Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Reproductive Biology and Endocrinology
Published in: Reproductive Biology and Endocrinology 1/2015

Open Access 01-12-2015 | Editorial

Infertility etiologies are genetically and clinically linked with other diseases in single meta-diseases

Authors: Juan J Tarín, Miguel A García-Pérez, Toshio Hamatani, Antonio Cano

Published in: Reproductive Biology and Endocrinology | Issue 1/2015

Login to get access

Abstract

The present review aims to ascertain whether different infertility etiologies share particular genes and/or molecular pathways with other pathologies and are associated with distinct and particular risks of later-life morbidity and mortality. In order to reach this aim, we use two different sources of information: (1) a public web server named DiseaseConnect (http://​disease-connect.​org) focused on the analysis of common genes and molecular mechanisms shared by diseases by integrating comprehensive omics and literature data; and (2) a literature search directed to find clinical comorbid relationships of infertility etiologies with only those diseases appearing after infertility is manifested. This literature search is performed because DiseaseConnect web server does not discriminate between pathologies emerging before, concomitantly or after infertility is manifested. Data show that different infertility etiologies not only share particular genes and/or molecular pathways with other pathologies but they have distinct clinical relationships with other diseases appearing after infertility is manifested. In particular, (1) testicular and high-grade prostate cancer in male infertility; (2) non-fatal stroke and endometrial cancer, and likely non-fatal coronary heart disease and ovarian cancer in polycystic ovary syndrome; (3) osteoporosis, psychosexual dysfunction, mood disorders and dementia in premature ovarian failure; (4) breast and ovarian cancer in carriers of BRCA1/2 mutations in diminished ovarian reserve; (5) clear cell and endometrioid histologic subtypes of invasive ovarian cancer, and likely low-grade serous invasive ovarian cancer, melanoma and non-Hodgkin lymphoma in endometriosis; and (6) endometrial and ovarian cancer in idiopathic infertility. The present data endorse the principle that the occurrence of a disease (in our case infertility) is non-random in the population and suggest that different infertility etiologies are genetically and clinically linked with other diseases in single meta-diseases. This finding opens new insights for clinicians and reproductive biologists to treat infertility problems using a phenomic approach instead of considering infertility as an isolated and exclusive disease of the reproductive system/hypothalamic–pituitary–gonadal axis. In agreement with a previous validation analysis of the utility of DiseaseConnect web server, the present study does not show a univocal correspondence between common gene expression and clinical comorbid relationship. Further work is needed to untangle the potential genetic, epigenetic and phenotypic relationships that may be present among different infertility etiologies, morbid conditions and physical/cognitive traits.
Literature
1.
2.
Thoma ME, McLain AC, Louis JF, King RB, Trumble AC, Sundaram R, et al. Prevalence of infertility in the United States as estimated by the current duration approach and a traditional constructed approach. Fertil Steril. 2013;99:1324–31.e1.
3.
Tarín JJ, García-Pérez MA, Cano A. Assisted reproductive technology results: why are live-birth percentages so low? Mol Reprod Dev. 2014;81:568–83.CrossRefPubMed
4.
Liu CC, Tseng YT, Li W, Wu CY, Mayzus I, Rzhetsky A, et al. DiseaseConnect: a comprehensive web server for mechanism-based disease-disease connections. Nucleic Acids Res. 2014;42:W137–46.CrossRefPubMedCentralPubMed
5.
6.
7.
Tomao F, Lo Russo G, Spinelli GP, Stati V, Prete AA, Prinzi N, et al. Fertility drugs, reproductive strategies and ovarian cancer risk. J Ovarian Res. 2014;7:51.CrossRefPubMedCentralPubMed
8.
Rizzuto I, Behrens RF, Smith LA. Risk of ovarian cancer in women treated with ovarian stimulating drugs for infertility. Cochrane Database Syst Rev. 2013;8, CD008215.PubMed
9.
Schüler S, Ponnath M, Engel J, Ortmann O. Ovarian epithelial tumors and reproductive factors: a systematic review. Arch Gynecol Obstet. 2013;287:1187–204.CrossRefPubMed
10.
Zreik TG, Mazloom A, Chen Y, Vannucci M, Pinnix CC, Fulton S, et al. Fertility drugs and the risk of breast cancer: a meta-analysis and review. Breast Cancer Res Treat. 2010;124:13–26.CrossRefPubMed
11.
Siristatidis C, Sergentanis TN, Kanavidis P, Trivella M, Sotiraki M, Mavromatis I, et al. Controlled ovarian hyperstimulation for IVF: impact on ovarian, endometrial and cervical cancer—a systematic review and meta-analysis. Hum Reprod Update. 2013;19:105–23.CrossRefPubMed
12.
Sergentanis TN, Diamantaras AA, Perlepe C, Kanavidis P, Skalkidou A, Petridou ET. IVF and breast cancer: a systematic review and meta-analysis. Hum Reprod Update. 2014;2:106–23.CrossRef
13.
14.
15.
Hotaling JM, Walsh TJ. Male infertility: a risk factor for testicular cancer. Nat Rev Urol. 2009;6:550–6.CrossRefPubMed
16.
Peng X, Zeng X, Peng S, Deng D, Zhang J. The association risk of male subfertility and testicular cancer: a systematic review. PLoS One. 2009;4, e5591.CrossRefPubMedCentralPubMed
17.
18.
Eisenberg ML, Li S, Behr B, Cullen MR, Galusha D, Lamb DJ, et al. Semen quality, infertility and mortality in the USA. Hum Reprod. 2014;29:1567–74.CrossRefPubMed
19.
Belloc S, Cohen-Bacrie M, Amar E, Izard V, Benkhalifa M, Dalléac A, et al. High body mass index has a deleterious effect on semen parameters except morphology: results from a large cohort study. Fertil Steril. 2014;102:1268–73.CrossRefPubMed
20.
Omu AE. Sperm parameters: paradigmatic index of good health and longevity. Med Princ Pract. 2013;22 Suppl 1:30–42.CrossRefPubMed
21.
Sermondade N, Faure C, Fezeu L, Shayeb AG, Bonde JP, Jensen TK, et al. BMI in relation to sperm count: an updated systematic review and collaborative meta-analysis. Hum Reprod Update. 2013;19:221–31.CrossRefPubMedCentralPubMed
22.
Eisenberg ML, Kim S, Chen Z, Sundaram R, Schisterman EF, Buck Louis GM. The relationship between male BMI and waist circumference on semen quality: data from the LIFE study. Hum Reprod. 2014;29:193–200.CrossRefPubMedCentralPubMed
23.
Li Y, Lin H, Li Y, Cao J. Association between socio-psycho-behavioral factors and male semen quality: systematic review and meta-analyses. Fertil Steril. 2011;95:116–23.CrossRefPubMed
24.
Ely JJ. Inadequate levels of essential nutrients in developed nations as a risk factor for disease: a review. Rev Environ Health. 2003;18:111–29.CrossRefPubMed
25.
Leon DA, Shkolnikov VM, McKee M. Alcohol and Russian mortality: a continuing crisis. Addiction. 2009;104:1630–6.CrossRefPubMed
26.
Pilgrim JL, Woodford N, Drummer OH. Cocaine in sudden and unexpected death: a review of 49 post-mortem cases. Forensic Sci Int. 2013;227:52–9.CrossRefPubMed
27.
Rizzuto D, Fratiglioni L. Lifestyle factors related to mortality and survival: a mini-review. Gerontology. 2014;60:327–35.CrossRefPubMed
28.
Povey AC, Clyma JA, McNamee R, Moore HD, Baillie H, Pacey AA, et al. Modifiable and non-modifiable risk factors for poor semen quality: a case-referent study. Hum Reprod. 2012;27:2799–806.CrossRefPubMed
29.
Pacey AA, Povey AC, Clyma JA, McNamee R, Moore HD, Baillie H, et al. Modifiable and non-modifiable risk factors for poor sperm morphology. Hum Reprod. 2014;29:1629–36.CrossRefPubMed
30.
Permuth-Wey J, Besharat A, Sellers TA. Epidemiology of ovarian cancer: an update. In: Farghaly SA, editor. Advances in Diagnosis and Management of Ovarian Cancer. New York: Springer Science & Business Media; 2014. p. 1–21.CrossRef
31.
Parikh NI, Cnattingius S, Mittleman MA, Ludvigsson JF, Ingelsson E. Subfertility and risk of later life maternal cardiovascular disease. Hum Reprod. 2012;27:568–75.CrossRefPubMedCentralPubMed
32.
Venn A, Hemminki E, Watson L, Bruinsma F, Healy D. Mortality in a cohort of IVF patients. Hum Reprod. 2001;16:2691–6.CrossRefPubMed
33.
Braat DD, Schutte JM, Bernardus RE, Mooij TM, van Leeuwen FE. Maternal death related to IVF in the Netherlands 1984–2008. Hum Reprod. 2010;25:1782–6.CrossRefPubMed
34.
Westerlund E, Brandt L, Hovatta O, Wallén H, Ekbom A, Henriksson P. Incidence of hypertension, stroke, coronary heart disease, and diabetes in women who have delivered after in vitro fertilization: a population-based cohort study from Sweden. Fertil Steril. 2014;102:1096–102.CrossRefPubMed
35.
Udell JA, Lu H, Redelmeier DA. Long-term cardiovascular risk in women prescribed fertility therapy. J Am Coll Cardiol. 2013;62:1704–12.CrossRefPubMed
36.
Yli-Kuha AN, Gissler M, Klemetti R, Luoto R, Hemminki E. Cancer morbidity in a cohort of 9175 Finnish women treated for infertility. Hum Reprod. 2012;27:1149–55.CrossRefPubMed
37.
Calogero AE, Calabrò V, Catanuso M, Condorelli RA, La Vignera S. Understanding polycystic ovarian syndrome pathogenesis: an updated of its genetic aspects. J Endocrinol Invest. 2011;34:630–44.CrossRefPubMed
38.
Teede H, Deeks A, Moran L. Polycystic ovary syndrome: a complex condition with psychological, reproductive and metabolic manifestations that impacts on health across the lifespan. BMC Med. 2010;8:41.CrossRefPubMedCentralPubMed
39.
Rotterdam ESHRE/ASRM-Sponsored PCOS consensus workshop group. Revised 2003 consensus on diagnostic criteria and long-term health risks related to polycystic ovary syndrome (PCOS). Hum Reprod. 2004;19:41–7.CrossRef
40.
41.
Kar S. Anthropometric, clinical, and metabolic comparisons of the four Rotterdam PCOS phenotypes: a prospective study of PCOS women. J Hum Reprod Sci. 2013;6:194–200.CrossRefPubMedCentralPubMed
42.
Anderson SA, Barry JA, Hardiman PJ. Risk of coronary heart disease and risk of stroke in women with polycystic ovary syndrome: A systematic review and meta-analysis. Int J Cardiol. 2014;176:486–7.CrossRefPubMed
43.
Vink JM, Sadrzadeh S, Lambalk CB, Boomsma DI. Heritability of polycystic ovary syndrome in a Dutch twin-family study. J Clin Endocrinol Metab. 2006;91:2100–4.CrossRefPubMed
44.
Hunter A, Vimplis S, Sharma A, Eid N, Atiomo W. To determine whether first-degree male relatives of women with polycystic ovary syndrome are at higher risk of developing cardiovascular disease and type II diabetes mellitus. J Obstet Gynaecol. 2007;27:591–6.CrossRefPubMed
45.
Davies MJ, Marino JL, Willson KJ, March WA, Moore VM. Intergenerational associations of chronic disease and polycystic ovary syndrome. PLoS One. 2011;6, e25947.CrossRefPubMedCentralPubMed
46.
Louwers YV, Roest-Schalken ME, Kleefstra N, Roeters van Lennep J, van den Berg M, Fauser BC, et al. Excess mortality in mothers of patients with polycystic ovary syndrome. Hum Reprod. 2014;29:1780–6.CrossRefPubMed
47.
Savaris RF, Groll JM, Young SL, DeMayo FJ, Jeong JW, Hamilton AE, et al. Progesterone resistance in PCOS endometrium: a microarray analysis in clomiphene citrate-treated and artificial menstrual cycles. J Clin Endocrinol Metab. 2011;96:1737–46.CrossRefPubMedCentralPubMed
48.
Ali AT. Risk factors for endometrial cancer. Ceska Gynekol. 2013;78:448–59.PubMed
49.
Chittenden BG, Fullerton G, Maheshwari A, Bhattacharya S. Polycystic ovary syndrome and the risk of gynaecological cancer: a systematic review. Reprod Biomed Online. 2009;19:398–405.CrossRefPubMed
50.
Barry JA, Azizia MM, Hardiman PJ. Risk of endometrial, ovarian and breast cancer in women with polycystic ovary syndrome: a systematic review and meta-analysis. Hum Reprod Update. 2014;20:748–58.CrossRefPubMedCentralPubMed
51.
Ali AT. Reproductive factors and the risk of endometrial cancer. Int J Gynecol Cancer. 2014;24:384–93.CrossRefPubMed
52.
Housman E, Reynolds RV. Polycystic ovary syndrome: a review for dermatologists: Part I. Diagnosis and manifestations. J Am Acad Dermatol. 2014;71:847.e1-e10.
53.
Daan NM, Louwers YV, Koster MP, Eijkemans MJ, de Rijke YB, Lentjes EW, et al. Cardiovascular and metabolic profiles amongst different polycystic ovary syndrome phenotypes: who is really at risk? Fertil Steril. 2014;102:1444–51.e3.
54.
Lambrinoudaki I. Cardiovascular risk in postmenopausal women with the polycystic ovary syndrome. Maturitas. 2011;68:13–6.CrossRefPubMed
55.
Silva CA, Yamakami LY, Aikawa NE, Araujo DB, Carvalho JF, Bonfá E. Autoimmune primary ovarian insufficiency. Autoimmun Rev. 2014;13:427–30.CrossRefPubMed
56.
57.
Maclaran K, Horner E, Panay N. Premature ovarian failure: long-term sequelae. Menopause Int. 2010;16:38–41.PubMed
58.
59.
Shuster LT, Rhodes DJ, Gostout BS, Grossardt BR, Rocca WA. Premature menopause or early menopause: long-term health consequences. Maturitas. 2010;65:161–6.CrossRefPubMedCentralPubMed
60.
Li S, Rosenberg L, Wise LA, Boggs DA, LaValley M, Palmer JR. Age at natural menopause in relation to all-cause and cause-specific mortality in a follow-up study of US black women. Maturitas. 2013;75:246–52.CrossRefPubMedCentralPubMed
61.
62.
Mahendru AA, Morris E. Cardiovascular disease in menopause: does the obstetric history have any bearing? Menopause Int. 2013;19:115–20.PubMed
63.
Scott EL, Zhang QG, Vadlamudi RK, Brann DW. Premature menopause and risk of neurological disease: basic mechanisms and clinical implications. Mol Cell Endocrinol. 2014;389:2–6.CrossRefPubMed
64.
Atwood CS, Bowen RL. The reproductive-cell cycle theory of aging: an update. Exp Gerontol. 2011;46:100–7.CrossRefPubMed
65.
Greene AD, Patounakis G, Segars JH. Genetic associations with diminished ovarian reserve: a systematic review of the literature. J Assist Reprod Genet. 2014;31:935–46.CrossRefPubMed
66.
67.
Richardson MC, Guo M, Fauser BC, Macklon NS. Environmental and developmental origins of ovarian reserve. Hum Reprod Update. 2014;20:353–69.CrossRefPubMed
68.
Gleicher N, Kim A, Weghofer A, Kushnir VA, Shohat-Tal A, Lazzaroni E, et al. Hypoandrogenism in association with diminished functional ovarian reserve. Hum Reprod. 2013;28:1084–91.CrossRefPubMed
69.
Verit FF, Keskin S, Omer B, Yalcinkaya S, Sakar N. Is there any relationship between cardiovascular risk markers and young women with diminished ovarian reserve? Gynecol Endocrinol. 2014;30:697–700.CrossRefPubMed
70.
Titus S, Li F, Stobezki R, Akula K, Unsal E, Jeong K, et al. Impairment of BRCA1-related DNA double-strand break repair leads to ovarian aging in mice and humans. Sci Transl Med. 2013;5:172ra21.
71.
Wang ET, Pisarska MD, Bresee C, Ida Chen YD, Lester J, Afshar Y, et al. BRCA1 germline mutations may be associated with reduced ovarian reserve. Fertil Steril. 2014;102:1723–8.CrossRefPubMed
72.
Brohet RM, Velthuizen ME, Hogervorst FB, Meijers-Heijboer HE, Seynaeve C, Collée MJ, et al. HEBON Resource. Breast and ovarian cancer risks in a large series of clinically ascertained families with a high proportion of BRCA1 and BRCA2 Dutch founder mutations. J Med Genet. 2014;51:98–107.CrossRefPubMed
73.
Mersch J, Jackson MA, Park M, Nebgen D, Peterson SK, Singletary C, et al. Cancers associated with BRCA1 and BRCA2 mutations other than breast and ovarian. Cancer. 2015;121:269–75.CrossRefPubMed
74.
Oktay K, Kim JY, Barad D, Babayev SN. Association of BRCA1 mutations with occult primary ovarian insufficiency: a possible explanation for the link between infertility and breast/ovarian cancer risks. J Clin Oncol. 2010;28:240–4.CrossRefPubMedCentralPubMed
75.
Rzepka-Górska I, Tarnowski B, Chudecka-Głaz A, Górski B, Zielińska D, Tołoczko-Grabarek A. Premature menopause in patients with BRCA1 gene mutation. Breast Cancer Res Treat. 2006;100:59–63.CrossRefPubMed
76.
Finch A, Valentini A, Greenblatt E, Lynch HT, Ghadirian P, Armel S, et al. Frequency of premature menopause in women who carry a BRCA1 or BRCA2 mutation. Fertil Steril. 2013;99:1724–8.CrossRefPubMed
77.
Lin WT, Beattie M, Chen LM, Oktay K, Crawford SL, Gold EB, et al. Comparison of age at natural menopause in BRCA1/2 mutation carriers with a non-clinic-based sample of women in northern California. Cancer. 2013;119:1652–9.CrossRefPubMedCentralPubMed
78.
Collins IM, Milne RL, McLachlan SA, Friedlander M, Hickey M, Weideman PC, et al. Do BRCA1 and BRCA2 mutation carriers have earlier natural menopause than their noncarrier relatives? Results from the Kathleen Cuningham Foundation Consortium for Research into Familial Breast Cancer. J Clin Oncol. 2013;31:3920–5.CrossRefPubMed
79.
Oktay K, Moy F, Titus S, Stobezki R, Turan V, Dickler M, et al. Age-related decline in DNA repair function explains diminished ovarian reserve, earlier menopause, and possible oocyte vulnerability to chemotherapy in women with BRCA mutations. J Clin Oncol. 2014;32:1093–4.CrossRefPubMed
80.
Batt RE, Martin DC, Odunsi K. Endometriosis of the retrocervical septum is proposed to replace the anatomically incorrect term endometriosis of the rectovaginal septum. Hum Reprod. 2014;29:2603–5.CrossRefPubMed
81.
Munksgaard PS, Blaakaer J. The association between endometriosis and gynecological cancers and breast cancer: a review of epidemiological data. Gynecol Oncol. 2011;123:157–63.CrossRefPubMed
82.
Pavlidou A, Vlahos NF. Endometriosis and ovarian cancer: clinical and molecular aspects. Minerva Endocrinol. 2014;39:155–65.PubMed
83.
Nezhat FR, Pejovic T, Reis FM, Guo SW. The link between endometriosis and ovarian cancer: clinical implications. Int J Gynecol Cancer. 2014;24:623–8.CrossRefPubMed
84.
Vlahos NF, Economopoulos KP, Fotiou S. Endometriosis, in vitro fertilization and the risk of gynaecological malignancies, including ovarian and breast cancer. Best Pract Res Clin Obstet Gynaecol. 2010;24:39–50.CrossRefPubMed
85.
86.
Hu X, Zhou Y, Feng Q, Wang R, Su L, Long J, et al. Association of endometriosis risk and genetic polymorphisms involving biosynthesis of sex steroids and their receptors: an updating meta-analysis. Eur J Obstet Gynecol Reprod Biol. 2012;164:1–9.CrossRefPubMed
87.
Forte A, Cipollaro M, Galderisi U. Genetic, epigenetic and stem cell alterations in endometriosis: new insights and potential therapeutic perspectives. Clin Sci (Lond). 2014;126:123–38.CrossRef
88.
Rahmioglu N, Nyholt DR, Morris AP, Missmer SA, Montgomery GW, Zondervan KT. Genetic variants underlying risk of endometriosis: insights from meta-analysis of eight genome-wide association and replication datasets. Hum Reprod Update. 2014;20:702–16.CrossRefPubMedCentralPubMed
89.
90.
Siufi Neto J, Kho RM, Siufi DF, Baracat EC, Anderson KS, Abrão MS. Cellular, histologic, and molecular changes associated with endometriosis and ovarian cancer. J Minim Invasive Gynecol. 2014;21:55–63.CrossRefPubMed
91.
Cetin I, Cozzi V, Antonazzo P. Infertility as a cancer risk factor - a review. Placenta. 2008;29 Suppl B:169–77.
92.
Pearce CL, Templeman C, Rossing MA, Lee A, Near AM, Webb PM, et al. Association between endometriosis and risk of histological subtypes of ovarian cancer: a pooled analysis of case–control studies. Lancet Oncol. 2012;13:385–94.CrossRefPubMedCentralPubMed
93.
Heidemann LN, Hartwell D, Heidemann CH, Jochumsen KM. The relation between endometriosis and ovarian cancer - a review. Acta Obstet Gynecol Scand. 2014;93:20–31.CrossRefPubMed
94.
Venn A, Watson L, Bruinsma F, Giles G, Healy D. Risk of cancer after use of fertility drugs with in-vitro fertilisation. Lancet. 1999;354:1586–90.CrossRefPubMed
95.
Ness RB, Cramer DW, Goodman MT, Kjaer SK, Mallin K, Mosgaard BJ, et al. Infertility, fertility drugs, and ovarian cancer: a pooled analysis of case–control studies. Am J Epidemiol. 2002;155:217–24.CrossRefPubMed
96.
Venn A, Healy D, McLachlan R. Cancer risks associated with the diagnosis of infertility. Best Pract Res Clin Obstet Gynaecol. 2003;17:343–67.CrossRefPubMed
97.
G S, A B, Kamath A, Shivaprakash P, Adhikari P, Up R, et al. Acanthosis nigricans in PCOS patients and its relation with type 2 diabetes mellitus and body mass at a tertiary care hospital in Southern India. J Clin Diagn Res. 2013;7:317–9.
98.
Xie J, Kvaskoff M, Li Y, Zhang M, Qureshi AA, Missmer SA, et al. Severe teenage acne and risk of endometriosis. Hum Reprod. 2014;29:2592–9.CrossRefPubMed
99.
Shah DK, Correia KF, Vitonis AF, Missmer SA. Body size and endometriosis: results from 20 years of follow-up within the Nurses’ Health Study II prospective cohort. Hum Reprod. 2013;28:1783–92.CrossRefPubMedCentralPubMed
100.
Vercellini P, Buggio L, Somigliana E, Barbara G, Viganò P, Fedele L. Attractiveness of women with rectovaginal endometriosis: a case–control study. Fertil Steril. 2013;99:212–8.CrossRefPubMed
101.
Vercellini P, Buggio L, Somigliana E, Dridi D, Marchese MA, Viganò P. ‘Behind blue eyes’: the association between eye colour and deep infiltrating endometriosis. Hum Reprod. 2014;29:2171–5.CrossRefPubMed
102.
Buggio L, Vercellini P, Somigliana E, Viganò P, Frattaruolo MP, Fedele L. “You are so beautiful”: behind women’s attractiveness towards the biology of reproduction: a narrative review. Gynecol Endocrinol. 2012;28:753–7.CrossRefPubMed
103.
Atkinson J, Pipitone RN, Sorokowska A, Sorokowski P, Mberira M, Bartels A, et al. Voice and handgrip strength predict reproductive success in a group of indigenous African females. PLoS One. 2012;7, e41811.CrossRefPubMedCentralPubMed
104.
Arden R, Gottfredson LS, Miller G, Pierce A. Intelligence and semen quality are positively correlated. Intelligence. 2009;37:277–82.CrossRef
105.
Soler C, Kekäläinen J, Núñez M, Sancho M, Álvarez JG, Núñez J, et al. Male facial attractiveness and masculinity may provide sex- and culture-independent cues to semen quality. J Evol Biol. 2014;27:1930–8.CrossRefPubMed
106.
Peters M, Rhodes G, Simmons LW. Does attractiveness in men provide clues to semen quality? J Evol Biol. 2008;21:572–9.CrossRefPubMed
Metadata
Title
Infertility etiologies are genetically and clinically linked with other diseases in single meta-diseases
Authors
Juan J Tarín
Miguel A García-Pérez
Toshio Hamatani
Antonio Cano
Publication date
01-12-2015
Publisher
BioMed Central
Published in
Reproductive Biology and Endocrinology / Issue 1/2015
Electronic ISSN: 1477-7827
DOI
https://doi.org/10.1186/s12958-015-0029-9

Other articles of this Issue 1/2015

Reproductive Biology and Endocrinology 1/2015 Go to the issue

Research

Interaction between common variants of FTO and MC4R is associated with risk of PCOS

Research

A prepartum diet supplemented with oilseeds high in oleic or linoleic acid reduced GnRH-induced LH release in dairy cows during second week postpartum

Research

Predictive factors for ovarian response in a corifollitropin alfa/GnRH antagonist protocol for controlled ovarian stimulation in IVF/ICSI cycles

Research

Resveratrol relieves gestational diabetes mellitus in mice through activating AMPK

Research

Conjugated linoleic acid improves oocyte cryosurvival through modulation of the cryoprotectants influx rate

Research

Risk of endometrial polyps in women with endometriosis: a meta-analysis