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Impaired Sexual and Reproductive Outcomes in Women with Classical Forms of Congenital Adrenal Hyperplasia

Centre de Référence des Maladies Rares de la Différenciation Sexuelle (F.G., C.B., L.D., P.B.), Lyon-Paris, France; Department of Pediatric and Adult Endocrinology (R.B., E.T., F.K.), Necker Hospital, Paris V University, 75015 Paris, France; and Department of Pediatric Endocrinology (C.B., L.D., P.B.), Saint Vincent de Paul Hospital, Paris V University, 75014 Paris, France

Address all correspondence and requests for reprints to: Pierre Bougnères: Department of Paediatric Endocrinology, Hôpital Saint Vincent de Paul, 82 Avenue Denfert Rochereau, 75014 Paris, France. E-mail: bougneres{at}paris5.inserm.fr.

	Abstract

Top Abstract Introduction Patients and Methods Results Discussion References

 
Objectives: The objectives of the study were 2-fold: 1) a detailed description of sexual and reproductive outcomes in adult women with congenital adrenal hyperplasia (CAH) of different phenotypic severity at birth; and 2) comparisons of these outcomes among CAH subtypes and between CAH women and non-CAH control women.

Design: This was a cross-sectional study using a face-to-face interview, a written questionnaire, the Female Sexual Function Index, and a gynecological examination.

Patients: Patients included 35 women with CAH, representing Prader stages I–V at birth, aged 18–43 yr, who had been treated from birth to adolescence in the same pediatric endocrine clinics. Sixty-nine non-CAH healthy control women were selected from hospital-staff families.

Results: None of the CAH women expressed doubts about their gender assignment. Twenty percent (seven of 35) had homosexual inclinations; 23% (eight of 35) were married; three reported a complete lack of sexual activity; and 37% (13 of 35) said they never had heterosexual intercourse with vaginal penetration. Sexual functioning as assessed by the Female Sexual Function Index was much lower in CAH women than controls and lowest in CAH women with high Prader stages. Eighty-one percent (18 of 22) experienced pain during vaginal penetration. Only eight women became pregnant, and 17% (six of 35) had children.

Conclusions: Despite expert medical and surgical care by physicians dedicated to this rare disease, women with CAH still suffer major limitations in their sexual function and reproductive life.

	Introduction

Top Abstract Introduction Patients and Methods Results Discussion References

 
FEMALE NEONATES WITH congenital adrenal hyperplasia (CAH) due to 21-hydroxylase deficiency have various degrees of masculinization of their external genitalia. Despite suppressive glucocorticoid therapy, many of them remain exposed postnatally to an excess of adrenal androgens. Girls with the severe forms of sexual ambiguity (Prader stages IV–V) undergo extensive reconstructive surgery to correct clitoris, vulva, and vaginal anatomy. CAH girls of any subtype may develop chronic virilization, with muscle hypertrophy, acne, and hirsutism as well as secondary effects of corticosteroid therapy (fat accumulation, impaired growth). These factors could influence the development of sexuality in CAH adolescents and young women and decrease their physical attractiveness to partners.

Previous studies indicate that 46, XX CAH patients develop their gender identity as girls and women (1, 2) but show a wide spectrum of sexual outcomes. Whereas earlier studies suggest that a majority of patients have satisfactory intercourse (3, 4, 5), a high incidence of sexual dysfunction was more recently reported (6, 7, 8, 9, 10, 11), partly related to vaginal penetration difficulties (10, 11, 12, 13). CAH women may nevertheless be satisfied with the perceived quality of sexual relationships at large (7), whereas the sexual outcomes of women with the more masculinized reproductive tract were found to be markedly impaired (6, 13, 14), and those of girls with only a minor degree of genital ambiguity were reported to be near normal.

The current cross-sectional study describes sexual outcomes in a series of 35 adult women who, during their entire childhood, received their medical care and reconstructive surgery from the same specialized centers. A cohort of 69 healthy women largely comparable in age, ethnicity, and socioeconomic criteria agreed to participate as controls.

Starting with the work of Masters and Johnson (15), the quantitative evaluation of sexual function and dysfunction in women has gone through a continuous evolution. Evaluating female sexuality is undoubtedly a complex task in the normal population but can be expected to be even more difficult in patients with intersex status. Although it is obvious that questionnaires designed for statistical analysis and testing of therapeutics (16, 17) capture only a part of women’s sexuality (18, 19), we used the questionnaire approach, in addition to personalized interviews, because it allows a quantitative evaluation that would otherwise be impossible.

	Patients and Methods

Top Abstract Introduction Patients and Methods Results Discussion References

 
Patients

We reviewed the clinical records of 83 European females with 21-hydroxylase deficiency followed up from birth (between 1959 and 1985) to adolescence in the pediatric endocrinology clinics of Saint Vincent de Paul and Necker Hospitals. External genitalia were staged at birth according to Prader. All patients were raised as girls. For the current study, we were able to trace 50 patients (35 from Saint Vincent de Paul and 15 from Necker). They were contacted by telephone by clinicians they knew and then received a personalized letter, and 35 of them gave their written consent to participate, after being informed of the anonymous handling of data. The distribution of Prader stages was comparable with the series of the literature (20), in the participating patients: I (four), II (six), III (11), IV (11), or V (three); in those who refused to participate: I (two), II (two), III (six), IV (four), or V (one); and in those who could not be reached: I (five), II (six), III (10), IV (nine), or V (three).

Neonatal diagnosis of 21-hydroxylase deficiency was based on plasma 17-hydroxyprogesterone exceeding 50 ng/ml. After the diagnosis was established, therapy was begun with oral hydrocortisone around 20 mg/m² of body surface area per 24 h. During childhood and adolescence, the dosage was adjusted according to height, weight, growth velocity, bone age, and plasma 17-hydroxyprogesterone. If needed, patients received fludrocortisone in a single daily dose of 0.05–0.15 mg.

Age at the time of first surgery ranged from 6 months to 18 yr. Seventy-one percent (25 of 35) had a single surgical correction, consisting of a one-stage procedure with clitoroplasty, associated with vulvoplasty and vaginoplasty. The type of vaginoplasty (perineal or pull-through procedure) was determined by the point of entry of the vagina into the urogenital sinus (21). Clitoroplasty preserved the neurovascular bundle, with reanastomosis of the clitoral corpora, except in the two older patients who underwent total clitorectomy. The survival of the clitoris was reconfirmed at the current physical examination: only one patient had clitoral atrophy after resection surgery. Twenty-eight percent (10 of 35) had to undergo additional surgery (clitoroplasty and/or vaginoplasty), most of them once (Table 1).

Healthy Caucasian European non-Islamic women were recruited between 2003 and 2006 among 90 hospital staff families so as to be largely comparable in age and ethnicity within a wide range of socioprofessional levels, including families of workers, nurses, students, technicians, and maintenance and administration people (no physicians). The women, initially unknown to the investigators, were subsequently selected after a direct discussion with the investigators (L.D., C.B.) about the purpose of the study. One hundred twenty-five women agreed to participate from whom 69 were randomly selected. They answered the interview and FSFI questionnaire under the same conditions as the CAH women. Although they are not likely to reflect exactly the general population, the 69 control women were found to have reasonably representative characteristics when compared with large surveys of age-matched women in France (ACSF) (23), and we think that the differences were not likely to affect comparison with the CAH patients.

The study protocol was approved by our institutional review board for medical bioethics.

In the late 1990s, a survey of sexual behaviors, called ACSF, was performed in 7094 French women aged 19–44 yr, 1778 of whom completed detailed questionnaires (23). We used data from this ACSF survey for a comparison of selected sexual behavior variables in which CAH women appeared to differ largely from those reported in ACSF survey.

Questionnaires and interviews

Educational levels were assessed using a French scale (23). We used a French translation (24) of the FSFI, a brief, self-report measure of female sexual function based on clinical interpretations of a principal components analysis, which identified a 6-domain structure that included desire, subjective arousal, lubrication, orgasm, satisfaction, and pain (17). The standard FSFI scoring procedures is known to exaggerate the sexual impairment scores of sexually inactive women by equating abstinence with the extreme degree of impairment. Thus, instead of the standard FSFI, which covers only the preceding month, we used a longer time interval of 3 months to evaluate sexual function. The FSFI combines items of arousal and desire under the same factor. Participants reported it was difficult to evaluate items about lubrication unless they felt it created a problem during vaginal intercourse.

After the completion of the FSFI, a personalized interview was used to complement the analysis of sexual life. This interview included a list of preformulated questions and preestablished response categories. Sexual activity during the last year was evaluated using Kinsey’s hetero-homosexual rating scale (25). Questions directly relevant to the clinical symptoms and management of CAH were directed at perceived adequacy of results of reconstructive surgery, details of sexual life, psychosexual feelings, marital status, fertility, menstrual cycles, and educational level.

Prompts to assess perception of distress because of these conditions were used during the interview after the completion of the questionnaire.

Statistical analysis

Nonparametric Wilcoxon rank tests were used to compare the results of the FSFI questionnaire among the three subgroups of CAH patients composed, respectively, of women with Prader stages I–II (group 1, n = 10), Prader III (group 2, n = 11), and Prader IV–V (group 3, n = 14). We also used nonparametric Wilcoxon rank tests to compare FSFI scores in CAH groups and the 69 control women recruited for this study. ² tests were used to compare proportions observed during interviews of the CAH patients and the 69 control women. Although it is not statistically valid stricto sensu, a comparison using ² tests was attempted with the 1778 women aged 19–44 yr from the French population studied with long questionnaires in the ACSF survey (23), knowing that the ACSF women were recruited years ago for a different purpose. Subsequently the comparisons between CAH women and the ACSF sample were restricted to a few items that showed large differences in mean proportions (23). Despite the small size of the studied CAH subgroups, results are expressed as mean ± SD for simplicity of presentation.

	Results

Top Abstract Introduction Patients and Methods Results Discussion References

 
The demographic characteristics are presented in Table 2. The mean age of the participating CAH women was 29.5 yr (range 18–43 yr). Educational and socioprofessional criteria were comparable across the three Prader stage groups of CAH women and in the controls. The main physical characteristics of the participating CAH and control women are presented in Table 3. CAH women were somewhat shorter and more corpulent than the control women.

Analysis of interview data

Interview data on gender and sexuality are presented in Table 4. None of the CAH women expressed doubts about female gender assignment. Twenty percent (seven of 35) had homosexual inclinations, including erotic homosexual dreams and fantasies, vs. 5.7% (four of 69) in the control group and 6.6% (P < 0.001) in the ACSF survey (23). Homosexual inclinations were expressed by 43% (six of 14) of Prader IV–V women; 5.8% (two of 35) stated they were lesbians or had active homosexual experience vs. 2% in the ACSF survey of the population of French women (23). The Kinsey scale among the 32 women who had sexual activities (not necessarily with vaginal penetration) showed that 29 were K0 (exclusively heterosexual), one was K1 (predominantly heterosexual, only incidentally homosexual), another was K5 (predominantly homosexual, only incidentally heterosexual), and one was K3 (equally heterosexual and homosexual). The three women who reported a complete lack of sexual activity had Prader IV stage. According to examination and their own opinion, these three CAH women had had satisfactory surgical clitoral, vulva, and vaginal reconstruction.

The FSFI questionnaire revealed a global decrease of sexual function when all 35 patients were compared with the 69 healthy women, who showed sexual function scores (Table 5) comparable with those reported by Meston (26).

Fertility

Eight patients cohabited with their partner (two of 35) or were married (six of 35). Two additional women with Prader IV had cohabited for a few years with a partner. Seventy-seven percent of patients (27 of 35) wished to be pregnant in the near future (17 patients) or later (10 patients), compared with 58.5% in the subgroup of the ACSF women aged 20–40 yr, a potential difference that for methodological reasons was not tested statistically. Eight patients became pregnant (only one in the Prader IV–V group). Only 17% women (six of 35) had children, whereas 71% of French women had children in the ACSF survey (P < 0.01) and 65% (45/69) in the normal women recruited for this study (P < 0.02).

	Discussion

Top Abstract Introduction Patients and Methods Results Discussion References

 
Because the definition of female sexual function is complex in the general population with respect to qualitative or quantitative analysis (18, 19) and even more complex in patients with organic causes of sexual dysfunction, the current description of self-reported sexual outcomes did not pretend to analyze all aspects of the sexuality of CAH women. Our aim was more simply to underscore major sexual dysfunctions as reported by the patients and compare them with healthy control women in whom sexual outcomes were estimated in parallel by the same investigators using a uniform methodology.

A fraction of studied CAH women, mostly those with Prader stages IV or V, expressed a marked sense of masculinity and homosexual orientation but did not report more sexual experiences with women than controls. As reported (14), self-reported sexual arousability of CAH women was lower and showed a nonsignificant trend with frequency of sexual experiences with men. The frequency of sexual intercourse in general was decreased, more notably in the Prader stages IV–V group, with a 60% decrease in the frequency of sexual acts with vaginal penetration and a lower number of heterosexual partners. Of the 35 patients enrolled, 32 reported sexual activities but only 22 had at least once experienced vaginal penetration by the penis of a partner. Clear-cut differences were observed in CAH women with Prader stages IV–V for lubrication, orgasm, pain during vaginal penetration, and overall satisfaction with sexual acts. The extent of these differences, however, was unanticipated to us. Confirming earlier reports (6, 10, 27), significant but milder differences were also observed in the women with Prader stages I, II, and III, of whom 76% (16 of 22) had heterosexual intercourse with vaginal penetration at a near-normal frequency. Despite lower mean scores of pain, lubrication, and orgasm, the overall satisfaction score for sexual acts was not statistically different from control women. As observed here, studies report that more than 50% of CAH women are single (10, 27). Early papers were pessimistic with regard to fertility (10, 27), but more recently this figure was reported to improve to 60% (4) and even 90% of spontaneous or induced conceptions (28, 29). In the current series, however, only 22% of CAH women became pregnant and only one of 14 in the Prader IV–V group.

With regard to potential relationships between reconstructive surgery and the parameters of analysis of sexual activity and function, a major weakness of our study is that we did not investigate the CAH women with assessment of thermal, vibratory, or light-touch sensory thresholds in the clitoris and vagina using a genitosensory analyzer and Von Frey filaments, as performed in the careful studies of genital sensation by Crouch et al. (7). Only the external genitalia were examined here, including clitoris inspection and evaluation of vaginal introitus, and although cosmetic and anatomic outcomes of surgery were considered good in 60–70% of cases, we could not determine whether CAH women had abnormal clitoral or vaginal sensation. The abnormal sensory data in all six CAH women studied by Crouch et al. (7) suggest that genital surgery disrupts sensory input. Sexual function also appears to be impaired in the current study, which may relate to the compromised sensitivity and restricted introitus. Several other studies report a high incidence of vaginal stenosis, amounting to 35–90% of the patients (10, 11, 12, 30), compared with 25% in the current study. Our nine cases of vaginal stenosis and frequent pain during penetration do not allow statistical analysis but suggest that vaginoplasty should not be undertaken before puberty, when higher estrogen levels may prevent stenosis and, if necessary, dilatation can be performed by the patient.

Parents of patients who undergo clitoral and more generally reconstructive surgery should be fully informed of the risk to sexual function and functional consequences of the disease and therapy should be explained by female specialists to avoid fears about sexual acts (8). Whereas medical and surgical therapy appear to provide near satisfactory physical and genital appearance in more than two thirds of CAH women, the frequency and importance of self-reported sexual dysfunction and impaired reproductive outcomes call for medical and surgical progress (31).

	Acknowledgments

 
The authors have been able to analyze this large series of cases thanks to the earlier involvement of J. C. Job, R. Rappaport, J. L. Chaussain, C. Nihoul-Feketé, and F. Bargy. Due to the sensitive nature of collected information, this work is dedicated to the women who agreed to participate. We thank an anonymous reviewer for his (her) thoughtful suggestions.

	Footnotes

 
Disclosure Statement: The authors have nothing to declare.

First Published Online February 6, 2007

Abbreviations: CAH, Congenital adrenal hyperplasia; FSFI, Female Sexual Function Index.

Received August 14, 2006.

Accepted January 26, 2007.

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This Article Abstract Full Text (PDF) Submit a related Letter to the Editor Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Request Copyright Permission Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Gastaud, F. Articles by Bougnères, P. Search for Related Content PubMed PubMed Citation Articles by Gastaud, F. Articles by Bougnères, P. Related Collections Adrenal and Hypertension Female Endocrinology