The association of female and male infertility with telomere length (Review)

Vasilopoulos,Eleni; Fragkiadaki,Persefoni; Kalliora,Charikleia; Fragou,Domniki; Docea,Anca Oana; Vakonaki,Elena; Tsoukalas,Dimitris; Calina,Daniela; Buga,Ana Maria; Georgiadis,George; Mamoulakis,Charalampos; Makrigiannakis,Antonios; Spandidos,Demetrios A.; Tsatsakis,Aristidis

doi:10.3892/ijmm.2019.4225

The association of female and male infertility with telomere length (Review)

Authors:
- Eleni Vasilopoulos
- Persefoni Fragkiadaki
- Charikleia Kalliora
- Domniki Fragou
- Anca Oana Docea
- Elena Vakonaki
- Dimitris Tsoukalas
- Daniela Calina
- Ana Maria Buga
- George Georgiadis
- Charalampos Mamoulakis
- Antonios Makrigiannakis
- Demetrios A. Spandidos
- Aristidis Tsatsakis
View Affiliations

Affiliations: Department of Biology, Temple University, Philadelphia, PA 19122, USA, Laboratory of Toxicology, Medical School, University of Crete, 71003 Heraklion, Greece, Department of Obstetrics and Gynecology, University of Pennsylvania, Philadelphia, PA 19104, USA, Laboratory of Forensic Medicine and Toxicology, School of Medicine, Aristotle University of Thessaloniki, 54124 Thessaloniki, Greece, Department of Toxicology, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania, Department of Clinical Pharmacy, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania, Department of Biochemistry, University of Medicine and Pharmacy of Craiova, 200349 Craiova, Romania, Department of Urology, University General Hospital of Heraklion, Medical School, University of Crete, 71003 Heraklion, Greece, Department of Obstetrics and Gynecology, University General Hospital of Heraklion, Medical School, University of Crete, 71003 Heraklion, Greece, Laboratory of Clinical Virology, School of Medicine, University of Crete, 71003 Heraklion, Greece
Published online on: May 31, 2019 https://doi.org/10.3892/ijmm.2019.4225
Pages: 375-389
Copyright: © Vasilopoulos et al. This is an open access article distributed under the terms of Creative Commons Attribution License.

Metrics: Total Views: 0 (Spandidos Publications: | PMC Statistics: )

Metrics: Total PDF Downloads: 0 (Spandidos Publications: | PMC Statistics: )

Cited By (CrossRef): 0 citations Loading Articles...

Abstract

Telomere length (TL) has long been associated with aging, as telomeres serve as protective caps of chromosomes, and are thus deeply involved in the preservation of genome integrity and are vital to cellular functions. Traditionally, a strong link connects aging and infertility in both sexes, with an earlier onset in females. Over the past decade, telomeres have attracted increasing attention due to the role they play in fertility. In this review, we investigated the potential positive or negative association between relative TL and different factors of female and male infertility. A systematic search of the PubMed database was conducted. Out of the 206 studies identified, 45 were reviewed as they fulfilled the criteria of validity and relevance. Following an analysis and a comparison of the study outcomes, several clear trends were observed. The majority of female infertility factors were associated with a shorter TL, with the exception of endometriosis, premature ovarian failure and clear cell carcinoma that were associated with a longer TL and polycystic ovary syndrome (PCOS), which revealed conflicting results among several studies, leading to ambiguous conclusions. Male infertility factors were associated with a shorter TL. Although this review can provide an outline of general trends in the association of TL with infertility factors, further epidemiological and original research studies are required to focus on investigating the basis of these varying lengths of telomeres.

View Figures

View References

1	Aghajanova L, Hoffman J, Mok-Lin E and Herndon CN: Obstetrics and gynecology residency and fertility needs. Reprod Sci. 24:428–434. 2017. View Article : Google Scholar
2	Center for Disease Control and Prevention: Assisted reproductive technology success rates: National summary and fertility clinic reports. 2016, http://www.cdc.gov/art/pdf/2016-report/ART-2016-National-Summary-Report.pdf.
3	Society for Assisted Reproductive Technology: National Summary Report. Society for Assisted Reproductive Technology; 2016, http://www.sartcorsonline.com/rptCSR_PublicMultYear.aspx?reportingYear=2016.
4	Agarwal A, Mulgund A, Hamada A and Chyatte MR: A unique view on male infertility around the globe. Reprod Biol Endocrinol. 13:372015. View Article : Google Scholar : PubMed/NCBI
5	Artini PG, Obino ME, Vergine F, Sergiampietri C, Papini F and Cela V: Assisted reproductive technique in women of advanced fertility age. Minerva Ginecol. 70:738–749. 2018. View Article : Google Scholar : PubMed/NCBI
6	Zhang WG, Zhu SY, Bai XJ, Zhao DL, Jian SM, Li J, Li ZX, Fu B, Cai GY, Sun XF, et al: Select aging biomarkers based on telomere length and chronological age to build a biological age equation. Age (Dordr). 36:96392014. View Article : Google Scholar
7	Pfeiffer V and Lingner J: Replication of telomeres and the regulation of telomerase. Cold Spring Harb Perspect Biol. 5:a0104052013. View Article : Google Scholar : PubMed/NCBI
8	Jones MJ, Goodman SJ and Kobor MS: DNA methylation and healthy human aging. Aging Cell. 14:924–932. 2015. View Article : Google Scholar : PubMed/NCBI
9	Rizvi S, Raza ST and Mahdi F: Telomere length variations in aging and age-related diseases. Curr Aging Sci. 7:161–167. 2014. View Article : Google Scholar
10	Tsatsakis A, Tsoukalas D, Fragkiadaki P, Vakonaki E, Tzatzarakis M, Sarandi E, Nikitovic D, Tsilimidos G and Alegakis AK: Developing BIOTEL: A semi-automated spreadsheet for estimating telomere length and biological age. Front Genet. 10:842019. View Article : Google Scholar : PubMed/NCBI
11	Petrakis D, Vassilopoulou L, Mamoulakis C, Psycharakis C, Anifantaki A, Sifakis S, Docea AO, Tsiaoussis J, Makrigiannakis A and Tsatsakis AM: Endocrine disruptors leading to obesity and related diseases. Int J Environ Res Public Health. 14:E12822017. View Article : Google Scholar : PubMed/NCBI
12	Mehrpour O, Karrari P, Zamani N, Tsatsakis AM and Abdollahi M: Occupational exposure to pesticides and consequences on male semen and fertility: A review. Toxicol Lett. 230:146–156. 2014. View Article : Google Scholar : PubMed/NCBI
13	Kalliora C, Mamoulakis C, Vasilopoulos E, Stamatiades GA, Kalafati L, Barouni R, Karakousi T, Abdollahi M and Tsatsakis A: Association of pesticide exposure with human congenital abnormalities. Toxicol Appl Pharmacol. 346:58–75. 2018. View Article : Google Scholar : PubMed/NCBI
14	Sifakis S, Androutsopoulos VP, Tsatsakis AM and Spandidos DA: Human exposure to endocrine disrupting chemicals: Effects on the male and female reproductive systems. Environ Toxicol Pharmacol. 51:56–70. 2017. View Article : Google Scholar : PubMed/NCBI
15	Katsikantami I, Sifakis S, Tzatzarakis MN, Vakonaki E, Kalantzi OI, Tsatsakis AM and Rizos AK: A global assessment of phthalates burden and related links to health effects. Environ Int. 97:212–236. 2016. View Article : Google Scholar : PubMed/NCBI
16	Yawson Emmanuel O, Obasi KK and Lawal I: Spermatogenic and spermatotoxic effects of Telfairia occidentalis (Ugu) aqueous leaves extract in adult male Wistar rats (Rattus novergicus). Toxicol Rep. 5:954–958. 2018. View Article : Google Scholar :
17	Acosta IB, Junior ASV, E Silva EF, Cardoso TF, Caldas JS, Jardim RD and Corcini CD: Effects of exposure to cadmium in sperm cells of zebrafish, Danio rerio. Toxicol Rep. 3:696–700. 2016. View Article : Google Scholar
18	Mello MSC, Delgado IF, Favareto APA, Lopes CMT, Batista MM, Kempinas WD and Paumgartten FJR: Sexual maturation and fertility of mice exposed to triphenyltin during prepubertal and pubertal periods. Toxicol Rep. 2:405–414. 2014. View Article : Google Scholar : PubMed/NCBI
19	Vakonaki E, Tzatzarakis M, Tsiminikaki K, Nathena D, Fragkiadaki P, Kalliantasi K, Kanaki K, Vaki G, Plaitis S, Tsoukalas D, et al: Effect of chronic and heavy drug abuse on biological aging. World Acad J Sci. 1:67–73. 2019.
20	Tsoukalas D, Fragkiadaki P, Docea AO, Alegakis AK, Sarandi E, Vakonaki E, Salataj E, Kouvidi E, Nikitovic D, Kovatsi L, et al: Association of nutraceutical supplements with longer telomere length. Int J Mol Med. 44:218–226. 2019.PubMed/NCBI
21	Shammas MA: Telomeres, lifestyle, cancer, and aging. Curr Opin Clin Nutr Metab Care. 14:28–34. 2011. View Article : Google Scholar
22	Valassi E, Crespo I, Santos A and Webb SM: Clinical consequences of Cushing's syndrome. Pituitary. 15:319–329. 2012. View Article : Google Scholar : PubMed/NCBI
23	Tedone E, Huang E, O'Hara R, Batten K, Ludlow AT, Lai TP, Arosio B, Mari D, Wright WE and Shay JW: Telomere length and telomerase activity in T cells are biomarkers of high-performing centenarians. Aging Cell. 18:e128592019. View Article : Google Scholar
24	Kordinas V, Ioannidis A and Chatzipanagiotou S: The telomere/telomerase system in chronic inflammatory Diseases Cause or effect? Genes (Basel). 7:E602016. View Article : Google Scholar
25	Chakravarthi BV, Nepal S and Varambally S: Genomic and epigenomic alterations in cancer. Am J Pathol. 186:1724–1735. 2016. View Article : Google Scholar : PubMed/NCBI
26	Moher D, Liberati A, Tetzlaff J and Altman DG; Group P; PRISMA Group: Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement. PLoS Med. 6:e10000972009. View Article : Google Scholar : PubMed/NCBI
27	Ma H, Zhou Z, Wei S, Liu Z, Pooley KA, Dunning AM, Svenson U, Roos G, Hosgood HD III, Shen M, et al: Shortened telomere length is associated with increased risk of cancer: A meta-analysis. PLoS One. 6:e204662011. View Article : Google Scholar : PubMed/NCBI
28	Haycock PC, Heydon EE, Kaptoge S, Butterworth AS, Thompson A and Willeit P: Leucocyte telomere length and risk of cardiovascular disease: Systematic review and meta-analysis. BMJ. 349. pp. g42272014, View Article : Google Scholar
29	Willeit P, Raschenberger J, Heydon EE, Tsimikas S, Haun M, Mayr A, Weger S, Witztum JL, Butterworth AS, Willeit J, et al: Leucocyte telomere length and risk of type 2 diabetes mellitus: New prospective cohort study and literature-based meta-analysis. PLoS One. 9:e1124832014. View Article : Google Scholar : PubMed/NCBI
30	Aviv A, Kark JD and Susser E: Telomeres, atherosclerosis, and human longevity: A causal hypothesis. Epidemiology. 26:295–299. 2015. View Article : Google Scholar : PubMed/NCBI
31	Zhang J, Rane G, Dai X, Shanmugam MK, Arfuso F, Samy RP, Lai MK, Kappei D, Kumar AP and Sethi G: Ageing and the telomere connection: An intimate relationship with inflammation. Ageing Res Rev. 25:55–69. 2016. View Article : Google Scholar
32	Parks CG, DeRoo LA, Miller DB, McCanlies EC, Cawthon RM and Sandler DP: Employment and work schedule are related to telomere length in women. Occup Environ Med. 68:582–589. 2011. View Article : Google Scholar : PubMed/NCBI
33	Valentijn AJ, Saretzki G, Tempest N, Critchley HO and Hapangama DK: Human endometrial epithelial telomerase is important for epithelial proliferation and glandular formation with potential implications in endometriosis. Hum Reprod. 30:2816–2828. 2015.PubMed/NCBI
34	Williams CD, Boggess JF, LaMarque LR, Meyer WR, Murray MJ, Fritz MA and Lessey BA: A prospective, randomized study of endometrial telomerase during the menstrual cycle. J Clin Endocrinol Metab. 86:3912–3917. 2001. View Article : Google Scholar : PubMed/NCBI
35	Hapangama DK, Turner MA, Drury J, Heathcote L, Afshar Y, Mavrogianis PA and Fazleabas AT: Aberrant expression of regulators of cell-fate found in eutopic endometrium is found in matched ectopic endometrium among women and in a baboon model of endometriosis. Hum Reprod. 25:2840–2850. 2010. View Article : Google Scholar : PubMed/NCBI
36	Kalyan S, Patel MS, Kingwell E, Côté HCF, Liu D and Prior JC: Competing factors link to bone health in polycystic ovary syndrome: Chronic low-grade inflammation takes a toll. Sci Rep. 7:34322017. View Article : Google Scholar : PubMed/NCBI
37	Miranda-Furtado CL, Ramos FK, Kogure GS, Santana-Lemos BA, Ferriani RA, Calado RT and Dos Reis RM: A nonrandomized trial of progressive resistance training intervention in women with polycystic ovary syndrome and its implications in telomere content. Reprod Sci. 23:644–654. 2016. View Article : Google Scholar
38	Pedroso DC, Miranda-Furtado CL, Kogure GS, Meola J, Okuka M, Silva C, Calado RT, Ferriani RA, Keefe DL and dos Reis RM: Inflammatory biomarkers and telomere length in women with polycystic ovary syndrome. Fertil Steril. 103:542–547.e2. 2015. View Article : Google Scholar
39	Turner S and Hartshorne GM: Telomere lengths in human pronuclei, oocytes and spermatozoa. Mol Hum Reprod. 19:510–518. 2013. View Article : Google Scholar : PubMed/NCBI
40	Pollack AZ, Rivers K and Ahrens KA: Parity associated with telomere length among US reproductive age women. Hum Reprod. 33:736–744. 2018. View Article : Google Scholar : PubMed/NCBI
41	Yu J, Berga SL, Zou W, Sun HY, Johnston-MacAnanny E, Yalcinkaya T, Sidell N, Bagchi IC, Bagchi MK and Taylor RN: Gap junction blockade induces apoptosis in human endometrial stromal cells. Mol Reprod Dev. 81:666–675. 2014. View Article : Google Scholar : PubMed/NCBI
42	Cheng EH, Chen SU, Lee TH, Pai YP, Huang LS, Huang CC and Lee MS: Evaluation of telomere length in cumulus cells as a potential biomarker of oocyte and embryo quality. Hum Reprod. 28:929–936. 2013. View Article : Google Scholar : PubMed/NCBI
43	Barha CK, Hanna CW, Salvante KG, Wilson SL, Robinson WP, Altman RM and Nepomnaschy PA: Number of children and telomere length in women: A prospective, longitudinal evaluation. PLoS One. 11:e01464242016. View Article : Google Scholar : PubMed/NCBI
44	Czamanski-Cohen J, Sarid O, Cwikel J, Douvdevani A, Levitas E, Lunenfeld E and Har-Vardi I: Cell-free DNA and telomere length among women undergoing in vitro fertilization treatment. J Assist Reprod Genet. 32:1697–1703. 2015. View Article : Google Scholar : PubMed/NCBI
45	Shalev I, Entringer S, Wadhwa PD, Wolkowitz OM, Puterman E, Lin J and Epel ES: Stress and telomere biology: A lifespan perspective. Psychoneuroendocrinology. 38:1835–1842. 2013. View Article : Google Scholar : PubMed/NCBI
46	Fragkiadaki P, Tsoukalas D, Fragkiadoulaki I, Psycharakis C, Nikitovic D, Spandidos DA and Tsatsakis AM: Telomerase activity in pregnancy complications (Review). Mol Med Rep. 14:16–21. 2016. View Article : Google Scholar : PubMed/NCBI
47	Perls TT, Alpert L and Fretts RC: Middle-aged mothers live longer. Nature. 389:1331997. View Article : Google Scholar : PubMed/NCBI
48	Sun F, Sebastiani P, Schupf N, Bae H, Andersen SL, McIntosh A, Abel H, Elo IT and Perls TT: Extended maternal age at birth of last child and women's longevity in the Long Life Family Study. Menopause. 22:26–31. 2015. View Article : Google Scholar
49	Fagan E, Sun F, Bae H, Elo I, Andersen SL, Lee J, Christensen K, Thyagarajan B, Sebastiani P, Perls T, et al Long Life Family Study: Telomere length is longer in women with late maternal age. Menopause. 24:497–501. 2017. View Article : Google Scholar :
50	Gray KE, Schiff MA, Fitzpatrick AL, Kimura M, Aviv A and Starr JR: Leukocyte telomere length and age at menopause. Epidemiology. 25:139–146. 2014. View Article : Google Scholar :
51	Hapangama DK, Turner MA, Drury JA, Martin-Ruiz C, Von Zglinicki T, Farquharson RG and Quenby S: Endometrial telomerase shows specific expression patterns in different types of reproductive failure. Reprod Biomed Online. 17:416–424. 2008. View Article : Google Scholar : PubMed/NCBI
52	Butts S, Riethman H, Ratcliffe S, Shaunik A, Coutifaris C and Barnhart K: Correlation of telomere length and telomerase activity with occult ovarian insufficiency. J Clin Endocrinol Metab. 94:4835–4843. 2009. View Article : Google Scholar : PubMed/NCBI
53	Treff NR, Su J, Taylor D and Scott RT Jr: Telomere DNA deficiency is associated with development of human embryonic aneuploidy. PLoS Genet. 7:e10021612011. View Article : Google Scholar : PubMed/NCBI
54	Xu X, Chen X, Zhang X, Liu Y, Wang Z, Wang P, Du Y, Qin Y and Chen ZJ: Impaired telomere length and telomerase activity in peripheral blood leukocytes and granulosa cells in patients with biochemical primary ovarian insufficiency. Hum Reprod. 32:201–207. 2017.
55	Kuhn E, Meeker A, Wang TL, Sehdev AS, Kurman RJ and Shih IeM: Shortened telomeres in serous tubal intraepithelial carcinoma: An early event in ovarian high-grade serous carcinogenesis. Am J Surg Pathol. 34:829–836. 2010. View Article : Google Scholar : PubMed/NCBI
56	Wei D, Xie J, Yin B, Hao H, Song X, Liu Q, Zhang C and Sun Y: Significantly lengthened telomere in granulosa cells from women with polycystic ovarian syndrome (PCOS). J Assist Reprod Genet. 34:861–866. 2017. View Article : Google Scholar : PubMed/NCBI
57	Wang C, Shen F, Zhu Y, Fang Y and Lu S: Telomeric repeat-containing RNA (TERRA) related to polycystic ovary syndrome (PCOS). Clin Endocrinol (Oxf). 86:552–559. 2017. View Article : Google Scholar
58	Li Q, Du J, Feng R, Xu Y, Wang H, Sang Q, Xing Q, Zhao X, Jin L, He L, et al: A possible new mechanism in the pathophysiology of polycystic ovary syndrome (PCOS): The discovery that leukocyte telomere length is strongly associated with PCOS. J Clin Endocrinol Metab. 99:E234–E240. 2014. View Article : Google Scholar
59	Li Y, Deng B, Ouyang N, Yuan P, Zheng L and Wang W: Telomere length is short in PCOS and oral contraceptive does not affect the telomerase activity in granulosa cells of patients with PCOS. J Assist Reprod Genet. 34:849–859. 2017. View Article : Google Scholar : PubMed/NCBI
60	Hapangama DK, Turner MA, Drury JA, Quenby S, Saretzki G, Martin-Ruiz C and Von Zglinicki T: Endometriosis is associated with aberrant endometrial expression of telomerase and increased telomere length. Hum Reprod. 23:1511–1519. 2008. View Article : Google Scholar : PubMed/NCBI
61	Sofiyeva N, Ekizoglu S, Gezer A, Yilmaz H, Kolomuc Gayretli T, Buyru N and Oral E: Does telomerase activity have an effect on infertility in patients with endometriosis? Eur J Obstet Gynecol Reprod Biol. 213:116–122. 2017. View Article : Google Scholar : PubMed/NCBI
62	Valentijn AJ, Palial K, Al-Lamee H, Tempest N, Drury J, Von Zglinicki T, Saretzki G, Murray P, Gargett CE and Hapangama DK: SSEA-1 isolates human endometrial basal glandular epithelial cells: Phenotypic and functional characterization and implications in the pathogenesis of endometriosis. Hum Reprod. 28:2695–2708. 2013. View Article : Google Scholar : PubMed/NCBI
63	Hanna CW, Bretherick KL, Gair JL, Fluker MR, Stephenson MD and Robinson WP: Telomere length and reproductive aging. Hum Reprod. 24:1206–1211. 2009. View Article : Google Scholar : PubMed/NCBI
64	Kuhn E, Meeker AK, Visvanathan K, Gross AL, Wang TL, Kurman RJ and Shih IeM: Telomere length in different histologic types of ovarian carcinoma with emphasis on clear cell carcinoma. Mod Pathol. 24:1139–1145. 2011. View Article : Google Scholar : PubMed/NCBI
65	Keefe DL, Liu L and Marquard K: Telomeres and aging-related meiotic dysfunction in women. Cell Mol Life Sci. 64:139–143. 2007. View Article : Google Scholar : PubMed/NCBI
66	Kalmbach KH, Antunes DM, Kohlrausch F and Keefe DL: Telomeres and female reproductive aging. Semin Reprod Med. 33:389–395. 2015. View Article : Google Scholar : PubMed/NCBI
67	Keefe DL and Liu L: Telomeres and reproductive aging. Reprod Fertil Dev. 21:10–14. 2009. View Article : Google Scholar : PubMed/NCBI
68	Yang Q, Zhao F, Dai S, Zhang N, Zhao W, Bai R and Sun Y: Sperm telomere length is positively associated with the quality of early embryonic development. Hum Reprod. 30:1876–1881. 2015. View Article : Google Scholar : PubMed/NCBI
69	Reig-Viader R, Capilla L, Vila-Cejudo M, Garcia F, Anguita B, Garcia-Caldés M and Ruiz-Herrera A: Telomere homeostasis is compromised in spermatocytes from patients with idiopathic infertility. Fertil Steril. 102:728–738.e1. 2014. View Article : Google Scholar : PubMed/NCBI
70	Yan L, Wu S, Zhang S, Ji G and Gu A: Genetic variants in telomerase reverse transcriptase (TERT) and telomerase-associated protein 1 (TEP1) and the risk of male infertility. Gene. 534:139–143. 2014. View Article : Google Scholar
71	Ferlin A, Rampazzo E, Rocca MS, Keppel S, Frigo AC, De Rossi A and Foresta C: In young men sperm telomere length is related to sperm number and parental age. Hum Reprod. 28:3370–3376. 2013. View Article : Google Scholar : PubMed/NCBI
72	Thilagavathi J, Kumar M, Mishra SS, Venkatesh S, Kumar R and Dada R: Analysis of sperm telomere length in men with idiopathic infertility. Arch Gynecol Obstet. 287:803–807. 2013. View Article : Google Scholar
73	Prescott J, Du M, Wong JY, Han J and De Vivo I: Paternal age at birth is associated with offspring leukocyte telomere length in the nurses' health study. Hum Reprod. 27:3622–3631. 2012. View Article : Google Scholar : PubMed/NCBI
74	Moskovtsev SI, Willis J, White J and Mullen JB: Disruption of telomere-telomere interactions associated with DNA damage in human spermatozoa. Syst Biol Reprod Med. 56:407–412. 2010. View Article : Google Scholar : PubMed/NCBI
75	Baird DM, Britt-Compton B, Rowson J, Amso NN, Gregory L and Kipling D: Telomere instability in the male germline. Hum Mol Genet. 15:45–51. 2006. View Article : Google Scholar
76	Biron-Shental T, Wiser A, Hershko-Klement A, Markovitch O, Amiel A and Berkovitch A: Sub-fertile sperm cells exemplify telomere dysfunction. J Assist Reprod Genet. 35:143–148. 2018. View Article : Google Scholar :
77	Vecoli C, Montano L, Borghini A, Notari T, Guglielmino A, Mercuri A, Turchi S and Andreassi MG: Effects of highly polluted environment on sperm telomere length: A Pilot Study. Int J Mol Sci. 18:E17032017. View Article : Google Scholar : PubMed/NCBI
78	Lafuente R, Bosch-Rue E, Ribas-Maynou J, Alvarez J, Brassesco C, Amengual MJ, Benet J, Garcia-Peiró A and Brassesco M: Sperm telomere length in motile sperm selection techniques: A qFISH approach. Andrologia. 50:e128402018. View Article : Google Scholar
79	Cariati F, Jaroudi S, Alfarawati S, Raberi A, Alviggi C, Pivonello R and Wells D: Investigation of sperm telomere length as a potential marker of paternal genome integrity and semen quality. Reprod Biomed Online. 33:404–411. 2016. View Article : Google Scholar : PubMed/NCBI
80	Mishra S, Kumar R, Malhotra N, Singh N and Dada R: Mild oxidative stress is beneficial for sperm telomere length maintenance. World J Methodol. 6:163–170. 2016. View Article : Google Scholar : PubMed/NCBI
81	Rocca MS, Speltra E, Menegazzo M, Garolla A, Foresta C and Ferlin A: Sperm telomere length as a parameter of sperm quality in normozoospermic men. Hum Reprod. 31:1158–1163. 2016. View Article : Google Scholar : PubMed/NCBI
82	Liu SY, Zhang CJ, Peng HY, Huang XQ, Sun H, Lin KQ, Huang K, Chu JY and Yang ZQ: Association study of telomere length with idiopathic male infertility. Yi Chuan. 37:1137–1142. 2015.In Chinese. PubMed/NCBI
83	Antunes DM, Kalmbach KH, Wang F, Dracxler RC, Seth-Smith ML, Kramer Y, Buldo-Licciardi J, Kohlrausch FB and Keefe DL: A single-cell assay for telomere DNA content shows increasing telomere length heterogeneity, as well as increasing mean telomere length in human spermatozoa with advancing age. J Assist Reprod Genet. 32:1685–1690. 2015. View Article : Google Scholar : PubMed/NCBI
84	Yang Q, Zhang N, Zhao F, Zhao W, Dai S, Liu J, Bukhari I, Xin H, Niu W and Sun Y: Processing of semen by density gradient centrifugation selects spermatozoa with longer telomeres for assisted reproduction techniques. Reprod Biomed Online. 31:44–50. 2015. View Article : Google Scholar : PubMed/NCBI
85	Yang Q, Luo X, Bai R, Zhao F, Dai S, Li F, Zhu J, Liu J, Niu W and Sun Y: Shorter leukocyte telomere length is associated with risk of nonobstructive azoospermia. Fertil Steril. 110:648–654.e1. 2018. View Article : Google Scholar : PubMed/NCBI
86	Heidary H, Pouresmaeili F, Mirfakhraie R, Omrani MD, Ghaedi H, Fazeli Z, Sayban S, Ghafouri-Fard S, Azargashb E and Shokri F: An association study between longitudinal changes of leukocyte telomere and the risk of azoospermia in a population of Iranian infertile men. Iran Biomed J. 22:231–236. 2018. View Article : Google Scholar : PubMed/NCBI
87	Jørgensen PB, Fedder J, Koelvraa S and Graakjaer J: Age-dependence of relative telomere length profiles during spermatogenesis in man. Maturitas. 75:380–385. 2013. View Article : Google Scholar : PubMed/NCBI
88	Pech MF, Garbuzov A, Hasegawa K, Sukhwani M, Zhang RJ, Benayoun BA, Brockman SA, Lin S, Brunet A, Orwig KE, et al: High telomerase is a hallmark of undifferentiated spermatogonia and is required for maintenance of male germline stem cells. Genes Dev. 29:2420–2434. 2015. View Article : Google Scholar : PubMed/NCBI
89	Ling X, Zhang G, Chen Q, Yang H, Sun L, Zhou N, Wang Z, Zou P, Wang X, Cui Z, et al: Shorter sperm telomere length in association with exposure to polycyclic aromatic hydrocarbons: Results from the MARHCS cohort study in Chongqing, China and in vivo animal experiments. Environ Int. 95:79–85. 2016. View Article : Google Scholar : PubMed/NCBI
90	Liu M, Hales BF and Robaire B: Effects of four chemotherapeutic agents, bleomycin, etoposide, cisplatin, and cyclophosphamide, on DNA damage and telomeres in a mouse spermatogonial cell line. Biol Reprod. 90:722014. View Article : Google Scholar : PubMed/NCBI
91	Dracxler RC, Oh C, Kalmbach K, Wang F, Liu L, Kallas EG, Giret MT, Seth-Smith ML, Antunes D, Keefe DL, et al: Peripheral blood telomere content is greater in patients with endometriosis than in controls. Reprod Sci. 21:1465–1471. 2014. View Article : Google Scholar : PubMed/NCBI