Cited by 109Sperm and Testicular FunctionReproductive Biology and FertilityReproductive biology and impacts on aquatic species

The DOI matches its Crossref record; 117 of the 120 references it cites were found in a registry or an index.

Ageing of the male germ line

Paul, Catriona, Robaire, Bernard·2013·Nature Reviews Urology

DOI 10.1038/nrurol.2013.18

Open this paper in CoChat — free account

Abstract

Several studies have demonstrated a decline in the male reproductive system, sperm quality, and fertility with advancing paternal age, yet many of the biological mechanisms that underlie this process remain poorly understood. It is unclear whether the problem arises from the progenitor spermatogonial stem cells (for example, from an accumulation of DNA damage and mutations), from the somatic niche present in the testis (consisting of Sertoli and peritubular myoid cells), or from a combination of the two. Current data, albeit from a small number of studies, suggest that both factors have a role in age-associated germ cell loss. What is clear, on the other hand, is that mounting evidence links paternal age to chromosomal damage and genetic problems in the children of older fathers. The frequency of de novo mutations increases markedly with age, leading to increased risk of breast cancer, cardiac defects, developmental disorders, behavioural disorders, and neurological disease in the children of older men. The current trend towards fathering children at a later age raises concerns regarding the risk of offspring developing complex multigene diseases.

Integrity signals

Registry

Crossref · 10.1038/nrurol.2013.18

Cites

117 of 117 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Instability and decay of the primary structure of DNA
Lindahl, T. (1993) · Nature · doi:10.1038/362709a0 · Cited by 5,679
Rate of de novo mutations and the importance of father’s age to disease risk
Kong, A., Frigge, M. L., Masson, G., Besenbacher, S., Sulem, P., Magnusson, G., Gudjonsson, S. A., Sigurdsson, A., Jonasdottir, A., Jonasdottir, A., et al. (2012) · Nature · doi:10.1038/nature11396 · Cited by 2,134
Alternative reading frames of the INK4a tumor suppressor gene encode two unrelated proteins capable of inducing cell cycle arrest
Ouelle, D. E., Zindy, F., Ashmun, R. A., & Sherr, C. J. (1995) · Cell · doi:10.1016/0092-8674(95)90214-7 · Cited by 1,485
Cell intrinsic alterations underlie hematopoietic stem cell aging
Rossi, D. J., Bryder, D., Zahn, J. M., Ahlenius, H., Sonu, R., Wagers, A. J., & Weissman, I. L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503280102 · Cited by 1,152
Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa
Aitken, R. J., & Clarkson, J. S. (1987) · Reproduction · doi:10.1530/jrf.0.0810459 · Cited by 1,020
Increasing p16INK4a expression decreases forebrain progenitors and neurogenesis during ageing
Molofsky, A. V., Slutsky, S. G., Joseph, N. M., He, S., Pardal, R., Krishnamurthy, J., Sharpless, N. E., & Morrison, S. J. (2006) · Nature · doi:10.1038/nature05091 · Cited by 972
The origins, patterns and implications of human spontaneous mutation
Crow, J. F. (2000) · Nature Reviews Genetics · doi:10.1038/35049558 · Cited by 928
Age-dependent DNA methylation of genes that are suppressed in stem cells is a hallmark of cancer
Teschendorff, A. E., Menon, U., Gentry-Maharaj, A., Ramus, S. J., Weisenberger, D. J., Shen, H., Campan, M., Noushmehr, H., Bell, C. G., Maxwell, A. P., et al. (2010) · Genome Research · doi:10.1101/gr.103606.109 · Cited by 855
Regulation of the INK4b–ARF–INK4a tumour suppressor locus: all for one or one for all
Gil, J., & Peters, G. (2006) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1987 · Cited by 843
Relative Impact of Oxidative Stress on the Functional Competence and Genomic Integrity of Human Spermatozoa1
Aitken, R. J., Gordon, E., Harkiss, D., Twigg, J., MILNE, P. A., Jennings, Z., & Irvine, D. S. (1998) · Biology of Reproduction · doi:10.1095/biolreprod59.5.1037 · Cited by 795
Human aging-associated DNA hypermethylation occurs preferentially at bivalent chromatin domainsPreprint
Rakyan, V. K., Down, T. A., Maslau, S., Andrew, T., Yang, T.-P., Beyan, H., Whittaker, P., McCann, O. T., Finer, S., Valdes, A. M., et al. (2010) · Genome Research · doi:10.1101/gr.103101.109 · Cited by 746
Effects of male age on semen quality and fertility: a review of the literature
Kidd, S. A., Eskenazi, B., & Wyrobek, A. J. (2001) · Fertility and Sterility · doi:10.1016/s0015-0282(00)01679-4 · Cited by 703
Births: final data for 2009.
Martin, J. A., Hamilton, B. E., Ventura, S. J., Osterman, M. J. K., Kirmeyer, S., Mathews, T. J., & Wilson, E. C. (2011) · PubMed · Cited by 700
The cycle of the seminiferous epithelium in man
Clermont, Y. (1963) · American Journal of Anatomy · doi:10.1002/aja.1001120103 · Cited by 682
Widespread and tissue specific age-related DNA methylation changes in mice
Maegawa, S., Hinkal, G., Kim, H. S., Shen, L., Zhang, L., Zhang, J., Zhang, N., Liang, S., Donehower, L. A., & Issa, J.-P. J. (2010) · Genome Research · doi:10.1101/gr.096826.109 · Cited by 553
Sperm DNA fragmentation: paternal effect on early post-implantation embryo development in ART
Borini, A., Tarozzi, N., Bizzaro, D., Bonu, M. A., Fava, L., Flamigni, C., & Coticchio, G. (2006) · Human Reproduction · doi:10.1093/humrep/del251 · Cited by 462
Effects of age on DNA double-strand breaks and apoptosis in human sperm
Singh, N. P., MULLER, C. H., & Berger, R. E. (2003) · Fertility and Sterility · doi:10.1016/j.fertnstert.2003.04.002 · Cited by 448
Advancing paternal age and risk of autism: new evidence from a population-based study and a meta-analysis of epidemiological studies
Hultman, C. M., Sandin, S., Levine, S. Z., Lichtenstein, P., & Reichenberg, A. (2011) · Molecular Psychiatry · doi:10.1038/mp.2010.121 · Cited by 444
Impact of aging on DNA methylation
Richardson, B. (2003) · Ageing Research Reviews · doi:10.1016/s1568-1637(03)00010-2 · Cited by 429
Human DNA repair genes, 2005
Wood, R. D., Mitchell, M., & Lindahl, T. L. (2005) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/j.mrfmmm.2005.03.007 · Cited by 428
Advancing age has differential effects on DNA damage, chromatin integrity, gene mutations, and aneuploidies in sperm
Wyrobek, A. J., Eskenazi, B., Young, S., Arnheim, N., Tiemann‐Boege, I., Jabs, E. W., Glaser, R. L., Pearson, F. S., & Evenson, D. P. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0506468103 · Cited by 402
Oxidative damage to DNA in human spermatozoa does not preclude pronucleus formation at intracytoplasmic sperm injection
Twigg, J., Irvine, D. S., & Aitken, R. J. (1998) · Human Reproduction · doi:10.1093/humrep/13.7.1864 · Cited by 380
Development of an Image Analysis System to Monitor the Retention of Residual Cytoplasm by Human Spermatozoa: Correlation With Biochemical Markers of the Cytoplasmic Space, Oxidative Stress, and Sperm Function
Gómez, E., Buckingham, D. W., Brindle, J., Lanzafame, F., Irvine, D. S., & Aitken, R. J. (1996) · Journal of Andrology · doi:10.1002/j.1939-4640.1996.tb01783.x · Cited by 375
Long-Term Effects of Mouse Intracytoplasmic Sperm Injection with DNA-Fragmented Sperm on Health and Behavior of Adult Offspring1
Fernández‐González, R., Moreira, P. N., Pérez-Crespo, M., Sánchez‐Martín, M., Ramírez, M. Á., Pericuesta, E., Bilbao, A., Bermejo‐Álvarez, P., Hourcade, J. D. D., de Fonseca, F. R., et al. (2008) · Biology of Reproduction · doi:10.1095/biolreprod.107.065623 · Cited by 366
Paternal Age Effect Mutations and Selfish Spermatogonial Selection: Causes and Consequences for Human Disease
Goriely, A., & Wilkie, A. O. M. (2012) · The American Journal of Human Genetics · doi:10.1016/j.ajhg.2011.12.017 · Cited by 365
Rare congenital disorders, imprinted genes, and assisted reproductive technology
Gosden, R. G., Trasler, J. M., Lucifero, D., & Faddy, M. J. (2003) · The Lancet · doi:10.1016/s0140-6736(03)13592-1 · Cited by 360
PARENTAL AGE AND MUTATION
Penrose, L. S. (1955) · The Lancet · doi:10.1016/s0140-6736(55)92305-9 · Cited by 348
A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation
Aitken, R. J., Harkiss, D., Knox, W., Paterson, M., & Irvine, D. S. (1998) · Journal of Cell Science · doi:10.1242/jcs.111.5.645 · Cited by 331
Effect of male age on fertility: evidence for the decline in male fertility with increasing age
Hassan, M. A. M., & Killick, S. R. (2003) · Fertility and Sterility · doi:10.1016/s0015-0282(03)00366-2 · Cited by 311
A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa
de Lamirande, E., & Gagnon, C. (1993) · International Journal of Andrology · doi:10.1111/j.1365-2605.1993.tb01148.x · Cited by 307
Antioxidant system in rat testicular cells
Bauché, F., Fouchard, M.-H., & Jégou, B. (1994) · FEBS Letters · doi:10.1016/0014-5793(94)00709-8 · Cited by 300
Paternal age and schizophrenia: a population based cohort study
Sipos, A., Rasmussen, F. E., Harrison, G. L., Tynelius, P., Lewis, G., Leon, D. A., & Gunnell, D. (2004) · BMJ · doi:10.1136/bmj.38243.672396.55 · Cited by 292
Offspring's Leukocyte Telomere Length, Paternal Age, and Telomere Elongation in Sperm
Kimura, M., Cherkas, L. F., Kato, B. S., Demissie, S., Hjelmborg, J., Brimacombe, M. B., Cupples, L. A., Hunkin, J., Gardner, J. P., Lu, X., et al. (2005) · PLoS Genetics · doi:10.1371/journal.pgen.0040037 · Cited by 280
Decline in Self-Renewal Factors Contributes to Aging of the Stem Cell Niche in the Drosophila Testis
Boyle, M., Wong, C., Rocha, M., & Jones, D. L. (2007) · Cell Stem Cell · doi:10.1016/j.stem.2007.08.002 · Cited by 268
Increasing paternal age is associated with delayed conception in a large population of fertile couples: evidence for declining fecundity in older men
Ford, W. C. L. (2000) · Human Reproduction · doi:10.1093/humrep/15.8.1703 · Cited by 267
Effects of Aging and Niche Microenvironment on Spermatogonial Stem Cell Self-Renewal
Ryu, B.-Y., Orwig, K. E., Oatley, J. M., Avarbock, M. R., & Brinster, R. L. (2006) · Stem Cells · doi:10.1634/stemcells.2005-0580 · Cited by 265
Advancing Paternal Age and Bipolar Disorder
Frans, E. M., Sandin, S., Reichenberg, A., Lichtenstein, P., Långström, N., & Hultman, C. M. (2008) · Archives of General Psychiatry · doi:10.1001/archpsyc.65.9.1034 · Cited by 249
Male age negatively impacts embryo development and reproductive outcome in donor oocyte assisted reproductive technology cycles
Frattarelli, J. L., Miller, K. A., Miller, B. T., Elkind-Hirsch, K. E., & Scott, R. T. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2007.06.009 · Cited by 243
The effects of male age on sperm DNA damage in healthy non-smokers
Schmid, T. E., Eskenazi, B., Baumgartner, A., Marchetti, F., Young, S., Weldon, R. H., Anderson, D. C., & Wyrobek, A. J. (2006) · Human Reproduction · doi:10.1093/humrep/del338 · Cited by 236
Parent-of-origin effects in multiple endocrine neoplasia type 2B.
Carlson, K. M., Bracamontes, J. R., Jackson, C. E., Clark, R., Lacroix, A., Wells, S. A., & Goodfellow, P. J. (1994) · PubMed Central · Cited by 229
DNA repair mechanisms and gametogenesis
Baarends, W. M., van der Laan, R., & Grootegoed, J. A. (2001) · Reproduction · doi:10.1530/rep.0.1210031 · Cited by 220
Fathers over 40 and increased failure to conceive: the lessons of in vitro fertilization in France
Rochebrochard, É. D. L., de Mouzon, J., Thépot, F., & Thonneau, P. F. (2006) · Fertility and Sterility · doi:10.1016/j.fertnstert.2005.11.040 · Cited by 216
Reproductive aging in the male brown-Norway rat: a model for the human
Wang, C., Leung, A., & Sinha‐Hikim, A. P. (1993) · Endocrinology · doi:10.1210/endo.133.6.8243304 · Cited by 212
Activating mutations in FGFR3 and HRAS reveal a shared genetic origin for congenital disorders and testicular tumors
Goriely, A., Hansen, R. M. S., Taylor, I. B., Olesen, I. A., Jacobsen, G. K., McGowan, S. J., Pfeifer, S. P., McVean, G. A. T., Meyts, E. R.-D., & Wilkie, A. O. M. (2009) · Nature Genetics · doi:10.1038/ng.470 · Cited by 205
Paternal Origin of FGFR2 Mutations in Sporadic Cases of Crouzon Syndrome and Pfeiffer Syndrome
Glaser, R. L., Jiang, W. G., Boyadjiev, S. A., Tran, A. K., Zachary, A. A., Maldergem, L. V., Johnson, D., Walsh, S., Oldridge, M., Wall, S. A., et al. (2000) · The American Journal of Human Genetics · doi:10.1086/302831 · Cited by 205
Delayed paternal age of reproduction in humans is associated with longer telomeres across two generations of descendants
Eisenberg, D. T. A., Hayes, M. G., & Kuzawa, C. W. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1202092109 · Cited by 199
Statement on guidance for genetic counseling in advanced paternal age
Toriello, H. V., & Meck, J. M. (2008) · Genetics in Medicine · doi:10.1097/gim.0b013e318176fabb · Cited by 194
Aging results in hypermethylation of ribosomal DNA in sperm and liver of male rats
Oakes, C. C., Smiraglia, D. J., Plass, C., Trasler, J. M., & Robaire, B. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437971100 · Cited by 185
Self-citation
Spermatogenesis and Aging in the Human
Johnson, L. W. (1986) · Journal of Andrology · doi:10.1002/j.1939-4640.1986.tb00943.x · Cited by 177
Age‐Related Decreased Leydig Cell Testosterone Production in the Brown Norway Rat
CHEN, H., Hardy, M. P., Huhtaniemi, I. T., & Zirkin, B. R. (1994) · Journal of Andrology · doi:10.1002/j.1939-4640.1994.tb00498.x · Cited by 171
Effect of paternal age in achondroplasia, thanatophoric dysplasia, and osteogenesis imperfecta
Orioli, I. M., Castilla, E. E., Scarano, G., & Mastroiacovo, P. (1995) · American Journal of Medical Genetics · doi:10.1002/ajmg.1320590218 · Cited by 166
The effect of advancing paternal age on pregnancy and live birth rates in couples undergoing in vitro fertilization or gamete intrafallopian transfer
Klonoff-Cohen, H. S., & Natarajan, L. (2004) · American Journal of Obstetrics and Gynecology · doi:10.1016/j.ajog.2004.01.035 · Cited by 150
Comparative analysis of the ability of precursor germ cells and epididymal spermatozoa to generate reactive oxygen metabolites
Fisher, H. M., & Aitken, R. J. (1997) · Journal of Experimental Zoology · doi:10.1002/(sici)1097-010x(19970401)277:5 · Cited by 149
Paternal Age and Spontaneous Abortion
Kleinhaus, K., Perrin, M. C., Friedlander, Y., Paltiel, O., Malaspina, D., & Harlap, S. (2006) · Obstetrics and Gynecology · doi:10.1097/01.aog.0000224606.26514.3a · Cited by 147
Association of Paternal Age and Risk for Major Congenital Anomalies From the National Birth Defects Prevention Study, 1997 to 2004
Green, R. F., Devine, O. J., Crider, K. S., Olney, R. S., Archer, N. P., Olshan, A. F., & Shapira, S. K. (2010) · Annals of Epidemiology · doi:10.1016/j.annepidem.2009.10.009 · Cited by 145
Parental Age As a Risk Factor of Childhood Leukemia and Brain Cancer in Offspring
Hemminki, K., Kyyrönen, P., & Vaittinen, P. (1999) · Epidemiology · doi:10.1097/00001648-199905000-00014 · Cited by 143
Ultrastructure of the aging human testis
Paniagua, R., Nistal, M., SÁEZ, F. J., & Fraile, B. (1991) · Journal of Electron Microscopy Technique · doi:10.1002/jemt.1060190209 · Cited by 143
Paternal Age and Schizophrenia: Further Support for an Association
Dalman, C., & Allebeck, P. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.9.1591 · Cited by 136
Mutation frequency declines during spermatogenesis in young mice but increases in old mice
Walter, C. A., Intano, G. W., McCarrey, J. R., McMahan, C. A., & Walter, R. B. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.17.10015 · Cited by 135
DNA repair in mammalian embryos
Jaroudi, S., & SenGupta, S. B. (2006) · Mutation Research/Reviews in Mutation Research · doi:10.1016/j.mrrev.2006.09.002 · Cited by 131
Spermatozoa Have Decreased Antioxidant Enzymatic Capacity and Increased Reactive Oxygen Species Production During Aging in the Brown Norway Rat
Weir, C., & Robaire, B. (2007) · Journal of Andrology · doi:10.2164/jandrol.106.001362 · Cited by 131
Self-citation
The effects of male aging on semen quality, sperm DNA fragmentation and chromosomal abnormalities in an infertile population
Brahem, S., Mehdi, M., Elghezal, H., & Saâd, A. (2011) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-011-9537-5 · Cited by 126
Prevalence and parental origin of de novo RET mutations in multiple endocrine neoplasia type 2A and familial medullary thyroid carcinoma. Le Groupe d'Etude des Tumeurs a Calcitonine.
Schuffenecker, I., Ginet, N., Goldgar, D., Eng, C., Chambe, B., Boneu, A., Houdent, C., Pallo, D., Schlumberger, M. J., Thivolet, C. H., et al. (1997) · Europe PMC (PubMed Central) · Cited by 117
Effect of sperm DNA damage and sperm protamine deficiency on fertilization and embryo development post-ICSI.
Mohammad, H. N.-E., Mohammad, S., Shahnaz, R., Maryam, A. I., Shahla, R., Fariba, M., & Mohammad, M. (2005) · Reproductive BioMedicine Online · doi:10.1016/s1472-6483(10)60959-5 · Cited by 115
Paternal age ≥40 years: An important risk factor for infertility
Rochebrochard, É. D. L., & Thonneau, P. F. (2003) · American Journal of Obstetrics and Gynecology · doi:10.1067/s0002-9378(03)00753-1 · Cited by 115
Attenuation of DNA polymerase β-dependent base excision repair and increased DMS-induced mutagenicity in aged mice
Cabelof, D. C., Raffoul, J. J., Yanamadala, S., Ganir, C., Guo, Z., & Heydari, A. R. (2002) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(02)00003-9 · Cited by 114
Aging of Male Germ Line Stem Cells in Mice1
Zhang, X., Ebata, K. T., Robaire, B., & Nagano, M. C. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.045591 · Cited by 110
Self-citation
Paternal age and the risk of congenital heart defects
Olshan, A. F., Schnitzer, P. G., & Baird, P. A. (1994) · Teratology · doi:10.1002/tera.1420500111 · Cited by 108
The correlation between male age, sperm quality and sperm DNA fragmentation in 320 men attending a fertility center
Winkle, T., Rosenbusch, B. E., Gagsteiger, F., Paiss, T., & Zoller, N. (2008) · Journal of Assisted Reproduction and Genetics · doi:10.1007/s10815-008-9277-3 · Cited by 98
Anti‐aging activity of the Ink4/Arf locus
Matheu, A., Maraver, A., Collado, M., Garcia‐Cao, I., Cañamero, M., Borras, C., Flores, J. M., Klatt, P., Viña, J., & Serrano, M. (2009) · Aging Cell · doi:10.1111/j.1474-9726.2009.00458.x · Cited by 94
Parental Age and Risk of Sporadic and Familial Cancer in Offspring
Hemminki, K., & Kyyrönen, P. (1999) · Epidemiology · doi:10.1097/00001648-199911000-00016 · Cited by 94
Developmental Regulation and In Vitro Culture Effects on Expression of DNA Repair and Cell Cycle Checkpoint Control Genes in Rhesus Monkey Oocytes and Embryos1
Zheng, P., Schramm, R. D., & Latham, K. E. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.104.039073 · Cited by 92
The Effect of Aging on the Seminiferous Epithelium of the Brown Norway Rat
Wright, W. W., FIORE, C., & Zirkin, B. R. (1993) · Journal of Andrology · doi:10.1002/j.1939-4640.1993.tb01661.x · Cited by 85
Association of paternal age at birth and the risk of breast cancer in offspring: a case control study
Choi, J., Lee, K.-M., Park, S. K., Noh, D., Ahn, S. H., Yoo, K., & Kang, D. (2005) · BMC Cancer · doi:10.1186/1471-2407-5-143 · Cited by 84
DNA double strand break repair in brain: Reduced NHEJ activity in aging rat neurons
Vyjayanti, V. N., & Rao, K. S. (2005) · Neuroscience Letters · doi:10.1016/j.neulet.2005.09.053 · Cited by 83
Advancing Paternal Age Is Associated with Deficits in Social and Exploratory Behaviors in the Offspring: A Mouse Model
Smith, R. G., Kember, R. L., Mill, J. S., Fernandes, C., Schalkwyk, L. C., Buxbaum, J. D., & Reichenberg, A. (2009) · PLoS ONE · doi:10.1371/journal.pone.0008456 · Cited by 81
Parental age effects on the occurrence of new mutations for the Marfan syndrome
Murdoch, J. L., Walker, B. A., & McKusick, V. A. (1972) · Annals of Human Genetics · doi:10.1111/j.1469-1809.1957.tb01406.x · Cited by 79
Sperm Structural and Motility Changes During Aging in the Brown Norway Rat
Syntin, P., & Robaire, B. (2001) · Journal of Andrology · doi:10.1002/j.1939-4640.2001.tb02176.x · Cited by 75
Self-citation
Aging Results in Differential Regulation of DNA Repair Pathways in Pachytene Spermatocytes in the Brown Norway Rat1
Paul, C., Nagano, M. C., & Robaire, B. (2011) · Biology of Reproduction · doi:10.1095/biolreprod.111.094219 · Cited by 74
Self-citation
Non‐homologous DNA end joining in the mature rat brain
Ren, K., & de Ortíz, S. P. (2002) · Journal of Neurochemistry · doi:10.1046/j.0022-3042.2002.00776.x · Cited by 72
Reproductive Aging in the Brown Norway Rat Is Characterized by Accelerated Germ Cell Apoptosis and Is Not Altered by Luteinizing Hormone Replacement
Wang, C., Hikim, A. P. S., Lue, Y., Leung, A., Baravarian, S., & Swerdloff, R. S. (1999) · Journal of Andrology · doi:10.1002/j.1939-4640.1999.tb02550.x · Cited by 71
Paternal Age Over 40 Years: The “Amber Light” in the Reproductive Life of Men?
Rochebrochard, É. D. L., McElreavey, K., & Thonneau, P. F. (2003) · Journal of Andrology · doi:10.1002/j.1939-4640.2003.tb02694.x · Cited by 71
Age and Sex Effects on Human Mutation Rates: An Old Problem with New Complexities
Crow, J. F. (2006) · Journal of Radiation Research · doi:10.1269/jrr.47.b75 · Cited by 69
Paternal age is a risk factor for Alzheimer disease in the absence of a major gene
Bertram, L., Busch, R., Spiegl, M., Lautenschlager, N. T., Müller, U., & Kurz, A. (1998) · Neurogenetics · doi:10.1007/s100480050041 · Cited by 68
Aneuploidies and micronuclei in the germ cells of male mice of advanced age
Lowe, X. R., Collins, B. W., Allen, J. W., Titenko-Holland, N. V., Breneman, J. W., van Beek, M., Bishop, J. B., & Wyrobek, A. J. (1995) · Mutation Research/DNAging · doi:10.1016/0921-8734(95)00012-u · Cited by 66
Tissue-specific changes of DNA repair protein Ku and mtHSP70 in aging rats and their retardation by caloric restriction
Um, J. H., Kim, S. J., Kim, D. W., Ha, M. Y., Jang, J. H., Kim, D. W., Chung, B., Kang, C., & Kim, S. H. (2003) · Mechanisms of Ageing and Development · doi:10.1016/s0047-6374(03)00169-6 · Cited by 64
Maternal age and paternal age are associated with distinct childhood behavioural outcomes in a general population birth cohort
Saha, S., Barnett, A. G., Buka, S. L., & McGrath, J. J. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.09.012 · Cited by 63
Mutation load and human longevity
Gavrilov, L. A., Gavrilova, N. S., Kroutko, V. N., Николаевна, Е. Г., Semyonova, V. G., Gavrilova, A. L., Lapshin, E. V., Nn, E., & Kushnareva, Y. E. (1997) · Mutation research. Fundamental and molecular mechanisms of mutagenesis · doi:10.1016/s0027-5107(97)00058-4 · Cited by 63
Structure and gametogenic potential of seminiferous tubules in ageing mice
Gosden, R. G., Richardson, D. C., Brown, N. A., & Davidson, D. W. (1982) · Reproduction · doi:10.1530/jrf.0.0640127 · Cited by 61
Paternal age affects fertility and progeny outcome in the Brown Norway rat
Serre, V., & Robaire, B. (1998) · Fertility and Sterility · doi:10.1016/s0015-0282(98)00259-3 · Cited by 60
Self-citation
Base Excision Repair Is Limited by Different Proteins in Male Germ Cell Nuclear Extracts Prepared from Young and Old Mice
Intano, G. W., McMahan, C. A., McCarrey, J. R., Walter, R. B., McKenna, A. E., Matsumoto, Y., MacInnes, M. A., Chen, D. J., & Walter, C. A. (2002) · Molecular and Cellular Biology · doi:10.1128/mcb.22.7.2410-2418.2002 · Cited by 60
Effects of ageing on spermatozoal chromatin and its sensitivity to in vivo and in vitro oxidative challenge in the Brown Norway rat.
Zubkova, E., & Robaire, B. (2006) · Human Reproduction · doi:10.1093/humrep/del193 · Cited by 60
Self-citation
Semen quality and aging: analysis of 9.168 samples in Cordoba. Argentina.
Molina, R. I., Martini, A. C., Tissera, A. D., Olmedo, J. J., Senestrari, D., de Cúneo, M. F., & Ruiz, R. D. (2010) · PubMed · Cited by 53
Long-Term Effects of Delayed Fatherhood in Mice on Postnatal Development and Behavioral Traits of Offspring1
García-Palomares, S., Pertusa, J. F., Miñarro, J., García‐Pérez, M. Á., Hermenegildo, C., Rausell, F., Cano, A., & Tarín, J. J. (2008) · Biology of Reproduction · doi:10.1095/biolreprod.108.072066 · Cited by 53
Reproductive functions, fertility and genetic risks of ageing men
Rolf, C., & Nieschlag, E. (2001) · Experimental and Clinical Endocrinology & Diabetes · doi:10.1055/s-2001-14825 · Cited by 52
Frequency of human sperm carrying structural aberrations of chromosome 1 increases with advancing age
Sloter, E. D., Marchetti, F., Eskenazi, B., Weldon, R. H., Nath, J., Cabreros, D., & Wyrobek, A. J. (2007) · Fertility and Sterility · doi:10.1016/j.fertnstert.2006.08.112 · Cited by 50
Advanced paternal age is associated with alterations in discrete behavioural domains and cortical neuroanatomy of C57BL/6J mice
Foldi, C. J., Eyles, D. W., McGrath, J. J., & Burne, T. H. J. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07074.x · Cited by 49
Increased de novo copy number variants in the offspring of older males
Flatscher‐Bader, T., Foldi, C. J., Chong, S., Whitelaw, E., Moser, R. J., Burne, T. H. J., Eyles, D. W., & McGrath, J. J. (2011) · Translational Psychiatry · doi:10.1038/tp.2011.30 · Cited by 47
Late paternity and stillbirth risk
Astolfi, P., Pasquale, A. D., & Zonta, L. A. (2004) · Human Reproduction · doi:10.1093/humrep/deh449 · Cited by 47
Spontaneous Mutation as a Risk Factor
Crow, J. F. (2015) · KARGER eBooks · doi:10.1159/000424865 · Cited by 45
The effects of male age on semen parameters: analysis of 1364 men attending an andrology center
Maya, W. D. C., Berdugo, J., & Jaramillo, Á. C. (2009) · The Aging Male · doi:10.3109/13685530903322841 · Cited by 42
Deoxyribonucleic acid repair and apoptosis in testicular germ cells of aging fertile men: the role of the poly(adenosine diphosphate-ribosyl)ation pathway
El-Domyati, M. M., Al-Din, A.-B. M., Barakat, M. T., El‐Fakahany, H. M., Xu, J., & Sakkas, D. (2008) · Fertility and Sterility · doi:10.1016/j.fertnstert.2008.03.027 · Cited by 42
Biological Clock Ticks for Men, Too
Thacker, P. D. (2004) · JAMA · doi:10.1001/jama.291.14.1683 · Cited by 41
Analysis of age-associated changes in mitochondrial free radical generation by rat testis
Vázquez-Memije, M. E., Capín, R., Tolosa, A., & El‐Hafidi, M. (2007) · Molecular and Cellular Biochemistry · doi:10.1007/s11010-007-9580-9 · Cited by 40
Exponential Decrease During Aging and Random Lifetime of Mouse Spermatogonial Stem Cells
Suzuki, N., & Withers, H. R. (1978) · Science · doi:10.1126/science.725597 · Cited by 36
DNA Repair Genes
(2007) · Hawley's Condensed Chemical Dictionary · doi:10.1002/9780470114735.hawley06132 · Cited by 27
Aging does not affect spermatogenic recovery after experimentally induced injury in mice
Ehmcke, J., Joshi, B., Hergenrother, S. D., & Schlatt, S. (2007) · Reproduction · doi:10.1530/rep-06-0148 · Cited by 25
Paternal age effect on age of onset in bipolar I disorder is mediated by sex and family history
Grigoroiu‐Serbânescu, M., WICKRAMARATNE, P. J., Mihăilescu, R., Prelipceanu, D., Sima, D., Codreanu, M., Grimberg, M., & Elston, R. C. (2012) · American Journal of Medical Genetics Part B Neuropsychiatric Genetics · doi:10.1002/ajmg.b.32063 · Cited by 23
When Fatherhood Should Stop?
Gavrilov, L. A. (1997) · Science · doi:10.1126/science.277.5322.17b · Cited by 23
Transgenic Mouse Models
Nishino, T., Ni, J., & Devuyst, O. (2007) · Peritoneal Dialysis International · doi:10.1177/089686080702700604 · Cited by 20
Envejecimiento y calidad seminal: un análisis de 9.168 casos en Córdoba, Argentina
Molina, R. I., Martini, A. C., Tissera, A. D., Olmedo, J. J., Senestrari, D., de Cúneo, M. F., & Ruiz, R. D. (2010) · Archivos Españoles de Urología · doi:10.4321/s0004-06142010000300007 · Cited by 19
Arrested germ cell divisions in the ageing human testis
Miething, A. (2005) · Andrologia · doi:10.1111/j.1439-0272.2004.00645.x · Cited by 16
Effects of primary testicular damage on sperm DNA oxidative status and embryonic and foetal development
Dimitriadis, F., Giannakis, D., Pardalidis, N. P., Τσουκανέλης, Κ., Kanakas, N., Saito, M., Watanabe, T., Miyagawa, I., Tsounapi, P., & Sofikitis, N. (2009) · Andrologia · doi:10.1111/j.1439-0272.2009.00929.x · Cited by 11
Spermatid micronucleus analysis of aging effects in hamsters
Allen, J. W., Collins, B. W., & Setzer, R. W. (1996) · Mutation Research/DNAging · doi:10.1016/s0921-8734(96)90008-9 · Cited by 10
Molecular diagnosis of deletions in the human multigene complex of growth and placental lactogen hormones
González-Rodríguez, E., Jaramillo‐Rangel, G., & Barrera-Saldaña, H. A. (1997) · American Journal of Medical Genetics · doi:10.1002/(sici)1096-8628(19971112)72:4 · Cited by 10
All for One, or One for All?
Adamson, P. C., Paradis, C., & Smith, M. L. (2007) · The Hastings Center Report · doi:10.1353/hcr.2007.0049 · Cited by 8
Aging and diethylstilbestrol-induced aneuploidy in male germ cells: a transgenic mouse model
Xiao, Y., Tates, A. D., Boei, J. J. W. A., & Natarajan, A. T. (1998) · Chromosoma · doi:10.1007/s004120050336 · Cited by 6

Flagged first, then by citations

3 of the 120 references couldn’t be matched to a known paper.

Sorted by citations

Inflammation and aging: signaling pathways and intervention therapies
Li, X., Li, C., Zhang, W., Wang, Y., Qian, P., & Huang, H. (2023) · Signal Transduction and Targeted Therapy · doi:10.1038/s41392-023-01502-8 · Cited by 1,443
Oxidative stress and male infertility
Bisht, S., Faiq, M. A., Tolahunase, M., & Dada, R. (2017) · Nature Reviews Urology · doi:10.1038/nrurol.2017.69 · Cited by 918
New insights into the generation and role of de novo mutations in health and disease
Acuña‐Hidalgo, R., Veltman, J. A., & Hoischen, A. (2016) · Genome biology · doi:10.1186/s13059-016-1110-1 · Cited by 474
Age-Associated Sperm DNA Methylation Alterations: Possible Implications in Offspring Disease Susceptibility
Jenkins, T. G., Aston, K. I., Pflueger, C., Cairns, B. R., & Carrell, D. T. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004458 · Cited by 299
Fertility preservation in men with cancer
Tournaye, H. J., Dohle, G. R., & Barratt, C. L. R. (2014) · The Lancet · doi:10.1016/s0140-6736(14)60495-5 · Cited by 146

See all 109

Authors: Paul, C., & Robaire, B.
Affiliations: McGill University (CA)
Corresponding author: Robaire, Bernard
ORCID: Robaire, Bernard
Venue: Nature Reviews Urology
Publisher: Springer Science and Business Media LLC
Published: 2013-02-26
Volume: 10
Issue: 4
Pages: 227-234
ISSN: 1759-4812 (ISSN-L)
1759-4820
DOI: 10.1038/nrurol.2013.18
OpenAlex: W1996219414
Cited by: 109
References: 120
Citations by year: 2026: 7 · 2025: 4 · 2024: 4 · 2023: 5 · 2022: 10 · 2021: 5 · 2020: 10 · 2019: 15 · 2018: 6 · 2017: 5 · 2016: 10 · 2015: 10 · 2014: 9 · 2013: 9
FWCI: 2.06
Type: journal article
Language: en
Open access: closed
Licence: www.springer.com/tdm (tdm)
Locations: Nature Reviews Urology (publishedVersion)
PubMed (publishedVersion)
Topics: Health Sciences › Medicine › Reproductive Medicine › Sperm and Testicular Function
Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords: paternal age, spermatogonial stem cells, DNA damage, Sertoli cells, peritubular myoid cells, de novo mutations, chromosomal damage, advanced paternal age, male fertility decline, semen quality
MeSH terms: Aging, Animals, Mental Disorders, DNA Damage, Germ Cells, Humans, Infertility, Male, Male, Mutation, Paternal Age, Spermatozoa, Cellular Senescence

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Ageing of the male germ line

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks