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Physicians' attitudes towards androgen replacement therapy for male and female sexual dysfunction

Abstract

Androgen deficiency syndrome is a commonly diagnosed condition. The aim of this study was to investigate common clinical practices of specialists in the field of sexual medicine regarding androgen replacement treatment for men and women. Attendees of the 16th Annual Congress of the European Society of Sexual Medicine held in January 2014 in Istanbul, Turkey, were asked to participate in a survey during the congress days. A 24-item self-report, closed-question questionnaire was distributed. Three sections were accessed: sociodemographic data, professional background and personal practice patterns regarding androgen substitution in men and women. A total of 133 physicians (mean age 47 years; range 25–79) completed the survey. Responses were inconsistent regarding the lab tests used for primary evaluation of male androgen deficiency. The majority of participants (62%) recommended testosterone replacement therapy for symptomatic men with testosterone levels <8 nmol l−1 (231 ng dl−1). Similarly, most physicians (88%) recognized a correlation between libido and testosterone levels in women. Only 42% and 53% reported they would prescribe testosterone to women with low libido, premenopausal and postmenopausal, respectively. This survey showed discrepancies among physicians regarding testosterone replacement therapy for men and women.

Introduction

Androgen deficiency syndrome in men is a commonly diagnosed condition. Clinical symptoms related to testosterone (T)-deficiency may include fatigue, decreased libido, erectile dysfunction, decreased muscle mass, osteoporosis and depression.1, 2, 3 Of clinical importance is the close link between metabolic syndrome in men and low T-plasma levels.4, 5

There is no consensus on the prevalence of androgen deficiency syndrome in men, and, in particular, regarding the recommended T-cutoff plasma levels below which men with related clinical symptoms should undergo T-replacement therapy. Several large epidemiological studies reported prevalence rates of T-deficiency (T<300 or 350 ng ml−1; ~10.4 or 12.0 nmol l−1) of up to 40% in men >40 years.4, 5, 6

In males aged 30–79 years, the prevalence of symptomatic androgen deficiency, defined as low total testosterone (<10.4 nmol l−1), in the presence of low libido, erectile dysfunction, osteoporosis or fracture, or two or more of the following symptoms: sleep disturbance, depressed mood, lethargy and diminished physical performance, was assessed as ~6%.7 Yet, owing to great inter- and intraindividual variations in sex hormone-binding globulin, and consequently in free testosterone levels, defining valid T-cutoff levels for T-deficiency is difficult, if not impossible. For example, symptoms of androgen deficiency often present in males with testosterone levels above 12.1 nmol l−1, who had T-levels >27.7 nmol l−1 at a younger age. About half of all men aged >80 years, and ~1/5th of men aged >60 years, have serum testosterone concentrations at least 2 s.d. below the mean concentration for younger men.8 Therefore, the relative reduction ratio of testosterone over time, and not only the absolute level, may serve as an important surrogate parameter, for or against treatment decisions for patients with clinical symptoms characteristic of T-deficiency. Once a physician and patient reach a decision to commence T-replacement therapy, a choice among the available T-preparation and T-application modes, such as oral, transdermal or parenteral, must be made.

In contrast to males, the concept of androgen insufficiency disorder in women was first described only in 2001.9 Symptoms of female androgen insufficiency syndrome may include a diminished sense of well-being, dysphoric mood, persistent and unexplained fatigue, irritability, insomnia and sexual disorders such as low levels of libido and desire, reduced number and intensity of orgasms and frequency of sexual activities.

In women as in men, the prevalence of sexual disorder increases with age. A cross-sectional study of a nationally representative US sample reported that ~27% of women of reproductive age and ~54% of postmenopausal women complained of low libido.10 Changes in estrogen levels during menopause often result in physiological changes of the external and internal genitals and can impair female sexual desire.11 Therefore, increased prevalence of hypoactive sexual desire with age is not necessarily due to decreased endogenous androgen levels. There are currently no well-defined criteria for the diagnosis of androgen insufficiency syndrome in women, and normative data on the serum levels of total and free testosterone during a woman's life cycle are obviously lacking in the literature. The absence of objective tests for measuring endogenous androgen levels, combined with the variety of factors influencing sexual desire and reasons contributing to low sexual desire, make the determination of candidates for T-treatment even more difficult. Moreover, evidence-based recommendations for doses and monitoring regimens have not been established. None of the currently available testosterone formulations for T-replacement therapy in men have been approved by the Food and Drug Administration for treating sexual dysfunction in women. In 2006, one testosterone formulation was officially approved in Europe for treating sexual dysfunction in women, yet was withdrawn from the market in 2012 by the European Medicines Agency, owing to a lack of long-term safety data. Hence, all available testosterone products are currently approved exclusively for use in men, with the exception of T-implants, which are approved in Australia for postmenopausal women. In contrast, for males there is increasing evidence that the use of testosterone replacement therapy is becoming more common. A study published by Handelsman12 demonstrated that off-label testosterone prescribing increased in most countries during 2000–2011, especially over the last half of the period.

A previous study conducted by Behre et al.13 evaluated the clinical practice of European physicians regarding diagnosis and management of testosterone deficiency syndrome in males, compared with current guidelines. The findings of the study demonstrated that the management appeared to be close to that recommended in international guidelines. Signs and symptoms of testosterone deficiency were fairly well known, but some diagnostic and treatment variations were observed. Although the study was comprehensive and included a large number of physicians, it did not investigate clinical practice regarding female androgen deficiency. Moreover, the participants in the survey were not specialized in sexual medicine. The present survey aimed to investigate clinical practice patterns of specialists in the field of sexual medicine, regarding diagnosis and treatment of androgen deficiency in men and women. Based on the responses, our intention is to develop an official statement of the European Society of Sexual Medicine (ESSM) on androgen replacement practice in both sexes.

Materials and methods

Attendees of the 16th annual congress of the ESSM held in January 2014 in Istanbul, Turkey, were invited to anonymously participate in a self-administered questionnaire comprising 24 closed questions (Appendix 1). Residents and trainees in sexual medicine were excluded from the study. The survey included a short introduction, which requested that the participants complete a questionnaire covering the criteria of diagnosis of androgen deficiency syndrome in men, and current clinical practice patterns related to androgen treatment in men and in women.

Main outcome measures

The survey consisted of three sections: the first assessed sociodemographic characteristics of the respondents; the second comprised four Likert-scale score items addressing professional background; the third comprised 16 Likert-scale score items assessing information about participants' current personal clinical practice patterns in terms of diagnosis and treatment modalities of androgen deficiency syndrome for men and women (Appendix 1).

Statistical analyses

Differences in proportions between independent respondent groups for categorical variables were assessed using the Pearson's χ2 test. All statistical tests were performed using SPSS v.21 (IBM Corp., Armonk, NY, USA). All tests were two-sided, with the significance level set at 0.05.

Results

Overall 705 physicians attended the meeting, out of which 138 were residents. Of the 567 specialized physicians, ESSM members approached 164 at the meeting venue. Thirty-one declined to fill the survey as the topic was beyond the scope of their everyday practice. Overall, 133 fellows participated in the survey. The mean age was 47 years (age range 25–79 years), of which 84% were males. The majority were urologists (n=96, 72%), 12 (9%) were family physicians, 13 (10%) gynecologists and 12 (9%) psychiatrists or of other specialties (e.g. cardiologists, endocrinologists). Sixty-six (50%) practiced medicine in academic institutes, whereas the remainder practiced in either public or private non-academic hospitals, or in private clinics, or both. A majority of participants, 80 (60%), practiced sexual medicine for >10 years, 20 (17%) for 5–10 years and 31 (23%) had <5 years experience in this discipline.

Male hypogonadism

Thirty-eight percent of participants reported that they frequently encounter men with suspected hypogonadism and another 9% reported that this occurs at least occasionally. Almost half of participants (66) reported that they assess serum testosterone levels for all males with erectile dysfunction, 35% for males with clinical symptoms of androgen deficiency, 28% for all males with metabolic syndrome (hypertension, diabetes, overweight and hyperlipidemia) and 14%, in general, for all males above the age of 50 years.

Regarding primary laboratory evaluation, 60% evaluated total testosterone; 19%, in addition, free testosterone; 22% sex hormone-binding globulin; 17% luteinizing hormone and 47% all of the above. The cutoff levels of testosterone below which the majority of participants (62%) considered testosterone replacement therapy in clinically symptomatic men was 8nmol l−1 (231 ng dl−1), 24% below a level of 10 nmol l−1 (298 ng dl−1) and 14% below a level of 12 nmol l−1 (346 ng dl−1).

When asked whether they prescribe testosterone replacement therapy for clinically symptomatic patients with total T-levels above 12 nmol l−1, 32% responded that they prescribe with no further evaluation, 25% only if there are obvious symptoms of androgen deficiency and 43% if the free testosterone level is also low. Among the different testosterone replacement therapy modalities, transdermal testosterone gel was most commonly prescribed (49%), followed by long-acting testosterone undecanoate injection (38%) and short-acting testosterone enanthate injection (13%).

The majority of practitioners restrict the period of T-replacement therapy: 40% prescribe it for a period of 3–6 months, 25% for 1 year, whereas the remaining 35% consider lifelong therapy. The majority (76%) of respondents were not concerned that treatment with testosterone replacement therapy in hypogonadal males may result in an increased risk of prostate cancer.

Female hypogonadism

The majority of participants in the survey correlated testosterone levels in women with libido (88%) and with sexual desire (79%); 40% with sexual arousal, 25% with lubrication and 17% with orgasm. Fifty-nine percent of participants confirmed that they evaluate serum testosterone levels in women with sexual disorders. Although 81% responded that testosterone treatment may have an effect on sexual desire, only 42% confirmed they would prescribe testosterone to premenopausal women with low sexual desire, and 53% to menopausal women with low desire. Of those who prescribe testosterone to postmenopausal women with low sexual desire and low testosterone level (51%), the majority prescribe transdermal testosterone gel (56%), 37% tibolone tablets and 7% testosterone injection. Most of the physicians who prescribe testosterone to women offer continuous treatment (69%) and the remaining recommend treatment only on demand, that is, before intercourse (31%).

χ2 Test of association was used to evaluate differences in the attitude of respondents according to age group, gender, specialty and number of years in practice. Our findings did not demonstrate significant differences according to subgroups, in the attitudes of physicians towards the diagnosis and treatment of male and female hypogonadism (P>0.05).

Discussion

More than two-thirds of the physicians who participated in this survey reported treating patients with suspected hypogonadism either on a regular or on an occasional basis. Differences were reported among the participants regarding the laboratory evaluations they order, indications for treatment, routes of testosterone administration and the duration of T-replacement treatment considered. These findings concur with the findings of a survey conducted by Shortridge et al.,14 in which ~2/3rd of males were prescribed with testosterone replacement therapy for androgen deficiency symptoms at the time of the survey.14 Establishing guidelines and publishing consensus statements are important to overcome the gaps in knowledge and to improve practice of specialists in the field of androgen deficiency. In addition, seminars, round tables and more educational activities are needed to disseminate knowledge among physicians around the world. Although our manuscript evaluated the attitudes of specialists toward androgen deficiency, patient education in this field is presumably also lacking. Bridging the gap of knowledge between patients and physicians is valuable to increase the rate of patient self- referral to primary care physicians. These actions will facilitate diagnosis at earlier stages, and will improve the compliance of patients toward treatment.

The International Society of Andrology, International Society for the Study of the Aging Male, the European Association of Urology, the European Academy of Andrology and the American Society of Andrology published a summary paper that details the definition, laboratory evaluation, indications and possible treatment for late onset hypogonadism in males.7 The authors concluded that there are no generally accepted lower limits of normal serum testosterone and that men with a serum concentration above 12 nmol l−1 mostly do not require substitution therapy, whereas those with concentrations below 8 nmol l−1 usually benefit from testosterone replacement therapy (Level 2b, grade A).7 These recommendations are in line with the clinical practice patterns of the participants of the present survey; the majority reported they would recommend testosterone replacement treatment in symptomatic males with testosterone levels <10 nmol ml−1, whereas only a small proportion considered treating symptomatic males with levels >12 nmol ml−1. The rationale for T-treatment of males with testosterone levels >12 nmol ml−1 and symptoms of testosterone deficiency may be explained by the relatively large interindividual variations of free testosterone concentrations and the lack of consensus regarding respective cutoff levels below which T-substitution should be considered.15 Regarding the available T-application modes, the majority of the physicians prefer a topical gel product over an injection or patch. This preference may be because of the ease of use of the gel16 and the possibility of immediately ceasing treatment in the case of side effects.

Only 24% of the participants in the survey expressed concerns that testosterone replacement therapy may increase the risk for prostate cancer in hypogonadal men. This is in agreement with the lack of conclusive evidence in the literature that testosterone therapy may increase the risk of prostate cancer or benign hyperplasia of the prostate. The International Society of Andrology recommends that before the administration of any testosterone therapy, the individual risk of prostate cancer must be assessed by adequate means, at minimum by a digital rectal examination (DRE), and determination of serum prostate-specific antigen. In addition, the risks and benefits of T-treatment are recommended to be clearly discussed with patients, during regular follow-up visits.

Regarding female sexual function, the majority of our participants expressed the opinion that testosterone levels and T-treatment correlate with sexual desire. The diagnosis of low androgen levels in women remains a challenging matter. This is mainly because the normal range of androgen-circulating levels has not yet been clearly defined, because of the intracellular conversion to active hormones17 and the relatively low absolute androgen serum levels, which are similar to the inter- and intra-assay variations of the commonly used tests in the clinical laboratories. The latter raises doubts about the reliability of the available lab tests to measure androgen levels in women. The role of androgens in women’s sexual health has long been an issue of debate. Despite numerous investigations, including randomized studies, the data linking low androgen levels to low sexual desire are still inconclusive and under debate. This problem is also mirrored by the inconsistency of related recommendations published over the years.18, 19 A task force group appointed by the Endocrine Society, the American Congress of Obstetricians and Gynecologists, the American Society for Reproductive Medicine, the European Society of Endocrinology and the International Menopause Society recently recommended short-term testosterone treatment for postmenopausal women with sexual dysfunction owing to hypoactive sexual desire disorder, but not for women with low androgen levels, as endogenous testosterone levels were not found to predict response to therapy.19 The results of our survey show a heterogeneous pattern regarding individual clinical practice, in terms of testosterone treatment for low sexual desire in pre- and postmenopausal women.

The most important limitation of this survey is the fact that the vast majority of participants were urologists; therefore, valid comparisons regarding clinical practice patterns related to androgen replacement therapy among practitioners from different specialties were not possible. Similarly, this limits the generalizability of the data. Our study did not evaluate the acquaintance of our participants with European or American guidelines. Rather, the validity of our findings is related to the common practice of specialists in sexual medicine. To better understand the reasons for the inconsistencies in this area, future study is needed to correlate common practice with general knowledge. Larger surveys that evaluate the common practice of family practitioners and gynecologists are also needed to better comprehend differences in practice and gaps in knowledge between specialists from different medical fields. The awareness and knowledge of patients from different geographical areas should also be evaluated. Once we gather all this information, educational activities for both health-care givers and patients can be targeted more effectively.

A study conducted by Tostain et al.20 showed fairly good knowledge of testosterone deficiency syndrome among French urologists, and a strong interest in administering treatment tailored to patient requirements and symptomatic efficiency. These findings suggest that part of the explanation for the large variability in the common practice of our surveyed physicians may be sourced in education.

In conclusion, the findings of our survey suggest consensus among physicians regarding the role of testosterone in sexual dysfunction, both in males and females. Most participants agree that symptomatic men with total testosterone <10 nmol l−1 should receive T-replacement therapy. Future research is needed to develop evidence-based guidelines for optimal laboratory tests and treatment for women with androgen deficiency syndrome and low sexual desire.

Despite the currently available literature, the diversity in knowledge and clinical practice patterns regarding the treatment of androgen deficiency in both women and men may reflect the need for comprehensive and substantial guidelines for this very common and significant medical condition.

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Correspondence to L Lowenstein.

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Appendix 1. The Questionnaire

Appendix 1. The Questionnaire

Section 1

Demographic data:

Please specify your

Age: _________ years

Gender: □Male □Female

Country of origin: _________

Country of practice: _________

Section 2

Professional background:

1. Please specify your occupation:

Physician 1□

Psychologist 2□

Sexual therapist 3□

Physical therapist 4□

Nurse (RN) 5□

Preclinical researcher 6□

Other, please specify _________

2. If you are a physician, please specify your specialty

Urologist 1□

Gynaecologist 2□

Psychiatrist 3□

Endocrinologist 4□

Cardiologist 5

General practitioner 6□

Other, please specify _________

3. For how long have you been practicing sexual medicine?

1□Less than 5 years 2□Between 5 and 10 years 3□More than 10 years

4. Do you practice in a private clinic or in the public health care system?

Academic hospital 1□

Private clinic/private practice 2□

Public health care system 3□

Both private and public health care system 4□

Other, please specify _________

Section 3

Male:

1. How often do you encounter men with suspected hypogonadism?

□Frequently

□Occasionally

□Almost never

□Never

2. For which indications do you order testing for serum testosterone levels in males?

All males with erectile dysfunction 1□

Only males with symptoms of androgen deficiency 2□

All males with metabolic syndrome (hypertension, diabetes, overweight and hyperlipidaemia) 3□

All males above the age of 50 years 4□

3. Which lab test do you order for primary evaluation of hypogonadism?

Free testosterone 1□

Free androgen index 2□

Total testosterone 3□

All the above 4□

4. What is the cutoff level of total testosterone under which you recommend androgen replacement treatment in symptomatic men?

8 nmol ml−1 1□

10 nmol ml−1 2□

12 nmol ml−1 3□

5. Do you prescribe androgen replacement treatment for symptomatic patients with total testosterone level above 12 nmol\ml

Yes, no need for further evaluation 1□

Yes, if free testosterone level is low 2□

No 3□

6. What is your drug of choice for treating androgen deficiency?

Short acting, Testosterone Enanthate injection 1□

Long acting, Undecanoate Testosterone injection 2□

Transdermal androgen preparate 3□

7. In your opinion, does treatment with androgen replacement in hypogonadal males result in an increased risk of prostate cancer?

Yes 1□

No 2□

Female:

8. In your opinion, is there a correlation between libido and testosterone level in women?

Yes 1□

No 2□

9. In your opinion, does testosterone prescription for women affect their libido?

Yes 1□

No 2□

10. Would you prescribe testosterone to pre menopausal women with low libido?

Yes 1□

No 2□

11. Would you prescribe testosterone to menopausal women with low libido?

Yes 1□

No 2□

12. In your opinion, which of the following sexual function domains in women are affected by a low level of androgen?

Libido 1□

Lubrication 2□

Sexual arousal 3□

Orgasm 4□

13. Do you test for serum testosterone level in women with sexual disorder?

Yes 1□

No 2□

14. How do you treat, if at all, postmenopausal women with low libido?

Transdermal testosterone gel 1□

Testosterone injection 2□

Tibolone tablets 3□

15. How do you prescribe testosterone to women?

Continuous treatment 1□

On demand before intercourse 2□

I don't prescribe 3□

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Lowenstein, L., Shechter, A., Porst, H. et al. Physicians' attitudes towards androgen replacement therapy for male and female sexual dysfunction. Int J Impot Res 28, 57–61 (2016). https://doi.org/10.1038/ijir.2016.2

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