International Journal of
Reproductive Biomedicine
Fri, May 3, 2024
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Volume 21, Issue 8 (August 2023)
IJRM 2023, 21(8): 599-618 |
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Zamani P, Hemati Z, Kelishadi R, Kolahdozan S, Dianatinasab M, Keikha M. Association between anogenital distance as a noninvasive index in the diagnosis and prognosis of reproductive disorder: A systematic review. IJRM 2023; 21 (8) :599-618
URL: http://ijrm.ir/article-1-2472-en.html
URL: http://ijrm.ir/article-1-2472-en.html
Parisa Zamani1 
, Zeinab Hemati2 , Roya Kelishadi2 , Sakineh Kolahdozan3 , Mostafa Dianatinasab4 , Mojtaba Keikha * 5
, Zeinab Hemati2 , Roya Kelishadi2 , Sakineh Kolahdozan3 , Mostafa Dianatinasab4 , Mojtaba Keikha * 5
1- Student Research Committee, School of Nursing and Midwifery, Shahroud University of Medical Sciences, Shahroud, Iran.
2- Child Growth and Development Research Center, Research Institute for Primordial Prevention of Non-Communicable Disease, Isfahan University of Medical Sciences, Isfahan, Iran.
3- Clinical Research Development Unit, Bahar Hospital, Shahroud University of Medical Sciences, Shahroud, Iran.
4- Department of Medical Sciences, School of Medical and Life Sciences, Sunway University, Malaysia. Department of Complex Genetics and Epidemiology, School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, The Netherlands.
5- Department of Biostatistics and Epidemiology, Faculty of Public Health, Kerman University of Medical Sciences, Kerman, Iran. , mr.mojtabakeikha@gmail.com
2- Child Growth and Development Research Center, Research Institute for Primordial Prevention of Non-Communicable Disease, Isfahan University of Medical Sciences, Isfahan, Iran.
3- Clinical Research Development Unit, Bahar Hospital, Shahroud University of Medical Sciences, Shahroud, Iran.
4- Department of Medical Sciences, School of Medical and Life Sciences, Sunway University, Malaysia. Department of Complex Genetics and Epidemiology, School of Nutrition and Translational Research in Metabolism, Maastricht University, Maastricht, The Netherlands.
5- Department of Biostatistics and Epidemiology, Faculty of Public Health, Kerman University of Medical Sciences, Kerman, Iran. , mr.mojtabakeikha@gmail.com
Abstract: (204 Views)
Background: There are 2 measures of anogenital distance (AGD) in men and women. AGD has been used as an indicator of fetal androgen dysfunction and an adverse outcome in adulthood. Some studies have shown the association of AGD as a predictor in the diagnosis and prognosis of diseases and disorders.
Objective: To systematically summarize the latest evidence for presenting AGD as a new approach for prognosis and early diagnosis of diseases.
Materials and Methods: A systematic review of the available literature was performed using Medline via PubMed, Scopus, and ISI Web of Knowledge up to July 2021, using search terms "anogenital distance" OR "anogenital index" OR "ano genital distance" OR "ano genital index". Language restrictions were not imposed.
Results: After reviewing the retrieved articles, 47 unique studies were included in this systematic review. Different outcomes, including endometriosis, prostate cancer, polycystic ovary syndrome, pelvic organ prolapse, hypospadias, cryptorchidism, fertility and semen parameters, maternal and birth development, and ovarian and gynecological-related disorders, have been studied in the included evidence. A negative association was observed between AGD and endometriosis and hypospadias and a positive association between AGD and prostate cancer, polycystic ovary syndrome, male fetal gender, and fertility parameters.
Conclusion: Using quantitative indicators such as AGD may be a useful clinical tool for the diagnosis of diseases. Although many studies have shown an association between AGD and diseases, some factors, including different measurement methods, different measurement tools, age, and different definitions of AGD, can be involved in the variation of AGD.
Corresponding Author: Mojtaba Keikha
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Objective: To systematically summarize the latest evidence for presenting AGD as a new approach for prognosis and early diagnosis of diseases.
Materials and Methods: A systematic review of the available literature was performed using Medline via PubMed, Scopus, and ISI Web of Knowledge up to July 2021, using search terms "anogenital distance" OR "anogenital index" OR "ano genital distance" OR "ano genital index". Language restrictions were not imposed.
Results: After reviewing the retrieved articles, 47 unique studies were included in this systematic review. Different outcomes, including endometriosis, prostate cancer, polycystic ovary syndrome, pelvic organ prolapse, hypospadias, cryptorchidism, fertility and semen parameters, maternal and birth development, and ovarian and gynecological-related disorders, have been studied in the included evidence. A negative association was observed between AGD and endometriosis and hypospadias and a positive association between AGD and prostate cancer, polycystic ovary syndrome, male fetal gender, and fertility parameters.
Conclusion: Using quantitative indicators such as AGD may be a useful clinical tool for the diagnosis of diseases. Although many studies have shown an association between AGD and diseases, some factors, including different measurement methods, different measurement tools, age, and different definitions of AGD, can be involved in the variation of AGD.
Corresponding Author: Mojtaba Keikha
View Orcid in Profile
You can search for this author in PubMed Google Scholar Profile
Type of Study: Review Article |
Subject:
Reproductive Epidemiology
References
1. Homan GF, Davies M, Norman R. The impact of lifestyle factors on reproductive performance in the general population and those undergoing infertility treatment: A review. Hum Reprod Update 2007; 13: 209-223. [DOI:10.1093/humupd/dml056] [PMID]
2. Johansson HKL, Svingen T, Fowler PA, Vinggaard AM, Boberg J. Environmental influences on ovarian dysgenesis - developmental windows sensitive to chemical exposures. Nat Rev Endocrinol 2017; 13: 400-414. [DOI:10.1038/nrendo.2017.36] [PMID]
3. Skakkebaek NE, Rajpert-De Meyts E, Buck Louis GM, Toppari J, Andersson AM, Eisenberg ML, et al. Male reproductive disorders and fertility trends: Influences of environment and genetic susceptibility. Physiol Rev 2016; 96: 55-97. [DOI:10.1152/physrev.00017.2015] [PMID] [PMCID]
4. Della Corte L, Di Filippo C, Gabrielli O, Reppuccia S, La Rosa VL, Ragusa R, et al. The burden of endometriosis on women's lifespan: A narrative overview on quality of life and psychosocial wellbeing. Int J Environ Res Public Health 2020; 17: 4683. [DOI:10.3390/ijerph17134683] [PMID] [PMCID]
5. Sánchez-Ferrer ML, Adoamnei E, Prieto-Sánchez MT, Mendiola J, Corbalán-Biyang Sh, Moñino-García M, et al. Health-related quality of life in women with polycystic ovary syndrome attending to a tertiary hospital in Southeastern Spain: A case-control study. Health Qual Life Outcomes 2020; 18: 232. [DOI:10.1186/s12955-020-01484-z] [PMID] [PMCID]
6. Main KM, Skakkebaek NE, Virtanen HE, Toppari J. Genital anomalies in boys and the environment. Best Pract Res Clin Endocrinol Metab 2010; 24: 279-289. [DOI:10.1016/j.beem.2009.10.003] [PMID]
7. Misseri R. Association between male genital anomalies and adult male reproductive disorders: A population-based data linkage study spanning more than 40 years. J Pediatr Urol 2020; 16: 504-505. [DOI:10.1016/j.jpurol.2020.07.010] [PMID]
8. Manríquez D, Velez J, Pinedo PJ. Incidence and risk factors for reproductive disorders in organic certified dairies. J Dairy Sci 2020; 103: 10797-10808. [DOI:10.3168/jds.2020-18592] [PMID]
9. Yang Sh, Shih Y-ChT, Huo J, Mehta HJ, Wu Y, Salloum RG, et al. Procedural complications associated with invasive diagnostic procedures after lung cancer screening with low-dose computed tomography. Lung Cancer 2022; 165: 141-144. [DOI:10.1016/j.lungcan.2021.12.020] [PMID] [PMCID]
10. Halliday SJ, Aboudara MC, Maldonado F. Complication rates in a study of invasive diagnostic procedures for lung abnormalities. JAMA Inter Med 2019; 179: 846-847. [DOI:10.1001/jamainternmed.2019.0960] [PMID]
11. Sipahi M, Tokgöz VY, Alanya Tosun Ş. An appropriate way to predict fetal gender at first trimester: Anogenital distance. J Matern Fetal Neonatal Med 2019; 32: 2012-2016. [DOI:10.1080/14767058.2018.1424131] [PMID]
12. Wainstock T, Yoles I, Sergienko R, Walfisch A. The association between anogenital distance, reproductive and general health in adult females- a prospective cohort of 17 years. Reprod Toxicol 2019; 90: 77-81. [DOI:10.1016/j.reprotox.2019.08.007] [PMID]
13. Di Nisio A, Sabovic I, Valente U, Tescari S, Rocca MS, Guidolin D, et al. Endocrine disruption of androgenic activity by perfluoroalkyl substances: Clinical and experimental evidence. J Clin Endocrinol Metab 2019; 104: 1259-1271. [DOI:10.1210/jc.2018-01855] [PMID]
14. Lymperi S, Giwercman A. Endocrine disruptors and testicular function. Metabolism 2018; 86: 79-90. [DOI:10.1016/j.metabol.2018.03.022] [PMID]
15. Suzuki Y, Yoshinaga J, Mizumoto Y, Serizawa S, Shiraishi H. Foetal exposure to phthalate esters and anogenital distance in male newborns. Int J Androl 2012; 35: 236-244. [DOI:10.1111/j.1365-2605.2011.01190.x] [PMID]
16. Liu C, Xu X, Huo X. Anogenital distance and its application in environmental health research. Environ Sci Pollut Res Int 2014; 21: 5457-5464. [DOI:10.1007/s11356-014-2570-z] [PMID]
17. Kurzrock EA, Jegatheesan P, Cunha GR, Baskin LS. Urethral development in the fetal rabbit and induction of hypospadias: A model for human development. J Urol 2000; 164: 1786-1792.
https://doi.org/10.1016/S0022-5347(05)67107-8 [DOI:10.1097/00005392-200011000-00102] [PMID]
18. Dean A, Sharpe RM. Clinical review: Anogenital distance or digit length ratio as measures of fetal androgen exposure: Relationship to male reproductive development and its disorders. J Clin Endocrinol Metab 2013; 98: 2230-2238. [DOI:10.1210/jc.2012-4057] [PMID]
19. Adibi JJ, Lee MK, Naimi AI, Barrett E, Nguyen RH, Sathyanarayana S, et al. Human chorionic gonadotropin partially mediates phthalate association with male and female anogenital distance. J Clin Endocrinol Metab 2015; 100: E1216-E1224. [DOI:10.1210/jc.2015-2370] [PMID] [PMCID]
20. Aydin E, Holt R, Chaplin D, Hawkes R, Allison C, Hackett G, et al. Fetal anogenital distance using ultrasound. Prenat Diagn 2019; 39: 527-535. [DOI:10.1002/pd.5459] [PMID] [PMCID]
21. Mendiola J, Sánchez-Ferrer ML, Jiménez-Velázquez R, Cánovas-López L, Hernández-Peñalver AI, Corbalán-Biyang S, et al. Endometriomas and deep infiltrating endometriosis in adulthood are strongly associated with anogenital distance, a biomarker for prenatal hormonal environment. Hum Reprod 2016; 31: 2377-2383. [DOI:10.1093/humrep/dew163] [PMID] [PMCID]
22. Parra MD, Mendiola J, Jørgensen N, Swan SH, Torres-Cantero AM. Anogenital distance and reproductive parameters in young men. Andrologia 2016; 48: 3-10. [DOI:10.1111/and.12403] [PMID]
23. Zarean M, Keikha M, Feizi A, Kazemitabaee M, Kelishadi R. The role of exposure to phthalates in variations of anogenital distance: A systematic review and meta-analysis. Environ Pollut 2019; 247: 172-179. [DOI:10.1016/j.envpol.2019.01.026] [PMID]
24. Zhou N, Sun L, Yang H, Chen Q, Wang X, Yang H, et al. Anogenital distance is associated with serum reproductive hormones, but not with semen quality in young men. Hum Reprod 2016; 31: 958-967. [DOI:10.1093/humrep/dew052] [PMID]
25. Thankamony A, Pasterski V, Ong KK, Acerini CL, Hughes IA. Anogenital distance as a marker of androgen exposure in humans. Andrology 2016; 4: 616-625. [DOI:10.1111/andr.12156] [PMID] [PMCID]
26. Schwartz CL, Christiansen S, Vinggaard AM, Axelstad M, Hass U, Svingen T. Anogenital distance as a toxicological or clinical marker for fetal androgen action and risk for reproductive disorders. Arch Toxicol 2019; 93: 253-272. [DOI:10.1007/s00204-018-2350-5] [PMID]
27. Jain VG, Goyal V, Chowdhary V, Swarup N, Singh RJ, Singal A, et al. Anogenital distance is determined during early gestation in humans. Hum Reprod 2018; 33: 1619-1627. [DOI:10.1093/humrep/dey265] [PMID]
28. Freire C, Ocón-Hernández O, Dávila-Arias C, Pérez-Lobato R, Calvente I, Ramos R, et al. Anogenital distance and reproductive outcomes in 9-to 11-year-old boys: the INMA-Granada cohort study. Andrology 2018; 6: 874-881. [DOI:10.1111/andr.12544] [PMID]
29. Sánchez-Ferrer ML, Moya-Jiménez LC, Mendiola J. Comparison of the anogenital distance and anthropometry of the perineum in patients with and without pelvic organ prolapse. Actas Urol Esp 2016; 40: 628-634. [DOI:10.1016/j.acuro.2016.04.004] [PMID]
30. Gilboa Y, Perlman S, Kivilevitch Z, Messing B, Achiron R. Prenatal anogenital distance is shorter in fetuses with hypospadias. J Ultrasound Med 2017; 36: 175-182. [DOI:10.7863/ultra.16.01006] [PMID]
31. Wu Y, Zhong G, Chen Sh, Zheng Ch, Liao D, Xie M. Polycystic ovary syndrome is associated with anogenital distance, a marker of prenatal androgen exposure. Hum Reprod 2017; 32: 937-943. [DOI:10.1093/humrep/dex042] [PMID]
32. Sánchez-Ferrer ML, Mendiola J, Hernández-Peñalver AI, Corbalán-Biyang S, Carmona-Barnosi A, Prieto-Sánchez MT, et al. Presence of polycystic ovary syndrome is associated with longer anogenital distance in adult Mediterranean women. Hum Reprod 2017; 32: 2315-2323. [DOI:10.1093/humrep/dex274] [PMID]
33. Fabregues F, González-Foruria I, Peñarrubia J, Carmona F. Ovarian response is associated with anogenital distance in patients undergoing controlled ovarian stimulation for IVF. Hum Reprod 2018; 33: 1696-1704. [DOI:10.1093/humrep/dey244] [PMID]
34. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. PLoS Med 2009; 6: e1000097. [DOI:10.1371/journal.pmed.1000097] [PMID] [PMCID]
35. Wells GA, O'Connell D, Peterson J, Welch V, Losos M, Fogwell P. The newcastle-ottawa scale (NOS) for assessing the quality of nonrandomised studies in meta-analysis. Available at: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp.
36. Sánchez-Ferrer ML, Jiménez-Velázquez R, Mendiola J, Prieto-Sánchez MT, Cánovas-López L, Carmona-Barnosi A, et al. Accuracy of anogenital distance and anti-müllerian hormone in the diagnosis of endometriosis without surgery. Int J Gynaecol Obstet 2019; 144: 90-96. [DOI:10.1002/ijgo.12691] [PMID]
37. Sánchez-Ferrer Ml, Mendiola J, Jiménez-Velázquez R, Cánovas-López L, Corbalán-Biyang S, Hernández-Peñalver AI, et al. Investigation of anogenital distance as a diagnostic tool in endometriosis. Reprod Biomed Online 2017; 34: 375-382. [DOI:10.1016/j.rbmo.2017.01.002] [PMID]
38. Crestani A, Arfi A, Ploteau S, Breban M, Boudy A-S, Bendifallah S, et al. Anogenital distance in adult women is a strong marker of endometriosis: Results of a prospective study with laparoscopic and histological findings. Hum Reprod Open 2020; 3: 1-9. [DOI:10.1093/hropen/hoaa023] [PMID] [PMCID]
39. Maldonado-Cárceles AB, Sánchez-Rodríguez C, Vera-Porras EM, Árense-Gonzalo JJ, Oñate-Celdrán J, Samper-Mateo P, et al. Anogenital distance, a biomarker of prenatal androgen exposure is associated with prostate cancer severity. Prostate 2017; 77: 406-411. [DOI:10.1002/pros.23279] [PMID]
40. Oñate-Celdrán J, Arense-Gonzalo JJ, Mendiola J, Samper-Mateo P, Sánchez-Rodríguez C, García-Escudero D, et al. [Prostate cancer is associated with the anogenital distance, a biomarker of prenatal androgen milieu]. Arch Esp Urol 2019; 72: 9-15. (in Spanish)
41. Castaño-Vinyals G, Carrasco E, Lorente JA, Sabaté Y, Cirac-Claveras J, Pollán M, et al. Anogenital distance and the risk of prostate cancer. BJU Int 2012; 110: E707-E710. [DOI:10.1111/j.1464-410X.2012.11516.x] [PMID]
42. Sahin A, Kutluhan MA, Toprak T, Vural Y, Ürkmez A, Akan S, et al. Assesment of anogenital distance as a marker in diagnosis of prostate cancer. Arch Ital Urol Androl 2019; 91: 163-165. [DOI:10.4081/aiua.2019.3.163] [PMID]
43. Hernández-Peñalver AI, Sánchez-Ferrer ML, Mendiola J, Adoamnei E, Prieto-Sánchez MT, Corbalán-Biyang S, et al. Assessment of anogenital distance as a diagnostic tool in polycystic ovary syndrome. Reprod Biomed Online 2018; 37: 741-749. [DOI:10.1016/j.rbmo.2018.08.020] [PMID]
44. Barrett E, Hoeger K, Sathyanarayana S, Redmon JB, Nguyen R, Swan SH. Anogenital distance, a biomarker of prenatal androgen exposure, is longer among newborn daughters of women with polycystic ovary syndrome (PCOS). Endocr Rev 2016; 37 (Suppl.).
45. Simsir C, Pekcan MK, Aksoy RT, Ecemis T, Coskun B, Kilic SH, et al. The ratio of anterior anogenital distance to posterior anogenital distance: A novel-biomarker for polycystic ovary syndrome. J Chin Med Assoc 2019; 82: 782-786. [DOI:10.1097/JCMA.0000000000000150] [PMID]
46. Sánchez-Ferrer ML, Prieto-Sánchez MT, Moya-Jiménez C, Mendiola J, García-Hernández CM, Carmona-Barnosi A, et al. Anogenital distance and perineal measurements of the pelvic organ prolapse (POP) quantification system. J Vis Exp 2018; 139: 57912.
https://doi.org/10.3791/57912 [DOI:10.3791/57912-v] [PMID] [PMCID]
47. Arfi A, Cohen J, Canlorbe G, Bendifallah S, Thomassin-Naggara I, Darai E, et al. First-trimester determination of fetal gender by ultrasound: Measurement of the ano-genital distance. Eur J Obstet Gynecol Reprod Biol 2016; 203: 177-181. [DOI:10.1016/j.ejogrb.2016.06.001] [PMID]
48. Fowler PA, Filis P, Bhattacharya S, Bizec Bl, Antignac J-P, Morvan M-L, et al. Human anogenital distance: An update on fetal smoke-exposure and integration of the perinatal literature on sex differences. Hum Reprod 2016; 31: 463-472. [DOI:10.1093/humrep/dev323] [PMID] [PMCID]
49. Najdi N, Safi F, Hashemi-Dizaji S, Sahraian G, Jand Y. First trimester determination of fetal gender by ultrasonographic measurement of anogenital distance: A cross-sectional study. Int J Reprod BioMed 2019; 17: 51-56. [DOI:10.18502/ijrm.v17i1.3820] [PMID] [PMCID]
50. Cox K, Kyriakou A, Amjad B, O'Toole S, Flett ME, Welsh M, et al. Shorter anogenital and anoscrotal distances correlate with the severity of hypospadias: A prospective study. J Pediatr Urol 2017; 13: 57. [DOI:10.1016/j.jpurol.2016.08.006] [PMID]
51. Hsieh MH, Breyer BN, Eisenberg ML, Baskin LS. Associations among hypospadias, cryptorchidism, anogenital distance, and endocrine disruption. Curr Urol Rep 2008; 9: 137-142. [DOI:10.1007/s11934-008-0025-0] [PMID]
52. Singal AK, Jain VG, Gazali Z, Shekhawat P. Shorter anogenital distance correlates with the severity of hypospadias in pre-pubertal boys. Hum Reprod 2016; 31: 1406-1410. [DOI:10.1093/humrep/dew115] [PMID]
53. Thankamony A, Lek N, Carroll D, Williams M, Dunger DB, Acerini CL, et al. Anogenital distance and penile length in infants with hypospadias or cryptorchidism: Comparison with normative data. Environ Health Perspect 2014; 122: 207-211. [DOI:10.1289/ehp.1307178] [PMID] [PMCID]
54. Eisenberg ML, Lipshultz LI. Anogenital distance as a measure of human male fertility. J Assist Reprod Genet 2015; 32: 479-484. [DOI:10.1007/s10815-014-0410-1] [PMID] [PMCID]
55. Mendiola J, Melgarejo M, Moñino-García M, Cutillas-Tolín A, Noguera-Velasco JA, Torres-Cantero AM. Is anogenital distance associated with semen quality in male partners of subfertile couples? Andrology 2015; 3: 672-676. [DOI:10.1111/andr.12059] [PMID]
56. Mendiola J, Stahlhut RW, Jørgensen N, Liu F, Swan SH. Shorter anogenital distance predicts poorer semen quality in young men in Rochester, New York. Environ Health Perspect 2011; 119: 958-963. [DOI:10.1289/ehp.1103421] [PMID] [PMCID]
57. Mira-Escolano MP, Mendiola J, Mı'nguez-Alarco'n L, Melgarejo M, Cutillas-Tolı'n A, Roca M, et al. Longer anogenital distance is associated with higher testosterone levels in women: A cross-sectional study. BJOG 2014; 121: 1359-1364. [DOI:10.1111/1471-0528.12627] [PMID]
58. Eisenberg ML, Hsieh MH, Walters RC, Krasnow R, Lipshultz LI. The relationship between anogenital distance, fatherhood, and fertility in adult men. PLoS One 2011; 6: e18973. [DOI:10.1371/journal.pone.0018973] [PMID] [PMCID]
59. Glintborg D, Jensen RC, Schmedes AV, Brandslund I, Kyhl HB, Jensen TK, et al. Anogenital distance in children born of mothers with polycystic ovary syndrome: the Odense child cohort. Hum Reprod 2019; 34: 2061-2070. [DOI:10.1093/humrep/dez122] [PMID]
60. Wainstock T, Shoham-Vardi I, Sheiner E, Walfisch A. Fertility and anogenital distance in women. Reprod Toxicol 2017; 73: 345-349. [DOI:10.1016/j.reprotox.2017.07.009] [PMID]
61. Moya-Jiménez LC, Sánchez-Ferrer ML, Adoamnei E, Mendiola J. New approach to the evaluation of perineal measurements to predict the likelihood of the need for an episiotomy. Int Urogynecol J 2018; 30: 815-821. [DOI:10.1007/s00192-018-3745-9] [PMID]
62. Eisenberg ML, Shy M, Herder D, Walters RC, Lipshultz LI. The relationship between anogenital distance and the efficacy of varicocele repair. BJU Int 2012; 110: E927-E930. [DOI:10.1111/j.1464-410X.2012.11154.x]
63. Jain VG, Singal AK. Shorter anogenital distance correlates with undescended testis: A detailed genital anthropometric analysis in human newborns. Hum Reprod 2013; 28: 2343-2349. [DOI:10.1093/humrep/det286] [PMID]
64. Domenici L, Musella A, Bracchi C, Lecce F, Schiavi MC, Colagiovanni V, et al. Comparison of anogenital distance and correlation with vulvo-vaginal atrophy: A pilot study on premenopausal and postmenopausal women. J Menopausal Med 2018; 24: 108-112. [DOI:10.6118/jmm.2018.24.2.108] [PMID] [PMCID]
65. Toprak T, Şahin A, Akgul K, Kutluhan MA, Ramazanoglu MA, Yilmaz M, et al. The relationship between anogenital distance and lifelong premature ejaculation. Andrology 2020; 8: 353-357. [DOI:10.1111/andr.12709] [PMID]
66. Sertkaya Z, Ertaş K, Tokuç E. The relationship between premature ejaculation and anogenital distance. Andrologia 2020; 52: e13571. [DOI:10.1111/and.13571]
67. Mendiola J, Roca M, Mínguez-Alarcón L, Mira-Escolano MP, López-Espín JJ, Barrett ES, et al. Anogenital distance is related to ovarian follicular number in young Spanish women: A cross-sectional study. Environ Health 2012; 11: 90. [DOI:10.1186/1476-069X-11-90] [PMID] [PMCID]
68. Park JY, Lim G, Oh KW, Ryu DS, Park S, Jeon JC, et al. Penile length, digit length, and anogenital distance according to birth weight in newborn male infants. Korean J Urol 2015; 56: 248-253. [DOI:10.4111/kju.2015.56.3.248] [PMID] [PMCID]
69. Liu R, Xu X, Zhang Y, Zheng X, Kim SS, Dietrich KN, et al. Thyroid hormone status in umbilical cord serum is positively associated with male anogenital distance. J Clin Endocrinol Metab 2015; 10: 3378-3385. [DOI:10.1210/jc.2015-3872] [PMID] [PMCID]
70. Singal AK, Jain VG. Maternal and infant characteristics influencing the anogenital distance and penile length in newborns. Andrologia 2016; 48: 708-713. [DOI:10.1111/and.12507] [PMID]
71. Mira-Escolano MP, Mendiola J, Mı'nguez-Alarco'n L, Roca M, Cutillas-Tolı'n A, pez-Espı'n JJL, et al. Anogenital distance of women in relation to their mother's gynaecological characteristics before or during pregnancy. Reprod Biomed Online 2014; 28: 209-215. [DOI:10.1016/j.rbmo.2013.09.026] [PMID]
72. Swan SH, Sathyanarayana S, Barrett ES, Janssen S, Liu F, Nguyen RH, et al. First trimester phthalate exposure and anogenital distance in newborns. Hum Reprod 2015; 30: 963-972. [DOI:10.1093/humrep/deu363] [PMID] [PMCID]
73. Gilboa Y, Kivilevitch Z, Oren M, Cohen YP, Katorza E, Achiron R. Anogenital distance in male and female fetuses at 20 to 35 weeks of gestation: Centile charts and reference ranges. Prenat Diagn 2014; 34: 946-951. [DOI:10.1002/pd.4399] [PMID]
74. Boyle P, Koechlin A, Bota M, Onofrio A, Zaridze DG, Perrin P, et al. Endogenous and exogenous testosterone and the risk of prostate cancer and increased prostate-specific antigen (PSA) level: A meta-analysis. BJU Int 2016; 118: 731-741. [DOI:10.1111/bju.13417] [PMID]
75. Barry JA, Kay AR, Navaratnarajah R, Iqbal S, Bamfo JEAK, David AL, et al. Umbilical vein testosterone in female infants born to mothers with polycystic ovary syndrome is elevated to male levels. J Obstet Gynaecol 2010; 30: 444-446. [DOI:10.3109/01443615.2010.485254] [PMID]
76. Wu X-Y, Li Zh-L, Wu Ch-Y, Liu Y-M, Lin H, Wang Sh-H, et al. Endocrine traits of polycystic ovary syndrome in prenatally androgenized female Sprague-Dawley rats. Endocr J 2010; 57: 201-209. [DOI:10.1507/endocrj.K09E-205] [PMID]
77. Hart R, Doherty DA, Norman RJ, Franks S, Dickinson JE, Hickey M, et al. Serum anti-Mullerian hormone (AMH) levels are elevated in adolescent girls with polycystic ovaries and the polycystic ovarian syndrome (PCOS). Fertil Steril 2010; 94: 1118-1121. [DOI:10.1016/j.fertnstert.2009.11.002] [PMID]
78. Barrett ES, Hoeger KM, Sathyanarayana S, Abbott DH, Redmon JB, Nguyen RHN. Anogenital distance in newborn daughters of women with polycystic ovary syndrome indicates fetal testosterone exposure. J Dev Orig Health Dis 2018; 9: 307-314. [DOI:10.1017/S2040174417001118] [PMID] [PMCID]
79. Swan SH. Environmental phthalate exposure in relation to reproductive outcomes and other health endpoints in humans. Environ Res 2008; 108: 177-184. [DOI:10.1016/j.envres.2008.08.007] [PMID] [PMCID]
80. Khunda A, Shek KL, Dietz HP. Can ballooning of the levator hiatus be determined clinically? Am J Obstet Gynecol 2012; 206: e1-e4. [DOI:10.1016/j.ajog.2011.10.876] [PMID]
81. Dietz HP. Ultrasound imaging of the pelvic floor. Part II: Three-dimensional or volume imaging. Ultrasound Obstet Gynecol 2004; 23: 615-625. [DOI:10.1002/uog.1072] [PMID]
82. Salazar-Martinez E, Romano-Riquer P, Yanez-Marquez E, Longnecker MP, Hernandez-Avila M. Anogenital distance in human male and female newborns: A descriptive, cross-sectional study. Environ Health Perspect 2004; 3: 8. [DOI:10.1186/1476-069X-3-8] [PMID] [PMCID]
83. Hua X-G, Hu R, Hu Ch-Y, Li FL, Jiang W, Zhang XJ. Associations between hypospadias, cryptorchidism and anogenital distance: Systematic review and meta‐analysis. Andrologia 2018; 50: e13152. [DOI:10.1111/and.13152] [PMID]
84. Swan SH, Main KM, Liu F, Stewart SL, Kruse RL, Calafat AM, et al. Decrease in anogenital distance among male infants with prenatal phthalate exposure. Environ Health Perspect 2005; 113: 1056-1061. [DOI:10.1289/ehp.8100] [PMID] [PMCID]
85. Eid SM. Is perineal body length measurement reinforcing the decision about performance or avoidance of episiotomy? Asian Acad Manage J 2011; 3: 209-226.
86. Barrett ES, Parlett LE, Swan SH. Stability of proposed biomarkers of prenatal androgen exposure over the menstrual cycle. J Dev Orig Health Dis 2015; 6: 149-157. [DOI:10.1017/S2040174414000646] [PMID] [PMCID]
87. Lee JW, Kim NH, Milanesi A. Thyroid hormone signaling in muscle development, repair and metabolism. J Endocrinol Diabetes Obes 2014; 2: 1046.
88. Loubière LS, Vasilopoulou E, Glazier JD, Taylor PM, Franklyn JA, Kilby MD, et al. Expression and function of thyroid hormone transporters in the microvillous plasma membrane of human term placental syncytiotrophoblast. Endocrinology 2012; 153: 6126-6135. [DOI:10.1210/en.2012-1753] [PMID] [PMCID]
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