The use of follicle stimulating hormone (FSH) for the treatment of the infertile man: position statement from the Italian Society of Andrology and Sexual Medicine (SIAMS)

Journal of Endocrinological Investigation

Volumn 41, Issue 9, 2018, Pages 1107-1122

  Barbonetti, A ^a   Calogero, A E ^b   Balercia, G ^c   Garolla, A ^d   Krausz, C ^e   La Vignera, S ^b   Lombardo, F ^f   Jannini, E A ^g   Maggi, M ^e   Lenzi, A ^f   Foresta, C ^d   Ferlin, A ^d,h  

^a Casa di Cura San Raffaele Sulmona   (Italy)

^b UNIVERSITY OF CATANIA   (Italy)

^c UNIVERSITÀ POLITECNICA DELLE MARCHE   (Italy)

^d UNIVERSITY OF PADOVA   (Italy)

^e UNIVERSITY OF FLORENCE   (Italy)

^f SAPIENZA UNIVERSITY OF ROME   (Italy)

^g UNIVERSITY OF ROME TOR VERGATA   (Italy)

^h UNIVERSITY OF BRESCIA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; PLACEBO; RECOMBINANT FOLLITROPIN; SPERM DNA; UNCLASSIFIED DRUG; FOLLITROPIN;

ARTICLE; AZOOSPERMIA; CONSENSUS DEVELOPMENT; DNA FRAGMENTATION; DNA STRAND BREAKAGE; DRUG EFFICACY; EMBRYO TRANSFER; EVIDENCE BASED MEDICINE; FEMALE INFERTILITY; GENETIC POLYMORPHISM; HUMAN; IN VITRO FERTILIZATION; INFERTILITY THERAPY; MALE INFERTILITY; OLIGOASTHENOTERATOZOOSPERMIA; OLIGOSPERMIA; OUTCOME ASSESSMENT; PHARMACOGENETICS; PREGNANCY RATE; PRESCRIPTION; SPERMATOZOON ABNORMALITY; SPERMATOZOON DENSITY; SPERMATOZOON MOTILITY; TREATMENT DURATION; TREATMENT RESPONSE; ADULT; ANDROLOGY; CONSENSUS; DRUG EFFECT; FEMALE; ITALY; MALE; MEDICAL SOCIETY; METABOLISM; ORGANIZATION AND MANAGEMENT; PRACTICE GUIDELINE; PREGNANCY; REPRODUCTION; SEMEN ANALYSIS; SPERMATOZOON; STANDARDS;

ADULT; ANDROLOGY; CONSENSUS; DNA FRAGMENTATION; FEMALE; FOLLICLE STIMULATING HORMONE; HUMANS; INFERTILITY, MALE; ITALY; MALE; PREGNANCY; PREGNANCY RATE; REPRODUCTIVE MEDICINE; SEMEN ANALYSIS; SOCIETIES, MEDICAL; SPERMATOZOA;

EID: 85045139021     PISSN: 03914097     EISSN: 17208386     Source Type: Journal    
DOI: 10.1007/s40618-018-0843-y     Document Type: Article

References (83)

1. Isaksson R, Tiitinen A (2004) Present concept of unexplained infertility. Gynecol Endocrinol 18(5):278–290
2. Krausz C (2011) Male infertility: pathogenesis and clinical diagnosis. Best Pract Res Clin Endocrinol Metab 25(2):271–285
3. Tournaye H, Krausz C, Oates RD (2017) Novel concepts in the aetiology of male reproductive impairment. Lancet Diabetes Endocrinol 5(7):544–553
4. Wang SX (2011) The past, present, and future of embryo selection in in vitro fertilization: frontiers in reproduction conference. Yale J Biol Med 84(4):487–490
5. Singh K, Jaiswal D (2011) Human male infertility: a complex multifactorial phenotype. Reprod Sci 18(5):418–425
6. Hirsh A (2003) Male subfertility. BMJ 327(7416):669–672
7. Baccetti B, Strehler E, Capitani S, Collodel G, De Santo M, Moretti E et al (1997) The effect of follicle-stimulating hormone therapy on human sperm structure (Notulae seminologicae). Hum Reprod 12(9):1955–1968
8. Kliesch S, Behre HM, Nieschlag E (1995) Recombinant human follicle stimulating hormone and human chorionic gonadotropin for induction of spermatogenesis in a hypogonadal male. Fertil Steril 63(6):1326–1328
9. van Rijkom J, Leufkens H, Crommelin D, Rutten F, Broekmans A (1999) Assessment of biotechnology drugs: what are the issues? Health Policy 47(3):255–274
10. Zwart-van Rijkom JE, Broekmans FJ, Leufkens HG (2002) From HMG through purified urinary FSH preparations to recombinant FSH: a substitution study. Hum Reprod 17(4):857–865
11. Vicari E, Mongioì A, Calogero AE, Moncada ML, Sidoti G, Polosa P, D’Agata R (1992) Therapy with human chorionic gonadotrophin alone induces spermatogenesis in men with isolated hypogonadotrophic hypogonadism-long-term follow-up. Int J Androl 15(4):320–329
12. Zacharin M, Sabin MA, Nair VV, Dabadghao P (2012) Addition of recombinant follicle-stimulating hormone to human chorionic gonadotropin treatment in adolescents and young adults with hypogonadotropic hypogonadism promotes normal testicular growth and may promote early spermatogenesis. Fertil Steril 98(4):836–842
13. La Vignera S, Condorelli RA, Cimino L, Russo GI, Morgia G, Calogero AE (2016) Late-onset hypogonadism: the advantages of treatment with human chorionic gonadotropin rather than testosterone. Aging Male 19(1):34–39
14. Acosta AA, Oehninger S, Ertunc H, Philput C (1991) Possible role of pure human follicle-stimulating hormone in the treatment of severe male infertility by assisted reproduction: preliminary report. Fertil Steril 55(6):1150–1156
15. Acosta AA, Khalifa E, Oehninger S (1992) Pure human follicle stimulating hormone has a role in the treatment of severe male infertility by assisted reproduction: Norfolk’s total experience. Hum Reprod 7(8):1067–1072
16. Bartoov B, Eltes F, Lunenfeld E, Har-Even D, Lederman H, Lunenfeld B (1994) Sperm quality of subfertile males before and after treatment with human follicle-stimulating hormone. Fertil Steril 61(4):727–734
17. Matorras R, Perez C, Corcostegui B, Pijoan JI, Ramon O, Delgado P et al (1997) Treatment of the male with follicle-stimulating hormone in intrauterine insemination with husband’s spermatozoa: a randomized study. Hum Reprod 12(1):24–28
18. Kamischke A, Behre HM, Bergmann M, Simoni M, Schäfer T, Nieschlag E (1998) Recombinant human follicle stimulating hormone for treatment of male idiopathic infertility: a randomized, double-blind, placebo-controlled, clinical trial. Hum Reprod 13(3):596–603
19. Ben-Rafael Z, Farhi J, Feldberg D, Bartoov B, Kovo M, Eltes F et al (2000) Follicle-stimulating hormone treatment for men with idiopathic oligoteratoasthenozoospermia before in vitro fertilization: the impact on sperm microstructure and fertilization potential. Fertil Steril 73(1):24–30
20. Baccetti B, Piomboni P, Bruni E, Capitani S, Gambera L, Moretti E et al (2004) Effect of follicle-stimulating hormone on sperm quality and pregnancy rate. Asian J Androl 6(2):133–137
21. Foresta C, Bettella A, Garolla A, Ambrosini G, Ferlin A (2005) Treatment of male idiopathic infertility with recombinant human follicle-stimulating hormone: a prospective, controlled, randomized clinical study. Fertil Steril 84(3):654–661
22. Efesoy O, Cayan S, Akbay E (2009) The efficacy of recombinant human follicle-stimulating hormone in the treatment of various types of male-factor infertility at a single university hospital. J Androl 30(6):679–684
23. Colacurci N, Monti MG, Fornaro F, Izzo G, Izzo P, Trotta C et al (2012) Recombinant human FSH reduces sperm DNA fragmentation in men with idiopathic oligoasthenoteratozoospermia. J Androl 33(4):588–593
24. Ding YM, Zhang XJ, Li JP, Chen SS, Zhang RT, Tan WL et al (2015) Treatment of idiopathic oligozoospermia with recombinant human follicle-stimulating hormone: a prospective, randomized, double-blind, placebo-controlled clinical study in Chinese population. Clin Endocrinol (Oxf) 83(6):866–871
25. Sigg C, Baclu M (1994) Improvement of sperm concentration and bovine mucus penetration in idiopathic oligozoospermia by administration of pure FSH. Hum Reprod 9(Suppl 4):47
26. Merino G, Carranza-Lira S, Martinez-Chequer JC (1996) Sperm characteristics and hormonal profile before and after treatment with follicle-stimulating hormone in infertile patients. Arch Androl 37(3):197–200
27. Strehler E, Sterzik K, De Santo M, Abt M, Wiedemann R, Bellati U et al (1997) The effect of follicle-stimulating hormone therapy on sperm quality: an ultrastructural mathematical evaluation. J Androl 18(4):439–447
28. Glander HJ, Kratzsch J (1997) Effects of pure human follicle stimulating hormone (pFSH) on sperm quality correlate with the hypophyseal response to gonadotropin-releasing hormone (GnRH). Andrologia 29(1):23–28
29. Radicioni A, Schwarzenberg TL (1999) The use of FSH in adolescents and young adults with idiopathic, unilateral, left varicocele not undergoing surgical intervention. Preliminary study. Minerva Endocrinol 24(2):63–68
30. Arnaldi G, Balercia G, Barbatelli G, Mantero F (2000) Effects of long-term treatment with human pure follicle-stimulating hormone on semen parameters and sperm-cell ultrastructure in idiopathic oligoteratoasthenozoospermia. Andrologia 32(3):155–161
31. Foresta C, Bettella A, Merico M, Garolla A, Plebani M, Ferlin A et al (2000) FSH in the treatment of oligozoospermia. Mol Cell Endocrinol 161(1–2):89–97
32. Zarrilli S, Paesano L, Colao A, Mirone V, Lombardi G, De Rosa M (2000) FSH treatment improves sperm function in patients after varicocelectomy. J Endocrinol Invest 23(2):68–73
33. Caroppo E, Niederberger C, Vizziello GM, D’Amato G (2003) Recombinant human follicle-stimulating hormone as a pretreatment for idiopathic oligoasthenoteratozoospermic patients undergoing intracytoplasmic sperm injection. Fertil Steril 80(6):1398–1403
34. Fernández-Arjona M, Díaz J, Cortes I, González J, Rodriguez JM, Alvarez E (2003) Relationship between gonadotrophin secretion, inhibin B and spermatogenesis in oligozoospermic men treated with highly purified urinary follicle-stimulating hormone (uFSH-HP): a preliminary report. Eur J Obstet Gynecol Reprod Biol 107(1):47–51
35. Paradisi R, Busacchi P, Seracchioli R, Porcu E, Venturoli S (2006) Effects of high doses of recombinant human follicle-stimulating hormone in the treatment of male factor infertility: results of a pilot study. Fertil Steril 86(3):728–731
36. Valenti D, La Vignera S, Condorelli RA, Rago R, Barone N, Vicari E et al (2013) Follicle-stimulating hormone treatment in normogonadotropic infertile men. Nat Rev Urol 10(1):55–62
37. Condorelli RA, Calogero AE, Vicari E, Mongioi’ L, Burgio G, Cannarella R et al (2014) Reduced seminal concentration of CD45pos cells after follicle-stimulating hormone treatment in selected patients with idiopathic oligoasthenoteratozoospermia. Int J Endocrinol 2014:372060
38. Paradisi R, Natali F, Fabbri R, Battaglia C, Seracchioli R, Venturoli S (2014) Evidence for a stimulatory role of high doses of recombinant human follicle-stimulating hormone in the treatment of male-factor infertility. Andrologia 46(9):1067–1072
39. Farrag A, Sagnella F, Pappalardo S, Costantini A, Lisi F, Carfagna P et al (2015) The use of r-hFSH in treatment of idiopathic male factor infertility before ICSI. Eur Rev Med Pharmacol Sci 19(12):2162–2167
40. Casamonti E, Vinci S, Serra E, Fino MG, Brilli S, Lotti F et al (2017) Short-term FSH treatment and sperm maturation: a prospective study in idiopathic infertile men. Andrology 5(3):414–422
41. Garolla A, Ghezzi M, Cosci I, Sartini B, Bottacin A, Engl B et al (2017) FSH treatment in infertile males candidate to assisted reproduction improved sperm DNA fragmentation and pregnancy rate. Endocrine 56(2):416–425
42. Attia AM, Abou-Setta AM, Al-Inany HG (2013) Gonadotrophins for idiopathic male factor subfertility. Cochrane Database Syst Rev 23(8):CD005071
43. Santi D, Granata AR, Simoni M (2015) FSH treatment of male idiopathic infertility improves pregnancy rate: a meta-analysis. Endocr Connect 4(3):R46–R58
44. Swiglo BA, Murad MH, Schünemann HJ, Kunz R, Vigersky RA, Guyatt GH et al (2008) A case for clarity, consistency, and helpfulness: state-of-the-art clinical practice guidelines in endocrinology using the grading of recommendations, assessment, development, and evaluation system. J Clin Endocrinol Metab 93(3):666–673
45. Palomba S, Falbo A, Espinola S, Rocca M, Capasso S, Cappiello F et al (2011) Effects of highly purified follicle-stimulating hormone on sperm DNA damage in men with male idiopathic subfertility: a pilot study. J Endocrinol Invest 34(10):747–752
46. Foresta C, Bettella A, Merico M, Garolla A, Ferlin A, Rossato M (2002) Use of recombinant human follicle-stimulating hormone in the treatment of male factor infertility. Fertil Steril 77(2):238–244
47. Knuth UA, Honigl W, Bals-Pratsch M, Schleicher G, Nieschlag E (1987) Treatment of severe oligospermia with human chorionic gonadotropin/human menopausal gonadotropin: a placebo-controlled, double blind trial. J Clin Endocrinol Metab 65(6):1081–1087
48. Selice R, Garolla A, Pengo M, Caretta N, Ferlin A, Foresta C (2011) The response to FSH treatment in oligozoospermic men depends on FSH receptor gene polymorphisms. Int J Androl 34(4):306–312
49. Ashkenazi J, Bar-Hava I, Farhi J, Levy T, Feldberg D, Orvieto R et al (1999) The role of purified follicle stimulating hormone therapy in the male partner before intracytoplasmic sperm injection. Fertil Steril 72(4):670–673
50. Foresta C, Selice R, Moretti A, Pati MA, Carraro M, Engl B et al (2009) Gonadotropin administration after gonadotropin-releasing-hormone agonist: a therapeutic option in severe testiculopathies. Fertil Steril 92(4):1326–1332
51. Zini A (2011) Are sperm chromatin and DNA defects relevant in the clinic? Syst Biol Reprod Med 57(1–2):78–85
52. Smit M, van Casteren NJ, Wildhagen MF, Romijn JC, Dohle GR (2010) Sperm DNA integrity in cancer patients before and after cytotoxic treatment. Hum Reprod 25(8):1877–1883
53. Ribas-Maynou J, Gawecka JE, Benet J, Ward WS (2014) Double-stranded DNA breaks hidden in the neutral Comet assay suggest a role of the sperm nuclear matrix in DNA integrity maintenance. Mol Hum Reprod 20(4):330–340
54. Muratori M, Tamburrino L, Marchiani S, Cambi M, Olivito B, Azzari C et al (2015) Investigation on the origin of sperm DNA Fragmentation: role of apoptosis, immaturity and oxidative stress. Mol Med 21:109–122
55. Zini A, Bielecki R, Phang D, Zenzes MT (2001) Correlations between two markers of sperm DNA integrity, DNA denaturation and DNA fragmentation, in fertile and infertile men. Fertil Steril 75(4):674–677
56. Zini A, Boman JM, Belzile E, Ciampi A (2008) Sperm DNA damage is associated with an increased risk of pregnancy loss after IVF and ICSI: systematic review and meta-analysis. Hum Reprod 23(12):2663–2668
57. Carrell DT, Wilcox AL, Lowy L, Peterson CM, Jones KP, Erickson L et al (2003) Elevated sperm chromosome aneuploidy and apoptosis in patients with unexplained recurrent pregnancy loss. Obstet Gynecol 101(6):1229–1235
58. Carlini T, Paoli D, Pelloni M, Faja F, Dal Lago A, Lombardo F et al (2017) Sperm DNA fragmentation in Italian couples with recurrent pregnancy loss. Reprod Biomed Online 34(1):58–65
59. Robinson L, Gallos ID, Conner SJ, Rajkhowa M, Miller D, Lewis S et al (2012) The effect of sperm DNA fragmentation on miscarriage rates: a systematic review and meta-analysis. Hum Reprod 27(10):2908–2917
60. Muratori M, Forti G, Baldi E (2008) Comparing flow cytometry and fluorescence microscopy for analyzing human sperm DNA fragmentation by TUNEL labeling. Cytom A 73(9):785–787
61. Evenson DP, Wixon R (2006) Clinical aspects of sperm DNA fragmentation detection and male infertility. Theriogenology 65(5):979–991
62. Castillo J, Estanyol JM, Ballesca JL, Oliva R (2015) Human sperm chromatin epigenetic potential: genomics, proteomics, and male infertility. Asian J Androl 17(4):601–609
63. Simon L, Zini A, Dyachenko A, Ciampi A, Carrell DT (2017) A systematic review and meta-analysis to determine the effect of sperm DNA damage on in vitro fertilization and intracytoplasmic sperm injection outcome. Asian J Androl 19(1):80–90
64. Ruvolo G, Roccheri MC, Brucculeri AM, Longobardi S, Cittadini E, Bosco L (2013) Lower sperm DNA fragmentation after r-FSH administration in functional hypogonadotropic hypogonadism. J Assist Reprod Genet 30(4):497–503
65. Simoni M, Santi D, Negri L, Hoffmann I, Muratori M, Baldi E et al (2016) Treatment with human, recombinant FSH improves sperm DNA fragmentation in idiopathic infertile men depending on the FSH receptor polymorphism p. N680S: a pharmacogenetic study. Hum Reprod 31(9):1960–1969
66. Piomboni P, Serafini F, Gambera L, Musacchio C, Collodel G, Morgante G et al (2009) Sperm aneuploidies after human recombinant follicle stimulating hormone therapy in infertile males. Reprod Biomed Online 18(5):622–629
67. Attia AM, Al-Inany HG, Farquhar C, Proctor M (2007) Gonadotrophins for idiopathic male factor subfertility. Cochrane Database Syst Rev 17:CD005071
68. Foresta C, Bettella A, Ferlin A, Garolla A, Rossato M (1998) Evidence for a stimulatory role of follicle-stimulating hormone on the spermatogonial population in adult males. Fertil Steril 69(4):636–642
69. Garolla A, Selice R, Engl B, Bertoldo A, Menegazzo M, Finos L et al (2014) Spermatid count as a predictor of response to FSH therapy. Reprod Biomed Online 29(1):102–112
70. Aittomaki K, Lucena JL, Pakarinen P, Sistonen P, Tapanainen J, Gromoll J et al (1995) Mutation in the follicle-stimulating hormone receptor gene causes hereditary hypergonadotropic ovarian failure. Cell 82(6):959–968
71. Behre HM, Greb RR, Mempel A, Sonntag B, Kiesel L, Kaltwasser P et al (2005) Significance of a common single nucleotide polymorphism in exon 10 of the follicle-stimulating hormone (FSH) receptor gene for the ovarian response to FSH: a pharmacogenetic approach to controlled ovarian hyperstimulation. Pharmacogenetics Genomics 15(7):451–456
72. Greb RR, Grieshaber K, Gromoll J, Sonntag B, Nieschlag E, Kiesel L et al (2005) A common single nucleotide polymorphism in exon 10 of the human follicle stimulating hormone receptor is a major determinant of length and hormonal dynamics of the menstrual cycle. J Clin Endocrinol Metab 90(8):4866–4872
73. Tuttelmann F, Laan M, Grigorova M, Punab M, Sober S, Gromoll J (2012) Combined effects of the variants FSHB-211G > T and FSHR 2039A > G on male reproductive parameters. J Clin Endocrinol Metab 97(10):3639–3647
74. Simoni M, Gromoll J, Nieschlag E (1997) The follicle-stimulating hormone receptor: biochemistry, molecular biology, physiology and pathophysiology. Endocr Rev 18(6):739–773
75. Liu JY, Gromoll J, Cedars MI, La Barbera AR (1998) Identification of allelic variants in the follicle-stimulating hormone receptor genes of females with or without hypergonadotropic amenorrhea. Fertil Steril 70(2):326–331
76. Simoni M, Gromoll J, Hoppner W, Kamischke A, Krafft T, Stahle D et al (1999) Mutational analysis of the follicle-stimulating hormone (FSH) receptor in normal and infertile men: identification and characterization of two discrete FSH receptor isoforms. J Clin Endocrinol Metab 84(2):751–755
77. Grigorova M, Rull K, Laan M (2007) Haplotype structure of FSHB, the beta-subunit gene for fertility-associated follicle-stimulating hormone: possible influence of balancing selection. Ann Hum Genet 71(Pt 1):18–28
78. Grigorova M, Punab M, Ausmees K, Laan M (2008) FSHB promoter polymorphism within evolutionary conserved element is associated with serum FSH level in men. Hum Reprod 23(9):2160–2166
79. Ferlin A, Vinanzi C, Selice R, Garolla A, Frigo AC, Foresta C (2011) Toward a pharmacogenetic approach to male infertility: polymorphism of follicle-stimulating hormone beta-subunit promoter. Fertil Steril 96(6):1344–1349
80. Worrilow KC, Eid S, Woodhouse D, Perloe M, Smith S, Witmyer J et al (2013) Use of hyaluronan in the selection of sperm for intracytoplasmic sperm injection (ICSI): significant improvement in clinical outcomes-multicenter, double-blinded and randomized controlledtrial. Hum Reprod 28(2):306–314
81. Grigorova M, Punab M, Punab AM, Poolamets O, Vihljajev V, Zilaitienė B et al (2014) Reproductive physiology in young men is cumulatively affected by FSH-action modulating genetic variants: FSHR -29G/A and c.2039 A/G, FSHB -211G/T. PLoS ONE 9(4):e94244
82. Iacono F, Barra S, Montano L, Lotti T (1996) Value of high-dose pure FSH in the treatment of idiopathic male infertility. J Urol (Paris) 102(2):81–84
83. Dirnfeld M, Katz G, Calderon I, Abramovici H, Bider D (2000) Pure follicle-stimulating hormone as an adjuvant therapy for selected cases in male infertility during in vitro fertilization is beneficial. Eur J Obstet Gynecol Reprod Biol 93(1):105–108