Publication Cover
Human Fertility
an international, multidisciplinary journal dedicated to furthering research and promoting good practice
Volume 22, 2019 - Issue 2
323
Views
13
CrossRef citations to date
0
Altmetric
Review Article

Telomeres as a molecular marker of male infertility

, &
Pages 78-87 | Received 28 Jun 2017, Accepted 22 Jan 2018, Published online: 02 Apr 2018

References

  • Achi, M.V., Ravindranath, N., & Dym, M. (2000). Telomere length in male germ cells is inversely correlated with telomerase activity. Biology of Reproduction, 63, 591–598. doi: 10.1095/biolreprod63.2.591.
  • Agarwal, A., & Said, T.M. (2003). Role of sperm chromatin abnormalities and DNA damage in male infertility. Human Reproduction, 9, 331–345. doi: 10.1093/humupd/dmg027.
  • Aida, J., Izumiyama-Shimomura, N., Nakamura, K., Ishikawa, N., Terai, M., Matsuda, Y., … Takubo, K. (2014). Determination of telomere length by the quantitative fluorescence in situ hybridization (Q-FISH) method. American Journal of Analytical Chemistry, 5, 775–783. doi: 10.4236/ajac.2014.512086.
  • Allsopp, R.C., Vaziri, H., Patterson, C., Goldstein, S., Younglai, E.V., Futcher, A.B., … Harley, C.B. (1992). Telomere length predicts replicative capacity of human fibroblasts. Proceedings of the National Academy of Sciences, USA, 89, 10114–10118. Retrieved from http://www.pnas.org/content/89/21/10114.
  • Antunes, D.M., Kalmbach, K.H., Wang, F., Dracxler, R.C., Seth-Smith, M.L., Kramer, Y., … Keefe, D.L. (2015). 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. Journal of Assisted Reproduction and Genetics, 2, 1685–1690. doi: 10.1007/s10815-015-0574-3.
  • Armanios, M. (2009). Syndromes of telomere shortening. Annual Review of Genomics and Human Genetics, 10, 45–61. doi: 10.1146/annurev-genom-082908-150046.
  • Armanios, M., & Blackburn, E. (2012). The telomere syndromes. Nature Reviews. Genetics, 13, 693–704. doi: 10.1038/nrg3246.
  • Artandi, S., & De Pinho, R. (2010). Telomeres and telomerase in cancer. Carcinogenesis, 31, 9–18. doi: 10.1093/carcin/bgp268.
  • Aston, K.I., Hunt, S.C., Susser, E., Kimura, M., Factor-Litvak, P., Carrell, D., & Aviv, A. (2012). Divergence of sperm and leukocyte age-dependent telomere dynamics: Implications for male-driven evolution of telomere length in humans. Molecular Human Reproduction, 18, 517–522. doi: 10.1093/molehr/gas028.
  • Aubert, G., & Lansdorp, P. (2011). Telomeres and aging. Physiological Reviews, 88, 557–579. doi: 10.1152/physrev.00026.2007.
  • Aviv, A., Hunt, S.C., Lin, J., Cao, X., Kimura, M., & Blackburn, E. (2011). Impartial comparative analysis of measurement of leukocyte telomere length/DNA content by Southern blots and qPCR. Nucleic Acids Research, 39, e134–e165. doi: 10.1093/nar/gkr634.
  • Baird, D.M., Britt-Compton, B., Rowson, J., Amso, N.N., Gregory, L., & Kipling, D. (2006). Telomere instability in the male germline. Human Molecular Genetics, 15, 45–51. doi: 10.1093/hmg/ddi424.
  • Biron-Shental, T., Wiser, A., Hershko-Klement, A., Markovitch, O., Amiel, A., & Berkovitch, A. (2017). Subfertile sperm cells exemplify telomere dysfunction. Journal of Assisted Reproduction and Genetics, 35, 143–148. doi: 10.1007/s10815-017-1029-9.
  • Bongso, A., Jarina, A.K., Ho, J., Ng, S.C., & Ratnam, S.S. (1993). Comparative evaluation of three sperm-washing methods to improve sperm concentration and motility in frozen-thawed oligozoospermic and normozoospermic samples. Archives of Andrology, 31, 223–230. doi: 10.3109/01485019308988403.
  • Bower, K., Napier, C., Cole, S., Dagg, R., Lau, L., Duncan, E., … Reddel, R. (2012). Loss of wild-type ATRX expression in somatic cell hybrids segregates with activation of alternative lengthening of telomeres. PLoS One, 7, e50062. doi: 10.1093/hmg/ddi424.
  • Buxton, J., Suderman, M., Pappas, J., Borghol, N., McArdle, W., Blacemore, A., … Pembrey, M. (2014). Human leukocyte telomere length is associated with DNA methylation levels in multiple subtelomeric and imprinted laci. Scientific Reports, 4, 4954. doi: 10.1038/srep04954.
  • Cariati, F., Jaroudi, S., Alfarawati, S., Raberi, A., Alviggi, C., Pivonello, R., & Wells, D. (2016). Investigation of sperm telomere length as a potential marker of paternal genome integrity and semen quality. Reproductive Biomedicine Online, 33, 404–411. doi: 10.1016/j.rbmo.2016.06.006.
  • Cawthon, R. (2002). Telomere measurement by quantitative PCR. Nucleic Acids Research, 30, 47–53. doi: 10.1093/nar/30.10.e47.
  • Cawthon, R. (2009). Telomere measurement by the novel monochrome multiplex quantative PCR method. Nucleic Acids Research, 37, 21–28. doi: 10.1093/nar/gkn1027.
  • Chen, S., Lin, J., Matsuguchi, T., Blackburn, E., Yeh, F., Best, L.G., … Zhao, J. (2014). Short leukocyte telomere length predicts incidence and progression of carotid atherosclerosis in American Indians: The Strong Heart Family Study. Aging, 6, 414–427. doi: 10.18632/aging.100671.
  • Coluzzi, E., Colamartino, M., Cozzi, R., Leone, S., Meneghini, C., O'Callaghan, N., & Sgura, A. (2014). Oxidative stress induces persistent telomeric DNA damage responsible for nuclear morphology change in mammalian cells. Plos One, 9, 110963. doi: 10.1371/journal.pone.0110963.
  • Cooper, T.G., Noonan, E., Von Eckardstein, S., Auger, J., Baker, H.W.G., Behre, H.M., …Vogelsong, K.M. (2010). World Health Organization reference values for human semen characteristics. Human Reproduction Update, 16, 231–245. doi: 10.1093/humupd/dmp048.
  • Daniali, L., Benetos, A., Susser, E., Kark, J.D., Labat, C., Kimura, M., … Aviv, A. (2013). Telomeres shorten at equivalent rates in somatic tissues of adults. Nature Communications, 4, 1597. doi: 10.1038/ncomms2602.
  • De Frutos, C., López-Cardona, A.P., Fonseca-Balvís, N., Laguna-Barraza, R., Rizos, D., Gutierrez-Adán, A., & Bermejo-Álvarez, P. (2016). Spermatozoa telomeres determine telomere length in early embryos and offspring. Reproduction, 151, 1–7. doi: 10.1530/REP-15-0375.
  • De Lange, T. (2005). Shelterin: The protein complex that shapes and safeguards human telomeres. Genes & Development, 19, 2100–2110. doi: 10.1101/gad.1346005.
  • De Meyer, T., Rietzschel, E.R., De Buyzere, M.L., De Bacquer, D., Van Criekinge, W., Debacker, G.G., … Bekaert, S. (2007). Paternal age at birth is an important determinant of offspring telomere length. Human Molecular Genetics, 16, 3097–3102. doi: 10.1093/hmg/ddm271.
  • Dohle, G.R., Halley, D.J., Van Hemel, J.O., Van Den Ouwel, A.M., Pieters, M.H., Weber, R.F., & Govaerts, L.C. (2002). Genetic risk factors in infertile men with severe oligozoospermia and azoospermia. Human Reproduction, 17, 13–16. doi: 10.1093/humrep/17.1.13.
  • Draskovic, I., & Vallejo, A. (2013). Telomere recombination and alternative telomere lengthening mechanisms. Frontiers in Bioscience, 18, 1–20. doi: 10.2741/4084.
  • Dunson, D.B., Baird, D.D., & Colombo, B. (2004). Increased infertility with age in men and women. Obstetrics and Gynecology, 103, 51–56. doi: 10.1097/01.AOG.0000100153.24061.45.
  • Eisenberg, D.T.A., Hayes, M.G., & Kuzawa, C.W. (2012). Delayed paternal age of reproduction in humans is associated with longer telomeres across two generations of descendants. Proceedings of the National Academy of Sciences, 109, 10251–10256. doi: 10.1073/pnas.1202092109.
  • Eisenstein, M. (2011). Telomeres: All’s well that ends well. Nature, 478, 13–15. doi: 10.1038/478S13a.
  • Ferlin, A., Rampazzo, E., Rocca, M.S., Keppel, S., Frigo, A.C., De Rossi, A., & Foresta, C. (2013). In young men sperm telomere length is related to sperm number and parental age. Human Reproduction, 28, 3370–3376. doi: 10.1093/humrep/det392.
  • Ferreira, R.C., Braga, D.P., Bonetti, T.C., Pasqualotto, F.F., Iaconelli, A., & Borges, E. (2010). Negative influence of paternal age on clinical intracytoplasmic sperm injection cycle outcomes in oligozoospermic patients. Fertility and Sterility, 93, 1870–1874. doi: 10.1016/j.fertnstert.2008.12.043.
  • Franco, S., Alsheimer, M., Herrera, E., Benavente, R., & Blasco, M.A. (2002). Mammalian meiotic telomeres: Composition and ultrastructure in telomerase-deficient mice. European Journal of Cell Biology, 81, 335–340. doi: 10.1078/0171-9335-00259.
  • Gertler, R., Doll, D., Maak, M., Feith, M., & Rosenberg, R. (2008). Telomere length and telomerase subunits as diagnostic and prognostic biomarkers in Barrett carcinoma. Cancer, 112, 2173–2180. doi: 10.1002/cncr.23419.
  • Harris, I.D., Fronczak, C., Roth, L., & Meacham, R.B. (2011). Fertility and the aging male. Reviews in Urology, 13, 184–190. doi: 10.3909/riu0538.
  • Henkel, R.R., & Schill, W.B. (2003). Sperm preparation for ART. Reproductive Biology and Endocrinology, 1, 108. doi: 10.1186/1477-7827-1-108.
  • Hjelmborg, J.B., Dalgård, C., Mangino, M., Spector, T.D., Halekoh, U., Möller, S., … Aviv, A. (2015). Paternal age and telomere length in twins: The germ stem cell selection paradigm. Aging Cell, 14, 701–703. doi: 10.1111/acel.12334.
  • Hou, L.A., Blaser, M.J., Perez-Perez, G., Hoxha, M., Dioni, L., Pegoraro, V., … Baccarelli, A., (2009). Telomere length in peripheral leukocyte DNA and gastric cancer risk. Cancer Epidemiology, Biomarkers & Prevention, 18, 3103–3109. doi: 10.1158/1055-9965.EPI-09-0347.
  • Iommiello, V.M., Albani, E., Di Rosa, A., Marras, A., Menduni, F., Morreale, G., … Levi-Setti, P.E. (2015). Ejaculate oxidative stress is related with sperm DNA fragmentation and round cells. International Journal of Endocrinology, 2015, 321901. doi: 10.1155/2015/321901.
  • Jodczyk, S. (2011). Establishment and validation of a telomere length assay (Bachelor of biomedical sciences thesis). University of Otago, Christchurch, New Zealand. Retrieved from http://hdl.handle.net/10523/2056.
  • Jungwirth, A., Diemer, T., Dohle, G.R., Giwercman, A., Kopa, Z., Krausz, C., & Tournaye, H. (2015). Guidelines on male infertility. European Association of Urology, the Netherlands. Retrieved from http://www.uroweb.org/guidelines/male-infertility/.
  • Kalmbach, K.H., Fontes Antunes, D.M., Dracxler, R.C., Knier, T.W., Seth-Smith, M.L., Wang, F., … Keefe, D.L. (2013). Telomeres and human reproduction. Fertility and Sterility, 99, 23–29. doi: 10.1016/j.fertnstert.2012.11.039.
  • Kawanishi, S., & Oikawa, S. (2004). Mechanism of telomere shortening by oxidative stress. Annals of the New York Academy of Sciences, 1019, 278–284. doi: 10.1196/annals.1297.047.
  • Kimura, M., Stone, R., & Hun, S. (2010). Measurement of telomere length by the Southern blot analysis of terminal restriction fragment lengths. Nature Protocols, 5, 1596–1607. doi: 10.1038/nprot.2010.124.
  • Kozik, A., Bradbury, E.M., & Zalensky, A. (1998). Increased telomere size in sperm cells of mammals with long terminal (TTAGGG)n arrays. Molecular Reproduction and Development, 51, 98–104. doi: 10.1002/(SICI)1098-2795(199809)51:1 < 98::AID-MRD12 > 3.0.CO;2-Q.
  • Lafuente, R., Bosch-Rue, E., Ribas-Maynou, J., Alvarez, J., Brassesco, C., Amengual, M., … Brassesco, M. (2017). Sperm telomere length in motile sperm selection techniques: A qFISH approach. Andrologia, 50. Advance online publication. doi: 10.1111/and.12840.
  • Law, H., & Lau, Y. (2001). Validation and development of quantitative flow cytometry-based fluorescence in situ hybridization for intercenter comparison of telomere length measurement. Cytometry, 43, 150–153. doi: 10.1002/1097-0320(20010201)43:2 < 150::AID-CYTO1030 > 3.0.CO;2-H.
  • Lee, M., Hills, M., Conomos, D., Stutz, M., Dagg, R., Lau, L., … Pickett, H. (2013). Telomere extension by telomerase and ALT generates variant repeats by mechanistically distinct processes. Nucleic Acids Research, 42, 1733–1746. doi: 10.1093/nar/gkt1117.
  • Ling, X., Zhang, G., Chen, Q., Yang, H., Sun, L., Zhou, N., … Cao, J. (2016). 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. Environment International, 95, 79–85. doi: 10.1016/j.envint.2016.08.001.
  • Liu, L., Blasco, M., Trimarchi, J., & Keefe, D. (2002). An essential role for functional telomeres in mouse germ cells during fertilization and early development. Developmental Biology, 249, 74–84. doi: 10.1006/dbio.2002.0735.
  • Mahadevan, M.M., Leeton, J.F., Trounson, A.O., & Wood, C. (1985). Successful use of in vitro fertilization for patients with persisting lowquality semen. Annals of the New York Academy of Sciences, 442, 293–300. doi: 10.1111/j.1749-6632.1985.tb37531.x.
  • Mishra, S., Kumar, R., Malhotra, N., Singh, N., & Dada, R. (2016). Mild oxidative stress is beneficial for sperm telomere length maintenance. World Journal of Methodology, 6, 163–170. doi: 10.5662/wjm.v6.i2.163.
  • Mishra, S.S., Kumar, S., Singh, G., Mohanty, K., Vaid, S., Malhotra, N., … Dada, R. (2015). Oxidative DNA damage in male germ cells in normozoospermic infertile men: A case for concern. Austin Journal of Reproductive Medicine and Infertility, 2, 1017. Retrieved from http://austinpublishinggroup.com/reproductive-medicine/fulltext/ajrm-v2-id10-17.php.
  • Moohan, J.M., & Lindsay, K.S. (1995). Spermatozoa selected by a discontinuous Percoll density gradient exhibit better motion characteristics,more hyperactivation, and longer survival than direct swim-up. Fertility and Sterility, 64, 160–165. doi: 10.1016/S0015-0282(16)57673-0.
  • Moyzis, R., Buckingham, J., Cram, L., Dani, M., Deaven, L., Jones, M., … Wu, J.R. (1988). Highly conserved repetitive DNA sequence presents at the telomeres of human chromosomes. Proceedings of the National Academy of Sciences, 85, 6622–6626. Retrieved from http://www.pnas.org/content/85/18/6622.
  • Muraki, K., Nyhan, K., Han, L., & Murnane, J. (2012). Mechanisms of telomere loss and their consequences for chromosome instability. Frontiers in Oncology, 2, 135. doi: 10.3389/fonc.2012.00135.
  • Neidle, S., & Parkinson, G. (2003). The structure of telomeric DNA. Current Opinion in Structural Biology, 13, 275–283. doi: 10.1016/S0959-440X(03)00072-1.
  • Ng, K.K., Donat, R., Chan, L., Lalak, A., Di Pierro, I., & Handelsman, D.J. (2004). Sperm output of older men. Human Reproduction (Oxford, England), 19, 1811–1815. doi: 10.1093/humrep/deh315.
  • Njajou, O.T., Cawthon, R.M., Blackburn, E.H., Harris, T.B., Li, R., Sanders, J.L., … Hsueh, W.C. (2012). Shorter telomeres are associated with obesity and weight gain in the elderly. International Journal of Obesity, 36, 1176–1179. doi: 10.1038/ijo.2011.196.
  • O’Callaghan, N., & Fenech, M. (2011). A quantitative PCR method for measuring absolute telomere length. Biological Procedures Online, 13, 3. doi: 10.1186/1480-9222-13-3.
  • O’Sullivan, R., & Karlseder, J. (2010). Telomeres: Protecting chromosomes against genome instability. Nature Reviews Molecular Cell Biology, 11, 171–181. doi: 10.1038/nrm2848.
  • Ozturk, S. (2015). Telomerase activity and telomere length in male germ cells. Biology of Reproduction, 92, 53. doi: 10.1095/biolreprod.114.124008.
  • Pańczyszyn, A., & Boniewska-Bernacka, E. (2016). Telomery jako molekularny marker chorób cywilizacyjnych [Telomeres as a molecular marker of civilization diseases]. Postępy Biologii Komórki, 43, 141–154. Retrieved from http://pbkom.eu/en/volume/43.
  • Pickett, H.A., Henson, J.D., Au, A.Y., Neumann, A.A., & Reddel, R.R. (2011). Normal mammalian cells negatively regulate telomere length by telomere trimming. Human Molecular Genetics, 20, 4684–4692. doi: 10.1093/hmg/ddr402.
  • Podlevsky, J., & Chen, J. (2012). It all comes together at the ends: telomerase stricter, function and biogenesis. Mutation Research, 730, 3–11. doi: 10.1016/j.mrfmmm.2011.11.002.
  • Practice Committee of the American Society for Reproductive Medicine. (2015). Diagnostic evaluation of the infertile male: a committee opinion. Fertility and Sterility, 103, e18–e25. doi: 10.1016/j.fertnstert.2014.12.103.
  • Prowse, K.R., & Greider, C.W. (1995). Developmental and tissue-specific regulation of mouse telomerase and telomere length. Proceedings of the National Academy of Sciences, 92, 4818–4822. Retrieved from http://www.pnas.org/content/92/11/4818.long10.1073/pnas.92.11.4818.
  • Radwan, J., & Wołczyński S. (Eds) (2011). Niepłodność i rozród wspomagany [Infertility and assisted reproduction]. Warsaw, Poznań: Termedia Publishing.
  • Ramlau-Hansen, C.H., Thulstrup, A.M., Aggerholm, A.S., Jensen, M.S., Toft, G., & Bonde, J.P. (2007). Is smoking a risk factor for decreased semen quality? A cross-sectional analysis. Human Reproduction, 22, 188–196. doi: 10.1093/humrep/del364.
  • Reig-Viader, R., Capilla, L., Vila-Cejudo, M., Garcia, F., Anguita, B., Garcia-Caldes, M., & Ruiz-Herrera, A. (2014). Telomere homeostasis is compromised in spermatocytes from patients with idiopathic infertility. Fertility and Sterility, 102, 728–738. doi: 10.1016/j.fertnstert.2014.06.005.
  • Rocca, M.S., Speltra, E., Menegazzo, M., Garolla, A., Foresta, C., & Ferlin, A. (2016). Sperm telomere length as a parameter of sperm quality in normozoospermic men. Human Reproduction, 31, 1158–1163. doi: 10.1093/humrep/dew061.
  • Rode, L., Nordestgaard, B.G., Weischer, M., & Bojesen, S.E. (2014). Increased body mass index, elevated C-reactive protein, and short telomere length. Journal of Clinical Endocrinology and Metabolism, 99, 1671–1675. doi: 10.1210/jc.2014-1161.
  • Romano, G.H., Harari, Y., Yehuda, T., Podhorzer, A., Rubinstein, L., Shamir, R., … Kupiec, M. (2013). Environmental stresses disrupt telomere length homeostasis. PLoS Genetics, 9, e1003721. doi: 10.1371/journal.pgen.1003721.
  • Santiso, R., Tamayo, M., Gosalvez, J., Meseguer, M., Garridon, F., & Fernandez, J.L. (2010). Swim-up procedure selects spermatozoa with longer telomere length. Mutation Research, 688, 88–90. doi: 10.1016/j.fertnstert.2012.11.039.
  • Sharma, R., Agarwal, A., Rohra, V.K., Assidi, M., Abu-Elmagd, M., & Turki, R.F. (2015). Effects of increased paternal age on sperm quality, reproductive outcome and associated epigenetic risks to offspring. Reproductive Biology and Endocrinology, 19, 13–35. doi: 10.1186/s12958-015-0028-x.
  • Shuyuan, L., Changjun, Z., Haiying, P., Xiaoqin, H., Hao, S., Keqin, L., … Zhaoqing, Y. (2015). Association study of telomere length with idiopathic male infertility. Yi Chuan, 37, 1137–1142. doi: 10.16288/j.yczz.15-267.
  • Slijepcevic, P. (2001). Telomere length measurement by Q-FISH. Methods in Cell Science: An Official Journal of the Society for In Vitro Biology, 23, 17–22. doi: 10.1023/A:1013177128297.
  • Suder, A., Janusz, M., Jagielski, P., Głodzik, J., Pałka, T., Cisoń, T., & Pilch, W. (2015). Prevalence and risk factors of abdominal obesity in Polish rural children. Homo, 66, 357–368. doi: 10.1016/j.jchb.2014.09.008.
  • Tanemura, K., Ogura, A., Cheong, C., Gotoh, H., Matsumoto, K., Sato, E., … Kondo, T. (2005). Dynamic rearrangement of telomeres during spermatogenesis in mice. Developmental Biology, 281, 196–207. doi: 10.1016/j.ydbio.2005.02.025.
  • Thilagavathi, J., Kumar, M., Mishra, S.S., Venkatesh, S., Kumar, R., & Dada, R. (2013). Analysis of sperm telomere length in men with idiopathic infertility. Archives of Gynecology and Obstetrics, 287, 803–807. doi: 10.1007/s00404-012-2632-8.
  • Thilagavathi, J., Mishra, S.S., Kumar, M., Vemprala, K., Deka, D., Dhadwal, V., & Dada, R. (2013). Analysis of telomere length in couples experiencing idiopathic recurrent pregnancy loss. Journal of Assisted Reproduction and Genetics, 30, 793–798. doi: 10.1007/s10815-013-9993-1.
  • Turner, S., & Hartshorne, G.M. (2013). Telomere lengths in human pronuclei, oocytes and spermatozoa. Molecular Human Reproduction, 19, 510–518. doi: 10.1093/molehr/gat021.
  • Vagnini, L., Baruffi, R.L., Mauri, A.L., Petersen, C.G., Massaro, F.C., Pontes, A., … Franco, J.G. (2007). The effects of male age on sperm DNA damage in an infertile population. Reproductive Biomedicine Online, 15, 514–519. doi: 10.1016/S1472-6483(10)60382-3.
  • Valdes, A.M., Andrew, T., Gardner, J.P., Kimura, M., Oelsner, E., Cherkas, L.F., … Spector, T.D. (2005). Obesity, cigarette smoking, and telomere length in women. Lancet, 366, 662–664. doi: 10.1016/S0140-6736(05)66630-5.
  • Vecoli, C., Montano, L., Borghini, A., Notari, T., Guglielmino, A., Mercuri, A., … Andreassi, M.G. (2017). Effects of highly polluted environment on sperm telomere length: A pilot study. International Journal of Molecular Sciences, 18, 1703–1711. doi: 10.3390/ijms18081703.
  • Walczak-Jędrzejowska, R. (2015). Oxidative stress and male infertility. Advances in Andrology Online, 2, 5–15. Retrieved from http://www.postepyandrologii.pl/pdf/Walczak-Jendrzejowska_Renata_1.pdf.
  • Willeit, P., Raschenberger, J., Heydon, E.E., Tsimikas, S., Haun, M., Mayr, A., … Kiechl, S. (2014). Leucocyte telomere length and risk of type 2 diabetes mellitus: New prospective cohort study and literature-based meta-analysis. PLoS One, 9, e112483. doi: 10.1371/journal.pone.0112483.
  • World Health Organization. (2010). WHO laboratory manual for the examination and processing of human semen (5th ed.). Geneva: World Health Organization.
  • Wosnitzer, M.S. (2014). Genetic evaluation of male infertility. Translational Andrology and Urology, 3, 17–26. doi: 10.3978/j.issn.2223-4683.2014.02.04.
  • Wysoczańska, B. (2013). Zachowanie długości telomerów [Maintaining telomere length]. Postępy Higieny i Medycyny Doświadczalnej, 67, 1319–1330. doi: 10.5604/17322693.1081034.
  • Yang, Q., Zhang, N., Zhao, F., Zhao, W., Dai, S., Liu, J., … Sun, Y. (2015). Processing of semen by density gradient centrifugation selects spermatozoa with longer telomeres for assisted reproduction techniques. Reproductive Biomedicine Online, 31, 44–50. doi: 10.1016/j.rbmo.2015.02.016.
  • Yang, Q., Zhao, F., Dai, S., Zhang, N., Zhao, W., Bai, R., & Sun, Y. (2015). Sperm telomere length is positively associated with the quality of early embryonic development. Human Reproduction, 30, 1876–1881. doi: 10.1093/humrep/dev144.
  • Zegers-Hochschild, F., Adamson, G.D., De Mouzon, J., Ishihara, O., Mansour, R., Nygren, K., … Vanderpoel, S. (2009). International Committee for Monitoring Assisted Reproductive Technology (ICMART), World Health Organization (WHO). International Committee for Monitoring Assisted Reproductive Technology (ICMART) and the World Health Organization (WHO) revised glossary of ART terminology. Fertility and Sterility, 92, 1520–1524. doi: 10.1016/j.fertnstert.2009.09.009.
  • Zhao, F., Yang, Q., Shi, S., Luo, X., & Sun, Y. (2016). Semen preparation methods and sperm telomere length: density gradient centrifugation versus the swim up procedure. Scientific Reports, 6, 39051. doi: 10.1038/srep39051.
  • Zong, S., Wang, Z., Chen, H., & Cui, Y. (2014). Assessing telomere length using surface enhanced raman scattering. Scientific Reports, 4, 6977. doi: 10.1038/srep06977.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.