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The Journal of Clinical Endocrinology & Metabolism Vol. 87, No. 8 3667-3671
Copyright © 2002 by The Endocrine Society

Original Article

A Prospective Controlled Study of the Impact of Hyperthyroidism on Reproductive Function in Males

G. E. Krassas, N. Pontikides, V. Deligianni and K. Miras

Department of Endocrinology and Metabolism, Panagia General Hospital, Thessaloniki 55132; and Department of Biochemistry, Medical School, University of Athens (V.D., K.M.), Athens 11527, Greece

Address all correspondence and requests for reprints to: Prof. G. E. Krassas, M.D., Department of Endocrinology and Metabolism, Panagia Hospital, Tsimiski 92, Thessaloniki 546 22, Greece. E-mail: . krassas{at}the.forthnet.gr

Abstract

The aim of this prospective controlled study was to ascertain the effect of hyperthyroidism on sperm quality and composition. We studied 23 thyrotoxic male patients, aged 43.8 ± 2.4 yr (mean ± SEM), and 15 healthy male controls of approximately the same age (42.2 ± 2.2 yr). Two semen analyses at intervals of 2–3 wk were obtained before and about 5 months after euthyroidism was achieved either by methimazole alone (14 patients) or 131I plus methimazole (9 patients). Total fructose, zinc (Zn), and magnesium (Mg) were also measured in seminal plasma in 16 patients, because 7 had semen volume less than 2 ml. In the control group semen analysis was performed only once. Mean (±SEM) semen volume was within normal range both in patients (3.3 ± 0.2 ml) and controls (3.5 ± 0.4 ml; P = NS). Mean sperm density was lower in patients, although the difference compared with controls did not reach statistical significance (35.7 ± 5.3 vs. 51.5 ± 6.1 x 106/ml; P = 0.062). The same was found with sperm morphology (68 ± 7% vs. 78 ± 8%; P = NS). Finally, mean motility was lower in thyrotoxic males than in controls (28 ± 8% vs. 57 ± 7%; P < 0.01). After treatment, sperm density and motility improved [35.7 ± 5.3 vs. 43.3 ± 6.5 x 106/ml (P = NS) and 28 ± 8% vs. 45 ± 7% (P < 0.05), respectively], but sperm morphology did not change (68 ± 7% vs. 70 ± 6%; P = NS). Mean values for fructose, Zn, and Mg did not differ between controls and patients either before or after achievement of euthyroidism [9.2 ± 0.7, 3.0 ± 0.5, and 4.2 ± 0.7 nmol/liter vs. 8.6 ± 0.9, 3.0 ± 0.5, and 4.7 ± 0.8 nmol/liter (patients before) and 9.1 ± 0.7, 3.1 ± 0.6, and 4.5 ± 0.9 nmol/liter (patients after treatment) for fructose, Zn, and Mg, respectively]. Moreover, according to the treatment given, no statistically significant differences were found before or after treatment. Finally, seminal plasma fructose, Zn, and Mg levels did not correlate with sperm parameters or with pretreatment thyroid hormone levels. In conclusion, the results of our study indicate that male patients with hyperthyroidism have abnormalities in seminal parameters, mainly sperm motility. These abnormalities improve or normalize when the patients become euthyroid. Restoration of sperm parameters was independent of the treatment provided for the hyperthyroid syndrome. Moreover, seminal plasma elements, such as fructose, Zn, and Mg, did not correlate with sperm density, motility, or morphology.

ALTHOUGH THE EFFECTS of hyperthyroidism (1, 2, 3) and hypothyroidism (4, 5) on female reproduction are well established, limited data exist concerning the impact of thyroid disorders on sperm quality in adult males. There are three possible reasons for this: 1) in thyrotoxic males attention usually is focused on other manifestations of the disease, and fertility status is frequently not evaluated; 2) thyroid diseases are more common in females than in males; and 3) the demonstration in experimental animals that adult male gonad is metabolically unresponsive to thyroid hormone (6), which has led to the widespread view that the testis is unaffected by iodothyronines. Hyperthyroidism has been found to cause oligospermia, asthenospermia, abnormal sperm morphology, or occasionally infertility in males. However, only few studies with a limited number of patients have been reported to date. It has been suggested that magnesium (Mg) may play a role in spermatogenesis, in particular sperm motility. Furthermore, Mg is regarded as a marker of the secretions of the seminal vesicles and acts as an intracellular calcium antagonist (7). Moreover, consensus exists that the zinc (Zn) concentration in seminal plasma is of importance for spermatogenesis, although the results of several studies are still contradictory (8, 9, 10). Data on fructose, Zn, and Mg concentrations in the seminal fluid of hyperthyroid patients are not available.

The present controlled, prospective study was undertaken to investigate the effects of hyperthyroidism on sperm quality and composition in thyrotoxic male patients of reproductive age before and during treatment for the disease.

Subjects and Methods

Twenty-three thyrotoxic male patients of reproductive age (range, 19–56 yr; mean age, 43.8 ± 2.4 yr) were investigated. Twenty were married, and all but 1 had fathered children. Three were not married and had no children. None of the patients had any serious illnesses in the past year or was taking any medication. Moreover, no patient had any known fertility problem, and semen analysis was performed in all patients for the first time. All patients were clinically thyrotoxic, and the diagnosis was confirmed by measuring serum TSH, free T4, and total T3 levels, the results of which were all consistent with hyperthyroidism (Table 1Go). Twenty patients had Graves’ disease, and 3 had toxic multinodular goiter. Testicular volume was assessed by Prader orchidometer in all patients. The patients were questioned carefully on the frequency of sexual intercourse, libido, and quality of erections. Written informed consent was obtained from all patients for their participation. The study was approved by the institutional ethics committee. Immediately after the diagnosis of hyperthyroidism, semen analysis was performed on all patients. Two semen samples at intervals of 2–3 wk were obtained from each patient after 3–5 d of abstinence from sexual activity. Results are presented as the mean values of the two samples. After evaluation of liquefaction and measurement of the pH, viscosity and volume, samples were examined for total sperm count, total number of motile spermatozoa, morphology, and percentage of dead sperm. Results were considered normal when the semen volume was greater than 2 ml, sperm density was greater than 20 x 106/ml, there was more than 50% forward progressive motility, and there were less than 40% abnormal forms including dead sperm (11). Total fructose, Zn, and Mg concentrations were measured in seminal plasma in 16 of 23 patients. Fructose was measured by Richterich method (12), and Zn and Mg were measured by atomic absorption spectroscopy (13, 14). Immediately after sperm evaluation, 14 patients were given methimazole, and 9 were given radioactive iodine (RAI). Patients who received RAI commenced antithyroid drugs after RAI, and they became euthyroid in approximately 3–4 wk after the administration of radioactive treatment. Six to 8 wk after the initiation of drug treatment, the patients were usually euthyroid and remained so with appropriate titration of the dose of antithyroid drugs, which was confirmed by a blood test. Six to 7 months after the first investigation a second sperm count was performed under the same conditions, and the same parameters were measured as before. Fifteen healthy volunteer males, aged 22–55 yr (mean age, 42.2 ± 2.2 yr), most of whom were hospital workers and had previously fathered children, were used as controls. Semen analysis was performed once, and the results were compared with those of the patients.


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  		Table 1. Mean (±SEM) age, testicular volume, thyroid hormones (free T4, total T3), and TSH levels in thyrotoxic males before and after treatment and in controls

 
Statistical analysis

Results are expressed as the mean ± SEM. Paired and unpaired two-tailed t tests were used to assess differences in the mean values among the various groups, and Spearman’s rank correlation coefficients were used to assess the strength of association between Zn and Mg concentrations and sperm density, motility, and morphology as well as thyroid hormone levels. Differences were considered significant at P < 0.05.

Results

Clinical aspects

The total testicular volume of the patients was 32.4 ± 2.8 ml (range, 18–46 ml). Three patients had a total testicular volume below the low limit of the quoted normal range (20 ml). Thirteen patients reported sexual disturbances, and in 9 of the 13 patients it was associated with decreased libido whose onset coincided with that of the hyperthyroid syndrome. Specifically, 6 of 13 patients had erectile dysfunction, and the rest had sexual intercourse 1 or 2 times every month instead of 1 or 2 times every week, which they reported was the norm before the onset of thyrotoxicosis. Their sexual function returned to normal after treatment of hyperthyroidism.

Sperm parameters

The evaluation of sperm parameters and the quantification of altered parameters in thyrotoxic males before and after 6 months of treatment are shown in Table 2Go. Mean semen volume was within the normal range in all groups studied and did not show any difference compared with controls (3.3 ± 0.2 and 3.4 ± 0.3 vs. 3.5 ± 0.4 ml; P = NS; patients pre- and posttreatment values vs. controls; Table 2Go). However, 7 of 23 thyrotoxic males and 3 controls had semen volumes less than 2 ml (P = NS). After treatment of hyperthyroidism only 3 patients had sperm volumes less than 2 ml. This difference was statistically not significant. The low semen volume precluded measurements of trace elements on those patients.


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  		Table 2. Mean (±SEM) values of sperm volume, density, motility and morphology, and seminal plasma levels of fructose, Zn, and Mg in thyrotoxic males before and after treatment (total group, and patients treated with MMZ or RAI) and controls

 
Sperm density was approximately 30% lower in patients compared with controls (35.7 ± 5.3 vs. 51.5 ± 6.1 x 106/ml), but this difference failed to reach statistical significance (P = 0.062). After treatment of hyperthyroidism, sperm density improved (from 35.7 ± 5.3 to 43.3 ± 6.5 x 106/ml), but again the difference was not statistically significant (Table 2Go and Fig. 1Go). When thyrotoxic males were divided into two subgroups according to the treatment given, no difference was found before or after treatment, although the RAI subgroup had a higher mean sperm density compared with those treated with antithyroid drugs (Table 2Go). It is interesting that 4 of 23 patients had sperm density of 1.5 x 106/ml or less before treatment (severe oligospermics or azoospermics). In only 1 of these patients did sperm density increase after treatment, and it reached a level of 10 x 106/ml. Two of these patients had fathered children in the past. In the control group only 1 individual had sperm density less than 5 x 106/ml, and he had fathered 2 children in the past. After exclusion of the 4 patients with low sperm density from the initial patient group, the mean sperm density for the remaining 19 patients was 15% lower than that in the controls (43.2 ± 4.9 vs. 51.5 ± 6.1 x 106/ml; P = 0.078). After treatment, sperm density rose to reach values close to those in the control group (50.8 ± 9.6 vs. 51.5 ± 6.1 x 106/ml; P = NS; Table 2Go). Forward motility was lower in thyrotoxic males compared with normal individuals (28 ± 8% vs. 57 ± 7%; P < 0.01). The same was true for the 2 subgroups of patients, i.e. treated with antithyroid drugs or RAI (29 ± 7% and 27 ± 8% vs. 57 ± 7%, respectively; P < 0.01 for both). After treatment, motility increased from 28 ± 8% to 45 ± 7%. This increment was statistically significant (P < 0.05). The same was true for the subgroup of 19 patients after exclusion of the 4 severe oligo- or azoospermics (35 ± 6% vs. 57.7%; P < 0.05). No significant differences were found when the posttreatment values were compared with controls (Table 2Go and Fig. 1Go). Finally, regarding morphology it was found that although thyrotoxic patients had lower values than normal individuals (68 ± 7% vs. 78 ± 8%), this difference was not significant. No significant changes in the mean values were noted after treatment for any of the subgroups studied (Table 2Go and Fig. 1Go). None of these parameters correlated with the pretreatment free T4 or total T3 levels.



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  		Figure 1. Mean (±SEM) sperm density, motility, and normal morphology values in thyrotoxic patients before (•) and after () and in controls ({square}).

 
Seminal plasma trace elements

Fructose, Zn, and Mg concentrations as well as the mean values in normal males and thyrotoxic patients are shown in Table 2Go and Fig. 2Go. Mean values for thyrotoxic males did not differ compared with controls. The same was true for the three subgroups of patients. After treatment, similar results were obtained (Table 2Go). Two thyrotoxic patients had low fructose levels before treatment, which returned to normal after treatment. Moreover, five patients had low or very low Zn levels, and another five patients had low or very low Mg levels. In three of five patients with low Zn, Zn levels were restored after 6 months of therapy, whereas in none of the five patients with low Mg levels were Mg levels restored after treatment. Finally, fructose, Zn, and Mg levels did not correlate with sperm density, motility, and morphology before or after treatment or with the pretreatment free T4 or total T3 levels.



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  		Figure 2. Seminal plasma values and means of fructose, Zn, and Mg in thyrotoxic patients before (•) and after ({circ}) treatment and in controls ({triangleup}).

 
Discussion

In this controlled prospective study we found that more than 50% of thyrotoxic males reported sexual dysfunction associated with decreased libido, which improved after 6 months of treatment of hyperthyroidism.

Regarding the semen parameters, some very interesting results emerged. First, although mean values of semen volume were within normal, 7 (30%) of 23 patients had lower than normal volumes, which were restored after treatment. Second, although no statistically significant differences were found in sperm densities, mean sperm densities were approximately 30% lower in patients than controls. Sperm motility however, was significantly lower than that of normal males. Finally, no difference was found concerning sperm morphology, although mean values were lower than those of controls. After treatment, sperm density and motility improved. This study has shown for the first time that mean values of fructose, Zn, and Mg concentrations in seminal plasma were within normal limits and did not correlate with sperm density, motility, or morphology in these patients or with pretreatment free T4 or total T3 levels.

Few studies have been published reporting on the effect of hyperthyroidism on semen quality. Clyde et al. (15) investigated three young males and found that two patients had marked oligospermia with decreased motility, and the third patient had a borderline low sperm count associated with decreased motility. These abnormalities were reversed after medical therapy for hyperthyroidism. Kidd et al. (16) investigated five patients and found that four of five subjects had total sperm counts of less than 40 x 106/ml, whereas only one had sperm density less than 24 x 106/ml. Motility was normal in all men. No data are available after treatment. In 1982, O’Brien et al. (17) reported the case of a man with oligospermia who suffered from thyrotoxicosis. Treatment of the latter was associated with a progressive increase in sperm count. In 1992 Hudson and Edwards (18) investigated testicular function in 16 thyrotoxic males. They found, as we did, that sperm densities were lower than but not significantly different from the mean sperm densities of the control individuals. However, the percent forward progressive sperm motility of hyperthyroid men was significantly lower than that of the control males, which also is in accord with our results. Moreover, they found, as we did, that the percentage of normal sperm forms in thyrotoxic males was not different from that in controls. They reinvestigated nine of those patients 3–6 months after becoming euthyroid. Their results are similar to what we have found in this study.

Finally, in one recent study Abalovich et al. (19) investigated the effect of hyperthyroidism on spermatogenesis in 21 patients. They found that 9 patients (43%) had a decrease in the total sperm count, whereas 18 (85.7%) had a grade a-lineal motility, and 13 (61.9%) had progressive motility problems. No patient had all seminal parameters in the normal range. They restudied 6 of these patients after they had been euthyroid for 7–19 months. In all of these patients, spermatogenesis improved or normalized. There are, however, 2 limitations in this study: 1) the low number of patients retested, and 2) the fact that semen analysis was performed only once.

Various mechanisms may explain these alterations. The first of these is a change in sex steroid and gonadotropins levels. SHBG is increased in male hyperthyroidism (20, 21) leading to a rise in circulating level of total testosterone (22) and to a decrease in the metabolic clearance rate of testosterone (21). However, the plasma level of free testosterone is not significantly different from normal (21, 22), whereas bioavailable testosterone has been reported recently to be low (19). Serum free estradiol levels are increased out of proportion to the rise in the SHBG (23), and increased peripheral conversion of androgen to estrogen has been reported (24). Serum progesterone levels are also elevated in these patients (22). Basal levels of gonadotropins are usually normal, with LH and FSH responses to exogenous GnRH significantly greater than those of controls (25). Second, we cannot rule out the direct action of thyroid hormones, the effect of thyroid-stimulating Igs on the testis, or another autoimmune mechanism associated with Graves’ disease. However, direct effects of thyroid hormone on the human adult testis have never been demonstrated (26). This is further substantiated by studies using molecular biology techniques (27). The trace elements Zn and Mg found in seminal plasma originate primarily from the prostate gland and may reflect prostatic secretory function (14, 28). Furthermore, such analyses are of great help in the assessment of the androgen activity and the functional status of the genital glands. Infections of the prostate gland markedly decrease the concentration of Zn and Mg in semen (29). Eliasson and Lindholmer (14) found no correlation between those two elements and sperm density, motility, viability, or morphological findings, which leads to the suggestion that they are not directly involved in the fertility status of men (14, 30). However, recent studies have suggested that Mg may play a role in spermatogenesis, particularly in sperm motility (7). The same is true for Zn, although the results of several studies are still contradictory (8, 9, 10). This study is the first to show that those two elements are not directly involved in the alterations of spermatogenesis, which are caused by thyrotoxicosis. As far as seminal fructose is concerned, its importance within human seminal plasma is unclear. No correlation between seminal fructose concentration and seminal activity and spermiogenesis was reported by Moon and Bunge (31) or Matschalut and Schirren (32). However, Biswas et al. (33) and Schirren et al. (34) reported decreased fructose concentrations with increasing sperm density and motility.

In conclusion, the results of the current study confirm that men with hyperthyroidism have abnormalities in seminal parameters, mainly sperm motility. These abnormalities improve or normalize when the patients become euthyroid. Restoration of semen parameters was independent of the treatment provided, as it was observed both in subjects who had been given antithyroid drugs and in those who received 131I. Moreover, trace elements in seminal plasma, such as fructose, Zn, and Mg, were within normal levels and did not correlate with sperm density, motility, or morphology in these men. No correlation was found between sperm parameters and pretreatment free T4 and total T3 values.

Acknowledgments

We are grateful to Dr. P. Perros, consultant physician and endocrinologist at Freeman Hospital (Newcastle, UK), for his valuable criticism and suggestions, and also to Ms. Anna Gialantzi for her excellent secretarial assistance.

Footnotes

Abbreviations: Mg, Magnesium; RAI, radioactive iodine; Zn, zinc.

Received February 19, 2002.

Accepted April 28, 2002.

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