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Journal of Endocrinological Investigation

, Volume 26, Issue 4, pp 372–380 | Cite as

Thyroid disease and male reproductive function

  • G. E. Krassas
  • P. Perros
Review Article

Abstract

Despite the high prevalence of thyroid diseases in the general population, male reproductive function in patients with thyroid disease has been the subject of only a few studies. Hyperthyroidism appears to cause sperm abnormalities (mainly reduction in motility), which reverse after restoration of euthyroidism. Radioiodine therapy for hyperthyroidism or thyroid cancer may cause transient reductions in sperm count and motility, but there appears to be little risk of permanent effects provided that the cumulative dose is less than 14 MBq. The effects of hypothyroidism on male reproduction appear to be more subtle than those of hyperthyroidism and reversible. Severe, prolonged hypothyroidism in childhood may be associated with permanent abnormalities in gonadal function.

Key-words

Hyperthyroidism Hypothyroidism Fertility Male reproduction 

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References

  1. 1.
    Winters S.J., Berga S.L. Gonadal dysfunction in patients with thyroid disorders. Endocrinologist 1997, 7: 167–173.CrossRefGoogle Scholar
  2. 2.
    Shetty A., Wilber J.F. Pituitary-thyroid hormone interactions in states of hyper- and hypothyroidism: Clinical implications in 2000. Endocrinologist 2000, 10: 118–123.CrossRefGoogle Scholar
  3. 3.
    Jannini E.A., Ulisse S., D’Armiento M. Thyroid hormone and male gonadal function. Endocr. Rev. 1995, 16: 443–459.PubMedGoogle Scholar
  4. 4.
    Jannini E.A., Crescenzi A., Rucci N., et al. Ontogenetic pattern of thyroid hormone receptor expression in the human testis. J. Clin. Endocrinol. Metab. 2000, 85: 3453–3457.PubMedCrossRefGoogle Scholar
  5. 5.
    Olivo J., Southren A.L., Gordon G.G., Tochimoto S. Studies of the protein binding of testosterone in plasma in disorders of thyroid function: effect of therapy. J. Clin. Endocrinol. Metab. 1970, 31: 539–545.PubMedCrossRefGoogle Scholar
  6. 6.
    Ruder H., Corvol P., Mahoudeau J.A., Ross G.T., Lipsett M.B. Effects of induced hyperthyroidism on steroid metabolism in man. J. Clin. Endocrinol. Metab. 1971, 33: 382–387.PubMedCrossRefGoogle Scholar
  7. 7.
    Ford H.C., Cooke R.R., Keightley E.A., Feek C.M. Serum levels of free and bound testosterone in hyperthyroidism. Clin. Endocrinol. (Oxf.) 1992, 36: 187–192.CrossRefGoogle Scholar
  8. 8.
    Gordon G.G., Southren A.L., Tochimoto S., Rand J.J., Olivo J. Effect of hyperthyroidism and hypothyroidism on the metabolism of testosterone and androstenedione in man. J. Clin. Endocrinol. Metab. 1969, 29: 164–170.PubMedCrossRefGoogle Scholar
  9. 9.
    Vermeulen A., Verdonck L., Van Der Straeten M., Orie N. Capacity of the testosterone-binding globulin in human plasma and influence of specific binding to testosterone on its metabolic clearance rate. J. Clin. Endocrinol. Metab. 1969; 29: 1470–1480.CrossRefGoogle Scholar
  10. 10.
    Kidd G.S., Glass A.R., Vigersky R.A. The hypothalamic-pituitary-testicular axis in thyrotoxicosis. J. Clin. Endocrinol. Metab. 1979, 48: 798–802.PubMedCrossRefGoogle Scholar
  11. 11.
    Chopra I.J., Tulchinsky D. Status of estrogen-androgen balance in hyperthyroid men with Graves’ disease. J. Clin. Endocrinol. Metab. 1974, 38: 269–277.PubMedCrossRefGoogle Scholar
  12. 12.
    Ridgway E.C., Maloof F., Longcope C. Androgen and oestrogen dynamics in hyperthyroidism. J. Endocrinol. 1982, 95: 105–115.PubMedCrossRefGoogle Scholar
  13. 13.
    Gallagher T.F., Fukushima D.K., Noguchi S., et al. Recent studies in steroid hormone metabolism in man. Recent Prog. Horm. Res. 1966, 22: 283–303.PubMedGoogle Scholar
  14. 14.
    Longcope C. Methods and results of aromatization studies in vivo. Cancer Res. 1982, 42 (8): 3307s-3311s.Google Scholar
  15. 15.
    Nomura K., Suzuki H., Saji M., et al. High serum progesterone in hyperthyroid men with Graves’ disease. J. Clin. Endocrinol. Metab. 1988, 66: 230–232.PubMedCrossRefGoogle Scholar
  16. 16.
    Abalovich M., Levalle O., Hermes R., et al. Hypothalamicpituitary- testicular axis and seminal parameters in hyperthyroid males. Thyroid 1999, 9: 857–863.PubMedCrossRefGoogle Scholar
  17. 17.
    Michnovicz J.J., Galbraith R.A. Effects of exogenous thyroxine on C-2 and C-16 alpha hydroxylations of estradiol in humans. Steroids 1990, 55: 22–26.PubMedCrossRefGoogle Scholar
  18. 18.
    Carlson H.E. Current concepts — gynecomastia. N. Engl. J. Med. 1980, 303: 795–799.PubMedCrossRefGoogle Scholar
  19. 19.
    Rojdmark S., Berg A., Kallner G. Hypothalamic-pituitarytesticular axis in patients with hyperthyroidism. Horm. Res. 1988, 29: 185–190.PubMedCrossRefGoogle Scholar
  20. 20.
    Wortsman J., Rosner W., Dufau M.L. Abnormal testicular function in men with primary hypothyroidism. Am. J. Med. 1987, 82: 207–212.PubMedCrossRefGoogle Scholar
  21. 21.
    Jaya Kumar B., Khurana M.L., Ammini A.C., Karmarkar M.G., Ahuja M.M. Reproductive endocrine functions in men with primary hypothyroidism: effect of thyroxine replacement. Horm. Res. 1990, 34: 215–218.PubMedCrossRefGoogle Scholar
  22. 22.
    Velazquez E.M., Bellabarba Arata G. Effects of thyroid status on pituitary gonadotropin and testicular reserve in men. Arch. Androl. 1997, 38: 85–92.PubMedCrossRefGoogle Scholar
  23. 23.
    Clyde H.R., Walsh P.C., English R.W. Elevated plasma testosterone and gonadotropin levels in infertile males with hyperthyroidism. Fertil. Steril. 1976, 27: 662–666.PubMedGoogle Scholar
  24. 24.
    Hudson R.W., Edwards A.L. Testicular function in hyperthyroidism. J. Androl. 1992, 13: 117–124.PubMedGoogle Scholar
  25. 25.
    Krassas G.E., Pontikides N., Deligianni V., Miras K. A prospective controlled study of the impact of hyperthyroidism on reproductive function in males. J. Clin. Endocrinol. Metab. 2002, 87: 3667–3671.PubMedCrossRefGoogle Scholar
  26. 26.
    Dunn J.T. Choice of therapy in young adults with hyperthyroidism of Graves’ disease. A brief, case-directed poll of fiftyfour thyroidologists. Ann. Intern. Med. 1984, 100: 891–893.PubMedCrossRefGoogle Scholar
  27. 27.
    Kaplan M.M., Meier D.A., Dworkin H.J. Treatment of hyperthyroidism with radioactive iodine. Endocrinol. Metab. Clin. North. Am. 1998, 27: 205–223.PubMedCrossRefGoogle Scholar
  28. 28.
    Hyer S., Vini L., O’Connell M., Pratt B., Harmer C. Testicular dose and fertility in men following 131I therapy for thyroid cancer. Clin. Endocrinol. (Oxf.) 2002, 56: 755–758.CrossRefGoogle Scholar
  29. 29.
    Mussey R.D. The thyroid gland and pregnancy. Am. J. Obstet. Gynecol. 1938, 36: 529–538.Google Scholar
  30. 30.
    Krassas G.E. Thyroid disease and female reproduction. Fertil. Steril. 2000, 74: 1063–1070.PubMedCrossRefGoogle Scholar
  31. 31.
    Handelsman D.J., Turtle J.R. Testicular damage after radioactive iodine (I-131) therapy for thyroid cancer. Clin. Endocrinol. (Oxf.) 1983, 18: 465–472.CrossRefGoogle Scholar
  32. 32.
    Starr P., Jaffe H.L., Oettinger L. Jr. Later results of 131-I treatment of hyperthyroidism in 73 children and adolescents: 1967 follow-up. J. Nucl. Med. 1969, 10: 586–590.PubMedGoogle Scholar
  33. 33.
    Hayek A., Chapman E.M., Crawford J.D. Long-term results of treatment of thyrotoxicosis in children and adolescents with radioactive iodine. N. Engl. J. Med. 1970, 283: 949–953.PubMedCrossRefGoogle Scholar
  34. 34.
    Safa A.M., Schumacher O.P., Rodriguez-Antunez A. Longterm follow-up results in children and adolescents treated with radioactive iodine (131-I) for hyperthyroidism. N. Engl. J. Med. 1975, 292: 167–171.PubMedCrossRefGoogle Scholar
  35. 35.
    Halnan K.E. Risks from radioiodine treatment of thyrotoxicosis. Br. Med. J. 1983, 287: 1821–1822.CrossRefGoogle Scholar
  36. 36.
    Trunnell J.B., Duffy D.G., Godwin J.T., Peacock W., Kirschner L., Hill R. The distribution of radioactive iodine in human tissues: necropsy study in nine patients. J. Clin. Endocrinol. Metab. 1950, 10: 1007–1021.PubMedCrossRefGoogle Scholar
  37. 37.
    Berman M., Braverman L.B., Burke J., et al. Iodine-123, iodine-124, iodine-125, iodine-126, iodine-130, iodine-131 and iodine-132 as sodium iodide MIRD pamphlet no 5. New York: The Society of Nuclear Medicine. 1988.Google Scholar
  38. 38.
    Erickson B.H. Effect of 60Co gamma radiation on the stem and differentiating spermatogonia of the postpuberal rat. Radiat. Res. 1976, 68: 433–448.PubMedCrossRefGoogle Scholar
  39. 39.
    Mian T.A., Suzuki N., Glenn H.J., Haynie T.P., Meistrich M.L. Radiation damage to mouse testis cells from [99mTc] pertechnetate. J. Nucl. Med. 1977, 18: 1116–1122.PubMedGoogle Scholar
  40. 40.
    Lushbaugh C.C., Casarett G.W. The effects of gonadal irradiation in clinical radiation therapy: a review. Cancer 1976, 37 (2): 1111–1125.PubMedCrossRefGoogle Scholar
  41. 41.
    Gorman C.A. Radioiodine and pregnancy (Review). Thyroid 1999, 9: 721–726.PubMedCrossRefGoogle Scholar
  42. 42.
    Handelsman D.J., Conway A.J., Donnelly P.E., Turtle J.R. Azoospermia after iodine-131 treatment for thyroid carcinoma. Br. Med. J. 1980, 281: 1527.PubMedCentralPubMedCrossRefGoogle Scholar
  43. 43.
    Edmonds C.J., Smith T. The long-term hazards of the treatment of thyroid cancer with radioiodine. Br. J. Radiol. 1986, 59: 45–51.PubMedCrossRefGoogle Scholar
  44. 44.
    Pacini F., Gasperi M., Fugazzola L., et al. Testicular function in patients with differentiated thyroid carcinoma treated with radioiodine. J. Nucl. Med. 1994, 35: 1418–1422.PubMedGoogle Scholar
  45. 45.
    Wichers M., Benz E., Palmedo H., Biersack H.J., Grunwald F., Klingmuller D. Testicular function after radioiodine therapy for thyroid carcinoma. Eur. J. Nucl. Med. 2000, 27: 503–507.PubMedCrossRefGoogle Scholar
  46. 46.
    Wartofsky L. Thyroid cancer. Humana Press, Totowa, New Jersey, 2000.CrossRefGoogle Scholar
  47. 47.
    Tunbridge W.M.G., Evered D., Hall R., et al. The spectrum of thyroid disease in a community: the Whickham survey. Clin. Endocrinol. (Oxf.) 1977, 7: 481–493.CrossRefGoogle Scholar
  48. 48.
    Canaris G.J., Manowitz N.R., Mayor G., Ridgway E.C. The Colorado thyroid disease prevalence study. Arch. Intern. Med. 2000, 160: 526–534.PubMedCrossRefGoogle Scholar
  49. 49.
    Delange F. The disorders induced by iodine deficiency. Thyroid 1994, 41: 107–128.CrossRefGoogle Scholar
  50. 50.
    Kolettis P.N., Sabanegh E.S. Significant medical pathology discovered during a male infertility evaluation. J. Urol. 2001, 166: 178–180.PubMedCrossRefGoogle Scholar
  51. 51.
    Trummer H., Ramschak-Schwarzer S., Haas J., Habermann H., Pummer K., Leb G. Thyroid hormones and thyroid antibodies in infertile males. Fertil. Steril. 2001, 76: 254–257.PubMedCrossRefGoogle Scholar
  52. 52.
    Vulsma T., Gons M.H., de Vijlder J.J.M. Maternal-fetal transfer of thyroxine in congenital hypothyroidism due to a total organification defect or thyroid agenesis. N. Engl. J. Med. 1989, 321: 13–16.PubMedCrossRefGoogle Scholar
  53. 53.
    Longcope C. The male and female reproductive systems in hypothyroidism. In: Braverman L.E., Utiger R.D. (Eds.) Werner & Ingbar’s The thyroid: A fundamental and clinical text, 8th edition. Lippincott Williams & Wilkins, Philadelphia, 2000, P. 824.Google Scholar
  54. 54.
    Salerno M., Micillo M., Di Maio S., et al. Longitudinal growth, sexual maturation and final height in patients with congenital hypothyroidism detected by neonatal screening. Eur. J. Endocrinol. 2001, 145: 377–383.PubMedCrossRefGoogle Scholar
  55. 55.
    Dickerman Z., De Vries L. Prepubertal and pubertal growth, timing and duration of puberty and attained adult height in patients with congenital hypothyroidism (CH) detected by the neonatal screening programme for CH — a longitudinal study. Clin. Endocrinol. (Oxf.) 1997, 47: 649–654.CrossRefGoogle Scholar
  56. 56.
    Hanna C.E., LaFranchi S.H. Adolescent thyroid disorders. Adolesc. Med. 2002, 13: 13–36.PubMedGoogle Scholar
  57. 57.
    Kendle F. Case of precocious puberty in a female cretin. Br. Med. J. 1905, 1: 246–248.PubMedCentralPubMedCrossRefGoogle Scholar
  58. 58.
    Panidis D.K., Rousso D.H. Macro-orchidism in juvenile hypothyroidism. Arch. Androl. 1999, 42: 85–87.PubMedCrossRefGoogle Scholar
  59. 59.
    Grossman M., Weintraub B.D., Szkudlinski M.W. Novel insights into the molecular mechanisms of human thyrotropin action: structural, physiological, and therapeutic implications for the glycoprotein hormone family. Endocr. Rev. 1997, 18: 476–501.CrossRefGoogle Scholar
  60. 60.
    Corrales Hernandez J.J., Miralles Garcia J.M., Garcia Diez L.C. Primary hypothyroidism and human spermatogenesis. Arch. Androl. 1990, 25: 21–27.PubMedCrossRefGoogle Scholar
  61. 61.
    Cavaliere H., Abelin N., Medeiros-Neto G. Serum levels of total testosterone and sex hormone binding globulin in hypothyroid patients and normal subjects treated with incremental doses of L-T4 or L-T3. J. Androl. 1988, 9: 215–219.PubMedGoogle Scholar
  62. 62.
    Tagawa N., Takano T., Fukata S., et al. Serum concentration of androstenediol and androstenediol sulfate in patients with hyperthyroidism and hypothyroidism. Endocr. J. 2001, 48: 345–354.PubMedCrossRefGoogle Scholar
  63. 63.
    Donnelly P., White C. Testicular dysfunction in men with primary hypothyroidism; reversal of hypogonadotrophic hypogonadism with replacement thyroxine. Clin. Endocrinol. (Oxf.) 2000, 52: 197–201.CrossRefGoogle Scholar
  64. 64.
    Horvath E., Kovacs K., Scheithauer B.W. Pituitary hyperplasia. Pituitary 1999, 1: 169–179.PubMedCrossRefGoogle Scholar
  65. 65.
    Kocova M., Netkov S., Sukarova-Angelovska E. Pituitary pseudotumor with unusual presentation reversed shortly after the introduction of thyroxine replacement therapy. J. Pediatr. Endocrinol. Metab. 2001, 14: 1665–1669.PubMedCrossRefGoogle Scholar
  66. 66.
    Honbo K.S., Van Herle A.J., Kellett K.A. Serum prolactin levels in untreated primary hypothyroidism. Am. J. Med. 1978, 64: 782–787.PubMedCrossRefGoogle Scholar
  67. 67.
    Notsu K., Ito Y., Furuya H., Ohguni S., Kato Y. Incidence of hyperprolactinemia in patients with Hashimoto’s thyroiditis. Endocr. J. 1997, 44: 89–94.PubMedCrossRefGoogle Scholar
  68. 68.
    Griboff S.I. Semen analysis in myxedema. Fertil. Steril. 1962, 13: 436–443.PubMedGoogle Scholar
  69. 69.
    De la Balze E.A., Arrilaga F, Mancini R.E., Janches M., Davidson O.W., Gurtman A.I. Male hypogonadism in hypothyroidism: a study of six cases. J. Clin. Endocrinol. Metab. 1962, 22: 212–222.CrossRefGoogle Scholar

Copyright information

© Italian Society of Endocrinology (SIE) 2003

Authors and Affiliations

  1. 1.Department of Endocrinology and Metabolism“Panagia” General HospitalThessalonikiGreece
  2. 2.Endocrine UnitFreeman HospitalNewcastle upon TyneUK

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