Journal of Reproduction & Infertility

Journal of Reproduction & Infertility

Serum Testosterone-Estradiol Ratio in Toxoplasma-Seropositive Infertile Men: A Prospective, Single-Center Study

Authors
Ahmed Ragab 1
Doaa Hamdy 2
Shimaa Ibrahim 2
1 Department of Andrology, Sexology and STIs, Faculty of Medicine, Beni-Suef University, Beni-Suef, Egypt
2 Department of Medical Parasitology, Faculty of Medicine, Beni-Suef University, Beni-Suef, Egypt
10.18502/jri.v25i1.15196
Abstract
Background: The purpose of the current study was to compare the testosterone-estradiol (T:E2) ratio in Toxoplasma gondii (T. gondii) seropositive infertile men with seropositive and seronegative normozoospermic controls. Methods: A total of 200 men with normal virilization, including 100 with idiopathic infertility and 100 normozoospermic men, were included in the study. Participants underwent a comprehensive evaluation including a detailed medical history assessment, physical examination, semen analysis, testing for T. gondii IgM/IgG, and estimation of serum T:E2 ratios. Statistical comparisons between groups were performed using t-test and Chi square (x 2 ) with a significance level set at p<0.05. Results: Infertile cases were diagnosed with oligozoospermia (63%), oligoasthenozoospermia (34%), and oligoasthenoteratozoospermia (3%). Regarding anti-Toxoplasma IgG and IgM antibodies, among infertile men, 34 tested positive for IgG and 8 tested positive for IgM. Among the 34 infertile men who tested positive for IgG antibodies, 13 individuals (38.2%) had disturbed T:E2 ratios. Also, among the 12 IgG-positive controls, 5 individuals (41.7%) had disturbed T:E2 ratios (p=0.834). However, only 2 out of the 83 seronegative controls (2.5%) had disturbed T:E2 ratios, which was statistically significant (p<0.001). Furthermore, 6 out of 8 IgM-positive infertile men had altered T:E2 ratios, compared to 3 out of 5 IgM-positive controls (p=0.568) and 2 out of 83 seronegative controls (p<0.001). The T:E2 ratio was significantly lower (8.68±1.95) among IgM-positive infertile men and higher (13.04±3.78) among IgG-positive infertile men when compared to seronegative controls (10.45±0.54) (p<0.001). There were no significant differences in the testosterone-estradiol (T:E2) ratios between infertile men with positive IgM or IgG serology and the control group with the same serology. Conclusion: A significant proportion of infertile men with toxoplasmosis exhibit altered T:E2 ratios. These findings emphasize the importance of conducting anti-T. gondii-IgG testing in individuals with abnormal T:E2 ratios.
Keywords
Asthenozoospermia
Estradiol
Immunoglobulin G
immunoglobulin M
Male infertility
Oligospermia
testosterone
Toxoplasma
  1. Devroey P, Fauser BC, Diedrich K; Evian annual reproduction (EVAR) workshop group 2008. Approaches to improve the diagnosis and management of infertility. Hum Reprod Update. 2009;15(4):391-408.
  2. Peterson BD, Gold L, Feingold T. The experience and influence of infertility: considerations for couple Counselors. Fam J. 2007;15(3):251-7.
  3. Krausz C. Male infertility: pathogenesis and clinical diagnosis. Best Pract Res Clin Endocrinol Metab. 2011;25(2):271-85.
  4. Aquila S, Sisci D, Gentile M, Carpino A, Middea E, Catalano S, et al. Towards a physiological role for cytochrome P450 aromatase in ejaculated human sperm. Hum Reprod. 2003;18(8):1650-9.
  5. Luboshitzky R, Kaplan-Zverling M, Shen-Orr Z, Nave R, Herer P. Seminal plasma androgen/oestrogen balance in infertile men. Int J Androl. 2002;25(6):345-51.
  6. Yamamoto M, Hibi H, Katsuno S, Miyake K. Serum estradiol levels in normal men and men with idiopathic infertility. Int J Urol. 1995;2(1):44-6.
  7. Schlegel PN. Aromatase inhibitors for male infertility. Fertil Steril. 2012;98(6):1359-62.
  8. Castelló-Porcar AM, Martínez-Jabaloyas JM. Testosterone/estradiol ratio, is it useful in the diagnosis of erectile dysfunction and low sexual desire? Aging Male. 2016;19(4):254-8.
  9. Gregoriou O, Bakas P, Grigoriadis C, Creatsa M, Hassiakos D, Creatsas G. Changes in hormonal profile and seminal parameters with use of aromatase inhibitors in management of infertile men with low testosterone to estradiol ratios. Fertil Steril. 2012;98(1):48-51.
  10. Hlaváčová J, Flegr J, Řežábek K, Calda P, Kaňková Š. Association between latent toxoplasmosis and fertility parameters of men. Andrology. 2021;9(3):854-62.
  11. Singh S. Congenital toxoplasmosis: clinical features, outcomes, treatment, and prevention. Trop Parasitol. 2016;6(2):113-22.
  12. Flegr J, Klapilová K, Kaňková S. Toxoplasmosis can be a sexually transmitted infection with serious clinical consequences. Not all routes of infection are created equal. Med Hypotheses. 2014;83(3):286-9.
  13. Kaňková Š, Hlaváčová J, Flegr J. Oral sex: a new, and possibly the most dangerous, route of toxoplasmosis transmission. Med Hypotheses. 2020;141:109725.
  14. Robert-Gangneux F, Dardé ML. Epidemiology of and diagnostic strategies for toxoplasmosis. Clin Microbiol Rev. 2012;25(2):264-96.
  15. Garg M, Stern D, Groß U, Seeberger PH, Seeber F, Varón Silva D. Detection of anti-toxoplasma gondii antibodies in human sera using synthetic glycosylphosphatidylinositol glycans on a bead-based multiplex assay. Anal Chem. 2019;91(17):11215-22.
  16. Dalimi A, Abdoli A. Toxoplasma gondii and male reproduction impairment: A new Aspect of Toxoplasmosis Research. Jundishapur J Microbiol. 2013;6(8):e7184.
  17. Dongmei X, Zhou Y, Diao W. Preliminary investigation on relationship between spermatogenic cells apoptosis and infection of toxoplasma gondii in male infertility. Chinese J Schistomiasis. 2005;17(6):451-53.
  18. Mohammed NS, Al-Muhsin A, Al-khayat FA, Hussien SK. The impact of Toxoplasma gondii on mitochondrial DNA of sub-fertile men sperms. Biomed Pharmacol J. 2017;10(2).
  19. Dardona Z, Amane M, Boussaa S. Toxoplasmosis-related psychological, behavioral, neurological, and hormonal changes: a literature review. Eur J Med Health Sci. 2023;5(5):128-44.
  20. Shirbazou S, Abasian L, Meymand FT. Effects of Toxoplasma gondii infection on plasma testosterone and cortisol level and stress index on patients referred to Sina hospital, Tehran. Jundishapur J Microbiol. 2011;4(3):167-73.
  21. Hodková H, Kolbeková P, Skallová A, Lindová J, Flegr J. Higher perceived dominance in Toxoplasma infected men--a new evidence for role of increased level of testosterone in toxoplasmosis-associated changes in human behavior. Neuro Endocrinol Lett. 2007;28(2):110-4.
  22. Flegr J, Lindová J, Pivoňková V, Havlíček J. Brief communication: latent toxoplasmosis and salivary testosterone concentration-important confounding factors in second to fourth digit ratio studies. Am J Phys Anthropol. 2008;137(4):479-84.
  23. Oktenli C, Doganci L, Ozgurtas T, Araz RE, Tanyuksel M, Musabak U, et al. Transient hypogonadotrophic hypogonadism in males with acute toxoplasmosis: suppressive effect of interleukin-1 on the secretion of GnRH. Hum Reprod. 2004;19(4):859-66.
  24. Zhang X, Liu J, Li M, Fu Y, Zhang T, Han Q, et al. Role of an estradiol regulatory factor-hydroxysteroid dehydrogenase (HSD) in Toxoplasma gondii infection and pathogenicity. J Steroid Biochem Mol Biol. 2017;174:176-82.
  25. World medical association. World medical association declaration of Helsinki: ethical principles for medical research involving human subjects. JAMA. 2013;310(20):2191-4.
  26. World Health Organization (WHO). WHO laboratory manual for the examination and processing of human semen. 5th ed. Geneva: WHO; 2010. 271 p.
  27. Farhan BA. Seroprevelance of toxoplasma gondii (IgM, IgG) among aborted women in some Karbala hospital by using ELISA technique and microscopic examination. Indian J Foren Med Toxicol. 2020;14.1.
  28. van Koeverden ID, de Bakker M, Haitjema S, van der Laan SW, de Vries JPM, Hoefer IE, et al. Testosterone to oestradiol ratio reflects systemic and plaque inflammation and predicts future cardiovascular events in men with severe atherosclerosis. Cardiovasc Res. 2019;115(2):453-62.
  29. Pavlovich CP, King P, Goldstein M, Schlegel PN. Evidence of a treatable endocrinopathy in infertile men. J Urol. 2001;165(3):837-41.
  30. Abdoli A. Toxoplasma, testosterone, and behavior manipulation: The role of parasite strain, host variations, and intensity of infection. Front Biol. 2014;9(2):151-60.
  31. Zghair KH, Al-Qadhi BN, Mahmood SH. The effect of toxoplasmosis on the level of some sex hormones in males blood donors in Baghdad. J Parasit Dis. 2015;39(3):393-400.
  32. Al-Kurdy MJ, A’aiz NN, Jawad TI. Study the Effect of Chronic Toxoplasmosis on Serum Testosterone Level in Men. Indian J Forensic Med Toxicol. 2020;14(4):3132-7.‏
  33. Qi R, Su XP, Gao XL, Liang XL. [Toxoplasma infection in males with sterility in Shenyang, China]. Zhonghua Nan Ke Xue. 2005;11(7):503-4. Chinese.
  34. Zhou YH, Lu YJ, Wang RB, Song LM, Shi F, Gao QF, et al. [Survey of infection of Toxoplasma gondii in infertile couples in Suzhou countryside]. Zhonghua Nan Ke Xue. 2002;8(5):350-2. Chinese.
  35. Muhsin SS, Mamdooh AM, Baseer AN. Seroprevalance study of toxoplasmosis among males in Al-Ruasfa institute of management in Baghdad province-Iraq. J Pharm Biol Sci. 2018;13(2):22-6.
  36. Rostami A, Seyyedtabaei SJ, Aghamolaie S, Behniafar H, Lasjerdi Z, Abdolrasouli A, et al. Seroprevalence and risk factors associated with Toxoplasma gondii infection among rural communities in northern Iran. Rev Inst Med Trop Sao Paulo. 2016;58:70.
  37. Kawashima T, Khin-Sane-Win, Kawabata M, Barzaga N, Matsuda H, Konishi E. Prevalence of antibodies to Toxoplasma gondii among urban and rural residents in the Philippines. Southeast Asian J Trop Med Public Health. 2000;31(4):742-6.
  38. Abdulla HE, Al-bashier NM, Al-kawaz U, Al-Shuwaikh AM, Abood AS, Cross-sectional study of infertile males with toxoplasmosis in Baghdad province. Int J Sci Eng Res. 2015;6(1):254.
  39. Eslamirad Z, Hajihossein R, Ghorbanzadeh B, Alimohammadi M, Mosayebi M, Didehdar M. Effects of toxoplasma gondii infection in level of serum testosterone in males with chronic toxoplasmosis. Iran J Parasitol. 2013;8(4):622-6.
  40. Obaid HM, Ahmed FF, Ismaeol AN. Some hormonal assay in toxoplasma infected university students. Kirkuk Univ J Sci Stud. 2016;11(3):66-80.
  41. Abbasian L. Role of toxoplasma gondii infection in serum level of testosterone. Kowsar Med J. 2011;16(2):123-7.
  42. Kanková S, Kodym P, Flegr J. Direct evidence of toxoplasma induced changes in serum testosterone in mice. Exp Parasitol. 2011;128(3):181-3.
  43. James WH: Potential solutions to problems posed by the offspring sex ratio of people with parasitic and viral infection. Folia Parasitol (Praha). 2010;57(2):114-20.
  44. Alardi MH. The role of toxoplasma gondii in concentration of some sex hormones in infertile individual. J Adv Med Pharm Sci. 2011;5(1):72-82.
  45. Flegr J, Lindová J, Kodym P. Sex-dependent toxoplasmosis-associated differences in testosterone concentration in humans. Parasitology. 2008;135(4):427-31.
  46. Khan AA, Araujo FG, Brighty KE, Gootz TD, Remington JS. Anti-toxoplasma gondii activities and structure-activity relationships of novel fluoroquinolones related to trovafloxacin. Antimicrob Agents Chemother. 1999;43(7):1783-7.
  47. Babu SR, Sadhnani MD, Swarna M, Padmavathi P, Reddy PP. Evaluation of FSH, LH and testosterone levels in different subgroups of infertile males. Indian J Clin Biochem. 2004;19(1):45-9.
  48. Roberts CW, Walker W, Alexander J. Sex-associated hormones and immunity to protozoan parasites. Clin Microbiol Rev. 2001;14(3):476-88.
  49. Harper JM, Huynh MH, Coppens I, Parussini F, Moreno S, Carruthers VB. A cleavable propeptide influences toxoplasma infection by facilitating the trafficking and secretion of the TgMIC2-M2AP invasion complex. Mol Biol Cell. 2006;17(10):4551-63.
  50. Montoya JG, Liesenfeld O. Toxoplasmosis. Lancet. 2004;363(9425):1965-76.
Journal of Reproduction & Infertility
Volume 25, Issue 1
Winter 2024
Pages 28-37