, methylmercury, welding, endocrine-disrupting compounds, organic solvents, radiation, household glues, etc. may affect reproductive male function,,. Alteration of the male reproductive health may due to effects on the endocrine control of reproductive system, or by direct effect on spermatogenesis,. However, a likely mechanism leaded to undesirable pregnancy outcomes owing to paternal susceptibility to organic solvents affecting sperm DNA directly, generating mutations and chromosomal abnormalities. Mehta et al in 2006 reported the cause of azoospermia and oligozoospermia in Indian male by analyzing the sperm count data from four major cities of India. They reported exposure of high concentration of fluoride and pesticides in some parts of India causing decreased serum testosterone level in men which resulted in low sperm production among Indian men.
As is known, Asia is the continent with wide cultural diversity; it is very difficult to find out a single possible cause of this trend. It is not clearly perceived how do ethnic and genetic backgrounds lay their influence upon semen quality. But, the correlations between prevalence of testicular cancer and ethnicity, as well as testicular cancer and altered germ cell formation were well known. Though it has been published in a recent report that India and China has the lowest incidence of testicular cancer over last two decades, it is also known that other Asian countries are showing increasing trend of incidence of testicular cancer. Lower testis parenchymal weight, lower sex steroid levels and lower testosterone production rate have been reported as the most common contributors of low sperm concentration in Asian men. As testified by Iwamoto et al in 2013, Japanese men are suffering from low blood testosterone level and that is the major causative agent of low sperm concentration in Japanese men. Age is also one of the contributing factors. A recent study has shown age-related changes in semen quality in Chinese men. It reported that men with age of more than 35 are having less sperm concentration than younger men.
The conceivable drawbacks of this study are: (1) since retrospective studies were carried out using sperm concentrations data, information on potential confounders, such as food habits, smoking, occupation of the subjects, and level of stress, could not be procured; (2) as per Velde and Bonde in 2013 on decreasing sperm counts and fertility in Europe, the present study is not claiming this decrease in sperm concentration in Asian men is the sole cause of declining fertility rate of them. There are innumerable factors which can contribute to reduced fertility rate,,,. Thus, from this present study, it cannot correlate the contributing factors of declining sperm concentration in Asia in past 50 years as well as cannot claim this is the cause of decreasing fertility in Asian countries. Following this review, future prospective studies including representative samples addressing life-style, occupational and other related factors from each region in general population are required to be sanguine that whether sperm concentration is still deteriorating in Asian countries.
In conclusion, this review has converged the dispersed data from the published articles to show a mild declining trend of sperm count in Asian countries, demonstrating an overall 22.17% decline in sperm concentration in Asian men over past 50 years. Sperm concentration has been found to be declined from 51.4×106/mL to 40.0×106/mL. There are scarce evidences for the influence of environmental factors and life style on semen quality. This review implies the fertility status of Asian men and accentuates the necessity for further analytical reports focusing on life-style and other factors with the aim of finding the proper correlation of this declining trend of sperm count with the causative agents.
Conflict of interest statement
The authors declare that they have no conflict of interest.
| References|| |
Nelson CMK, Bunge RG. Semen analysis-evidence of changing parameters of male fertility potential. Fertil Steril
Carlsen E, Giwercman A, Keiding N, Skakkebaek NE. Evidence for decreasing quality of semen during past 50 years. Brit Med J
Swan SH, Elkin EP, Fenster L. Have sperm densities declined? A reanalysis of global trend data. Environ Health Perspect
Swan SH, Elkin EP, Fenster L. The question of declining sperm density revisited: An analysis of 101 studies published 1934-1996. Environ Health Perspect
Rolland M, Le Moal J, Wagner V, Royère D, De Mouzon J. Decline in semen concentration and morphology in a sample of 26 609 men close to general population between 1989 and 2005 in France. Hum Reprod
Van Waeleghem K, De Clercq N, Vermeulen L, Schoonjans F, Comhaire F. Deterioration of sperm quality in young healthy Belgian men. Hum Reprod
Younglai EV, Collins JA, Foster WG. Canadian semen quality: An analysis of sperm density among eleven academic fertility centers. Fertil Steril
Horte A, Vierula M, Toppari J, Suominen J. Reassessment of sperm morphology of archival semen smears from the period 1980-1994. Int J Androl
Auger J, Kunstmann JM, Czyglik F, Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N Engl J Med
Adamopoulos DA, Pappa A, Nicopoulou S, Andreou E, Karamertzanis M, Michopoulos J, et al. Seminal volume and total sperm number trends in men attending subfertility clinics in the greater Athens area during the period 1977-1993. Hum Reprod
Bendvold E. Semen quality in Norwegian men over a 20-year period. Int J Fertl
Irvine S, Cawood E, Richardson D, MacDonald E, Aitken J. Evidence of deteriorating semen quality in the United Kingdom: Birth cohort study in 577 men in Scotland over 11 years. BMJ
Leto S, Frensilli FJ. Changing parameters of donor semen. Fertil Steril
Swan SH, Brazil C, Drobinis EZ, Liu F, Kruse RL, Hatch M, et al. Geographic differences in semen quality of fertile US males. Environ Health Perspect
Ginsburg J, Okolo S, Prelevic G, Hardiman P. Residence in the London area and sperm density. Lancet
Rasmussen PE, Erb K, Westergaard LG, Laursen SB. No evidence for decreasing semen quality in four birth cohorts of 1 055 Danish men born between 1950 and 1970. Fertil Steril
Benshushan A, Shoshani O, Paltiel O, Schenker JG, Lewin A. Is there really a decrease in sperm parameters among healthy young men? A survey of sperm donations during 15 years. J Assist Reprod Genet
Handelsman DJ. Sperm output of healthy men in Australia: Magnitude of bias due to self-selected volunteers. Hum Reprod
Brushan S, Pandey RC, Singh SP, Pandey DN, Seth P. Some observations on human semen analysis. Indian J Physiol Pharmacol
Zhang SC, Wang HY, Wang JD. Analysis of change in sperm quality of Chinese fertile men during 1981-1996. Reprod Contracep
Almagor M, Ivnitzki I, Yaffe H, Baras M. Changes in semen quality in Jerusalem between 1990 and 2000: A cross-sectional and longitudinal study. Arch Androl
Liang XW, Lu WH, Chen ZW, Wang XH, Zhao H, Zhang GY, et al. Changes of semen parameters in Chinese fertile men in the past 25 years. Natl J Androl
Haimov-Kochman R, Har-Nir R, Ein-Mor E, Ben-Shoshan V, Greenfield C, Eldar I, et al. Is the quality of donated semen deteriorating? Findings from a 15-year longitudinal analysis of weekly sperm samples. Israel Med Assoc J
Huang C, Li B, Xu K, Liu D, Hu J, Yang Y, et al. Decline in semen quality among 30 636 young Chinese men from 2001 to 2015. Fertil Steril
Stroup DF, Berlin JA, Morton SC, Olkin I, Williamson GD, Rennie D, et al. Meta-analyes of observational studies in epidemiology: A proposal for reporting. JAMA
Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med
Johnson RA, Wichern DW. Applied multivariate statistical analysis
. New Jersey: Prentice-Hall; 2014.
Aribarg A, Kenkeerati W, Vorapaiboonsak V, Leepipatpaiboon S, Farley TMM. Testicular volume, semen profile and serum hormone levels in fertile Thai males. Int J Androl
Singer R, Sagiv M, Levinsky H, Allalouf D. Andrological parameters in men with high sperm counts and possible correlation with age. Arch Androl
Zhong CQ, Lui QL, Tang YJ, Wang Y, Shi FJ, Qian SZ. Study on sperm function in men long after cessation of gossypol treatment. Contraception
El-Shoura SM, Abdel AM, Ali ME, El-Said MM, Ali KZ, Kemeir MA, et al. Deleterious effects of khat addiction on semen parameters and sperm ultrastructure. Hum Reprod
Benshushan A, Shoshani O, Paltiel O, Schenker JG, Lewin A. Is there really a decrease in sperm parameters among healthy young men? A survey of sperm donations during 15 years. J Assist Reprod Genet
Marimuthu P, Kapilashrami MC, Misro MM, Singh G. Evaluation of trend in semen analysis for 11 years in subjects attending a fertility clinic in India. Asian J Androl
Pal PC, Rajalakshmi M, Manocha M, Sharma RS, Mittal S, Rao DN. Semen quality and sperm functional parameters in fertile Indian men. Andrologia
Iwamoto T, Nozawa S, Yoshiike M, Hoshino T, Baba K, Matsushita T, et al. Semen quality of 324 fertile Japanese men. Hum Reprod
Mukhopadhyay D, Varghese AC, Pal M, Banerjee SK, Bhattacharyya AK, Sharma RK, et al. Semen quality and age-specific changes: A study between two decades on 3 729 male partners of couples with normal sperm count and attending an andrology laboratory for infertility-related problems in an Indian city. Fertil Steril
Bahk JY, Jung JH, Jin LM, Min SK. Cut-off value of testes volume in young adults and correlation among testes volume, body mass index, hormonal level, and seminal profiles. Urology
Iwamoto T, Nozawa S, Yoshiike M, Namiki M, Koh E, Kanaya J, et al. Semen quality of fertile Japanese men: A cross-sectional population- based study of 792 men. BMJ Open
Tang YG, Tang LX, Wang QL, Song G, Jiang YJ, Deng SM, et al. The reference values for semen parameters of 1 213 fertile men in Guangdong province in China. Asian J Androl
Sengupta P, Dutta S, Krajewska-Kulak E. The disappearing sperms: Analysing the reports published between 1980 and 2015. Am J Mens Health
2017: 11(4): 1279-1304.
Sengupta P, Borges Jr E, Dutta S, Krajewska-Kulak E. Decline in sperm count in European men during the past 50 years. Hum Exp Toxicol
2017. doi: 10.1177/0960327117703690.
Sengupta P, Nwagha U, Dutta S, Krajewska-Kulak E, Izuka E. Evidence of decreasing sperm count in African population from 1965 to 2015. Afr Health Sci
Cocuzza M, Esteves SC. Shedding light on the controversy surrounding the temporal decline in human sperm counts: A systematic review. Sci World J
Andolz P, Bielsa MA, Vila J. Evolution of semen quality in north-eastern Spain: A study in 22 759 infertile men over a 36-year period. Hum Reprod
Sengupta P, Banerjee R. Environmental toxins: Alarming impacts of pesticides on male fertility. Hum Exp Toxicol
Sengupta P. Environmental and occupational exposure of metals and their role in male reproductive functions. Drug Chem Toxicol
Sengupta P. Current trends of male reproductive health disorders and the changing semen quality. Int J Prev Med
Sengupta P. Recent trends in male reproductive health problems. Asian J Pharm Clin Res
Mendiola J, Torres-Cantero AM, Moreno-Grau JM, Ten J, Roca M, Moreno-Grau S, et al. Exposure to environmental toxins in males seeking infertility treatment: A case-controlled study. Reprod Biomed Online
Mendola P, Messer LC, Rappazzo K. Science linking environmental contaminant exposures with fertility and reproductive health impacts in the adult female. Fertil Steril
(2 suppl): e81-94.
Sengupta P. Reviewing reports of semen volume and male ageing in last 33 years: From 1980 through 2013. Asian Pac J Reprod
Dutta S, Joshi KR, Sengupta P, Bhattacharya K. Unilateral and bilateral cryptorchidism and its effect on the testicular morphology, histology, accessory sex organs and sperm count in Laboratory Mice. J Hum Repro Sci
Sharpe RM, Irvine DS. How strong is the evidence of a link between environmental chemicals and adverse effects on human reproductive health? BMJ
Sengupta P, Agarwal A, Pogrebtskaya M, Roychoudhury S, Durairajanayagam D, Henkel R. Role of Withania somnifera
(Ashwagandha) in the management of male infertility. Reprod Biomed Online
2017; DOI: http://dx.doi.org/10.1016/j.rbmo.2017.11.007
Mehta RH, Makwana S, Ranga GM, Srinivasan RJ, Virk SS. Prevalences of oligozoospermia and azoospermia in male partners of infertile couples from different parts of India. Asian J Androl
Sarfati D, Shaw C, Blakely T, Atkinson J, Stanley J. Ethnic and socioenonomic trends in testicular cancer incidence in New Zealand. Int J Cancer
Shanmugalingam T, Soultati A, Chowdhury S, Rudman S, Hemelrijck MV. Global incidence and outcome of testicular cancer. Clin Epidemiol
Beri A, Matzkin H, Liphshitz I, Barchana M. Epidemiological characteristics and trends of testicular cancer in Israel in 1992-2002. Harefuah
Zhu Q, Meads C, Lu M, Wu J, Zhou W, Gao E. Turning point of age for semen quality: A population based study in Chinese men. Fertil Steril
Velde ER, Bonde JP. Misconceptions about falling sperm counts and fertility in Europe. Asian J Androl
Bhattarai T, Chaudhuri P, Bhattacharya K, Sengupta P. Effect of progesterone supplementation on post-coital unilaterally ovariectomized superovulated mice in relation to implantation and pregnancy. Asian J Pharm Clin Res
Sengupta P, Banerjee R, Nath S, Das S, Banerjee S. Metals and female reproductive toxicity. Hum Exp Toxicol
Krajewska-Kulak E, Sengupta P. Thyroid function in male infertility. Front Endocrinol
[Figure 1], [Figure 2]