Hypersexuality, Paraphilic Behaviors, and Gender Dysphoria in Individuals with Klinefelter s Syndrome
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1 1 ORIGINAL RESEARCH Hypersexuality, Paraphilic Behaviors, and Gender Dysphoria in Individuals with Klinefelter s Syndrome Alessandra D. Fisher, MD, PhD,* Giovanni Castellini, MD, PhD,* Helen Casale, Psy D,* Egidia Fanni, Psy D,* Elisa Bandini, MD,* Beatrice Campone, MD, Naika Ferruccio, MD, Elisa Maseroli, MD,* Valentina Boddi, MD,* Davide Dèttore, Psy D, Alessandro Pizzocaro, MD, Giancarlo Balercia, MD, Alessandro Oppo, MD,** Valdo Ricca, MD, and Mario Maggi, MD, PhD* *Department of Experimental, Clinical and Biomedical Sciences, Sexual Medicine and Andrology Unit, University of Florence, Florence, Italy; Psychiatry Unit, Department of Neurological and Psychiatric Sciences, University of Florence, Florence, Italy; Department of Health Sciences, University of Florence, Florence, Italy; Endocrinology Unit, IRCCS, Humanitas Research Hospital, Milan, Italy; Department of Clinical and Molecular Sciences, Endocrinology, Università Politecnica delle Marche, Ancona, Italy; **U.O.C. dell Azienda Ospedaliero, Universitaria di Monserrato, Monserrato, Italy DOI: /jsm ABSTRACT Introduction. An increased risk of autistic traits in Klinefelter syndrome (KS) has been reported. In addition, some studies have shown an increased incidence of gender dysphoria (GD) and paraphilia in autism spectrum disorder. Aim. The aim of this study was to evaluate the presence of (i) paraphilic fantasies and behaviors; and (ii) GD symptomatology in KS. Methods and Main Outcomes Measures. A sample of 46 KS individuals and 43 healthy male controls (HC) were evaluated. Subjects were studied by means of several psychometric tests, such as Autism Spectrum Quotient (AQ) and Reading the Mind in the Eyes Revised (RME) to measure autistic traits, Gender Identity/GD questionnaire (GIDYQ-AA), and Sexual Addiction Screening Test (SAST). In addition, body uneasiness psychopathological symptoms were assessed using Symptom Checklist 90 Revised (SCL-90-R). The presence and frequency of any paraphilic fantasy and behavior was assessed by means of a clinical interview based on Diagnostic and Statistical Manual of Mental Disorders, 5th Edition criteria. Finally, all individuals included were assessed by Wechsler Adult Intelligence Scale-Revised to evaluate intelligence quotient (IQ). Data from a subsample of a previous published series of male to female GD individuals, with the battery of psychological measures useful to provide a psychopathological explanation of GD in KS population available, was also considered. Results. When compared with HC, KS reported significantly lower total, verbal and performance IQ scores and higher SCL-90 obsession-compulsive symptoms (all P < 0.001). In line with previously reported findings, KS showed higher autistic traits according with both RME and AQ tests (P < 0.001). With respect to sexuality, KS showed a significant higher frequency of voyeuristic fantasies during masturbation (52.2% vs. 25.6%) and higher SAST scores (P = 0.012). A mediation role of obsessive symptoms on the relationship between Klinefelter and SAST was confirmed (unstandardized estimate b = 2.75, standard error = 0.43 P < 0.001). Finally, KS individuals showed significantly higher gender dysphoric symptoms than HC (P = 0.004), which were mediated by the presence of autistic traits (Sobel s test; P < 0.05). Conclusions. KS is associated with hypersexuality, paraphilic behaviors, and GD, which were mediated by obsessivecompulsive and autistic traits. Alessandra D. Fisher, Giovanni Castellini, Helen Casale, Egidia Fanni, Elisa Bandini, Beatrice Campone, Naika Ferruccio, Elisa Maseroli, Valentina Boddi, Davide Dèttore, Alessandro Pizzocaro, Giancarlo Balercia, Alessandro Oppo, Valdo Ricca, and Mario Maggi. Hypersexuality, paraphilic behaviors, and gender dysphoria in individuals with Klinefelter s syndrome.. Key Words. Paraphilias, Hypersexuality, Gender Dysphoria, Klinefelter Syndrome 2015 International Society for Sexual Medicine
2 2 Fisher et al. Introduction Klinefelter s syndrome (KS) is the most frequent Disorder of Sex Development [1] with an estimated prevalence ranging between 1:400 and 1:1000 [2]. The majority of affected men carry a 47,XXY karyotype, while the other cases remaining have supernumerary X chromosomes or mosaic forms [3,4]. According to their original description [5], Klinefelter individuals have been described with small testes, sterility, hypergonadotropic hypogonadism, gynecomastia, and tall stature with eunuchoid body proportions. Individuals with KS seem to be at a higher risk for intellectual disability [6], emotional, and behavioral dysregulation, as well as for difficulties in communication and social skills [7]. Characteristic cognitive defects have been reported, with specific impairment in expressive language skills (i.e., verbal processing speed, expressive grammar, word retrieval [7]). In addition, men with KS experience insufficient emotional arousal [8]. Men with KS usually report a male gender identity [9]. However, two recent studies [9,10], analyzing the karyotypes of large samples of transsexuals, found that, although chromosomal abnormalities were not overrepresented in this sample, the prevalence of KS was significantly higher than what was to be expected, based on population data [11]. In addition, a case report describing female gender identity in KS individuals is available [12]. It should be recognized that KS gender identity has not been systematically studied, and it is possible that not all gender clinics have reported the observed karyotype variations [9]. In addition, there is evidence that KS is markedly underdiagnosed in the general male population [13], and increasing the detection rate of this syndrome in the general population would be desirable. With respect to mental health, the phenotype is quite variable. Data on psychiatric screenings in adult with KS have demonstrated a high prevalence of psychosis and depression [7,8]. Furthermore, an increased risk of autistic traits has been reported in patients with KS [14,15]. It could be speculated that the autistic spectrum represents an explanative mechanism for some of the clinical features of the KS population. Indeed, some studies have shown an increased incidence of GD in subjects with autism spectrum disorders [16 19]. Furthermore, in persons affected by autism spectrum disorders, inappropriate sexual behavior has been observed [20,21], ranging from unusual forms of masturbation with unconventional objects to unwanted sexual contact and paraphilias. However, no systemic studies are available in literature that address paraphilic traits, as well as gender identity and orientation, in KS subjects. Aims The aim of the present study was to assess the presence of (i) paraphilic fantasies and behaviors; and (ii) gender dysphoria (GD) symptomatology in KS. Moreover, given the increased prevalence of GD and paraphilia reported in autism spectrum disorder and the increased risk of autistic traits in the KS population, we attempted to evaluate the role of autistic traits as a possible mediator of GD and sexual behaviors in KS. Methods and Main Outcomes Measures Study Design The study was conducted at the Sexual Medicine and Andrology Unit of the University of Florence, Ancona, Milano and Cagliari University Hospitals. A consecutive series of 47,XXY individuals referred was evaluated on the first day of admission to the clinics by means of a clinical and psychometric assessment. Patients were compared with a group of healthy male controls (HC) recruited by means of advertisement in the University Hospital; HC men were asked to participate as controls in a study assessing psychosexual characteristics of patients with a chromosomal disorder and they underwent the same assessment described below. Study procedures were fully explained during the first routine visit and prior to the collection of data; after that, the patients were asked to provide a written informed consent. Finally a series of GD male to female (MtF) persons referred to Florence Gender Clinic were enrolled. The MtF GD group mentioned was a subsample of a previous published series of GD individuals [22] in which the battery of psychological measures useful to provide a psychopathological explanation of GD in KS population was available. The study protocol was approved by the Institution s Ethics Committee. Participants KS patients attending the Sexual Medicine and Andrology Unit of Florence, Ancona, Milano and
3 Klinefelter Syndrome, Hypersexuality, Gender Dysphoria 3 Cagliari University Hospitals between December 2013 and March 2015 were enrolled in the study, provided they met the following inclusion criteria: (i) minimum age of 18; (ii) total serum testosterone 10.4 nmol/l [23]; and (iii) if testosterone replacement therapy was used, the latter should have started at least 6 months before enrollment. The exclusion criteria were based on the presence of a total intelligence quotient (TIQ) < 50 and illitteracy. A total of seven subjects were excluded from the initial sample because of the following reasons: low IQ (n = 3), age < 18 yers (n = 4). KS was diagnosed on the basis of clinical and biochemical suspicion and confirmed through the karyotype analysis. For the HC group the inclusion criteria included (i) minimum age of 18, (ii) total serum testosterone 10.4 nmol/l. The exclusion criteria for HC group were a TIQ < 50, and the presence of congenital hypogonadism diagnosis. In addition, 67 individuals referred to Florence Gender Clinic, with MtF GD diagnosis, based on formal psychiatric classification criteria [24,25] and performed through several sessions with two different mental health professionals specializing in GD, were included. Participants did not receive any payment. Assessment KS and HC individuals underwent a complete physical examination, with measurement of height, weight, and body mass index. Blood samples were drawn in the morning for determination of total testosterone levels (by electrocheminulescent method, Modular Roche, Milan, Italy). In addition, KS and HC individuals were asked to complete several psychometric tests, such as the Body Uneasiness Test (BUT [26]), Symptom Checklist 90 revised (SCL-90-R [27,28]), Autism Spectrum Quotient (AQ [29]), Reading the Mind in the Eyes Revised (RME [30]), Gender Identity/GD questionnaire (GIDYQ-AA [31,32]), visual analog scale (VAS) for gender identity, VAS for Sexual Orientation, Sexual Addiction Screening Test (SAST [33]), and International Index for Erectile Dysfunction ([34,35]). Moreover, subjects were evaluated using the SIEDY Structured Interview for erectile dysfunction [36] as well as the Structured Clinical Interviews for Diagnostic and Statistical Manual of Mental Disorders (DSM) (SCID I and SCID II) to evaluate axis I and II disorders [37 39].The presence and frequency of any paraphilic fantasy and behavior (associated or not to masturbatory activity) was evaluated by means of a clinical interview based on DSM-5 criteria [24]. Finally, all individuals included were assessed by Wechsler Adult Intelligence Scale-Revised to evaluate the TIQ, verbal intelligence quotient (VIQ) and performance intelligence quotient (PIQ) [40]. The testing protocol took about 2 hours. GD Clients Were Asked to Complete GIDYQ-AA, RME and AQ Questionnaires BUT is a self-rating scale exploring different areas of body-related psychopathology, in particular specific worries about certain body parts or characteristics [26]. Subjects were asked to rate 37 body parts, indicating how often they happen to dislike each experience or each body part. Higher scores indicate greater body uneasiness. Psychopathological symptoms were assessed through the Italian version of SCL-90-R [28]. SCL-90-R is a measure of the psychological state using question items that ask, on a 5-point scale, how much a certain problem has bothered the subject over the past 7 days, allowing nine primary symptom scales and three global indices of distress to be derived [27,28]. Internal coherence was good for all subscales (α values between 0.70 and 0.96). AQ is a self-rating questionnaire measuring the extent of autistic traits in adults and exploring five domains of behaviors: social skill, attention switching, attention to detail, communication, and imagination. Total score equal or higher than 32 is suggestive of significant autistic traits [29]. RME [30] evaluates the ability to attribute mental states to another person ( mentalizing ) and this capacity is the main way to predict other people s behavior. The Italian version of AQ and RME have been downloaded from the Autism Research Center official website ( GIDYQ-AA is a 27-item questionnaire evaluating GD [31,32]. Each item is rated on a 5-point response scale, with the past 12 months as the time frame. The response options were always (coded as 1), often (2), sometimes (3), rarely (4), or never (5). Lower scores are associated with higher GD. Internal coherence was good for the Italian validated version (α value of between 0.97) [32]. VAS for gender identity evaluates gender identity dimensionally, rating 0 when the subject has an absolute identification with the opposite genotypic sex and 10 with their own sex. Depending on the
4 4 Fisher et al. evaluated score, every individual is considered as having a feminine (=0), masculine (=10) or gender variant identity (>0 and <10). VAS for sexual orientation evaluates sexual orientation dimensionally, rating 0 when sexual attraction was exclusively toward men and 10 when sexual attraction was exclusively toward women. Depending on the evaluated score, every individual is considered as having a homosexual (=0), heterosexual (=10) or bisexual (>0 and <10) sexual orientation. Sexual Addiction Screening Test (SAST) is a self-rating questionnaire designed to assess sexually compulsive or addictive behavior or thoughts and to help clinicians to discriminate between addictive and non-addictive behaviors [33]. In order to obtain an Italian version of SAST, a process of translation, back-translation and semantic concordance evaluation has been performed independently by two bilingual translators, who were experienced psychiatrists and English native speakers. Finally, International Index of Erectile Function (IIEF-15) was used to evaluate erectile function (EF domain), orgasmic function, sexual satisfaction (overall satisfaction; intercourse satisfaction), and sexual desire [34]. We used the IIEF in its Italian translation [35]. Statistical Analyses Continuous variables were reported as mean ± standard deviation (SD), whereas categorical variables were reported as numbers and percentages. The independent sample t-test and the χ 2 were used for continuous and categorical variables, respectively, to compare KS and healthy controls groups. In order to evaluate the effects of different confounders, logistic regression analyses were performed, entering age and TIQ as covariates, the latter adjustment because TIQ was different between HC and KS individuals. Analysis of covariance was used to assess differences between groups for different variables. Control variables used in the models were age and TIQ for comparison between HC and KS, whereas only age was used as control variable when GD and KS were compared. An ordinal logistic model, adjusted for the same confounders was applied to assess the relationship between having KS and BUT scores. Finally, moderators and mediators analyses were performed, according to Baron & Kenny and a more recently Hayes & Preacher model [41,42]. A moderator is a qualitative or quantitative variable that affects the direction and/or strength of the relationship between an independent or predictor variable and a dependent or criterion variable. Linear Regression Analyses and General Linear Model were adopted to test the moderator function, adjusting for age and TIQ. For mediation analyses, we adopted PROCESS program, a computational tool for path analysisbased moderation and mediation analysis as well as their combination as a conditional process model [42]. According to this method, when mediation is hypothesized, an independent variable (diagnosis of Klinefelter) is expected to affect an intervening variable (obsessive symptoms), which, in turn, is expected to affect a dependent variable (SAST score). In the framework of path analysis, the mediated effect is referred to as an indirect effect [42]. Complete mediation requires that the full effect of the independent variable on the dependent variable be carried by the mediator, while partial mediation recognizes that independent variables may have their own direct effects on the dependent variable that are independent of the mediator. To test indirect effect and the mediation hypothesis the Sobel test [43] was adopted, providing an approximate significance test for the indirect effect of the independent variable on the dependent variable via the mediator. Moreover, given that the Sobel method for testing the indirect effect has been reported to show reduced power to test the indirect effect that may be appreciable with small effect sizes or small sample sizes, following recommendations by Edwards and Lambert [44], we also used the bias-corrected bootstrapping method to construct the 95% confidence interval for the indirect effect. All analyses were performed using SPSS version 20 (SPSS Inc., Chicago, IL, USA). Results Comparisons between Klinefelter Patients and Healthy Controls: Clinical Variables Of the 49 Klinefelter subjects who met the participation criteria, 46 (93.8%) agreed to participate in the study (mean ± SD age = ± years). A control group of 43 healthy subjects (HC), of similar age was also enrolled (mean ± SD age = ± years, P = 0.07). Among the subjects studied (n = 89), 79 (88%) were from Florence, 4 (4.5%) from Milano, 4 (4.5%) from Ancona, and 2 (2.2%) from Cagliari University Hospitals. No criminal offences were reported by the participant (including both KS and control groups).
5 Klinefelter Syndrome, Hypersexuality, Gender Dysphoria 5 Table 1 Socio-demographic and clinical characteristics Healthy controls (n = 43) Klinefelter (n = 46) Age-adjusted d ± SD Adjusted P Testosterone (nmol/l) ± ± ± Testis volume (ml) ± ± ± 0.54 <0.001 Height (cm) 1.76 ± ± ± 0.02 <0.001 Weight (kg) ± ± ± 2.73 <0.001 Body mass index (kg/m 2 ) ± ± ± Waist (cm) ± ± ± 2.20 <0.001 Educational level (years of school) ± ± ± 0.68 <0.001 TIQ ± ± ± 2.99 <0.001 PIQ ± ± ± 3.09 <0.001 VIQ ± ± ± 3.02 <0.001 Healthy controls (n = 43) Klinefelter (n = 46) Age-adjusted d ± SD OR 95% CI Adjusted P Adjusted P Gynecomastia %, (n) 0 (0) 58.7 (27) 1.07; Stable relationship %, (n) 90.1 (39) 80.4 (37) 1.18; Current smoker %, (n) 11.6 (5) 37.0 (17) 4.73; Alcohol consumption ( l4 drinks/day)%, (n) 4.7 (2) 4.3 (2) 0.34; Data are expressed as mean ± SD when normally distributed and as percentages and absolute number, reported in brackets, when categorical The multivariate analysis (entering age as a covariate) has been performed using analysis of covariance for linear variables and binary logistic regression for dummy variables Adjusted d = adjusted mean difference; OR = odds ratio; PIQ = performance intelligence quotient; SD = standard deviation, TIQ = total intelligence quotient; VIQ = verbal intelligence quotient Table 1 reports the socio-demographic and clinical variables of both groups and their differences in an age-adjusted model. As expected (all the KS patients were on testosterone substitution), no significant differences were observed in terms of testosterone levels. KS patients showed higher weight, height and waist, as well as a lower testis volume than HC subjects. In addition, 58.7% of KS subjects reported gynecomastia. KS subjects obtained lower TIQ, VIQ, and PIQ scores, along with a lower education level, when compared with HC. In particular, 17.1% of KS obtained just the primary school degree and only 2.4% the university one (vs. 0% and 75%, respectively). Smoking habit was more often reported in KS (KS = 37.0% vs. HC = 11.6%), while no significant difference was found in terms of alcohol assumption ( 4 drinks/day: KS = 4.3% vs. HC = 4.7%). Table 2 reports differences in terms of psychopathological variables and autistic traits after adjusting for age, and TIQ. As far as psychopathological condition is concerned, compared with HC, KS subjects reported higher SCL-90-R Positive Symptom Distress Index (PSDI), and subscale scores as follows: SCL-90 Obsession-Compulsive (O-C), and SCL-90-R Somatization (SOM). Furthermore, KS subjects showed a higher frequency of Axis I Psychiatric Disorders according to DSM-IV criteria (30.4% vs. 7.0%), which was due to a higher prevalence of Mood Disorders. In line with previously findings, KS subjects showed higher autistic traits, as compared with the HC, according to both RME and Autism Spectrum Quotient (AQ) tests. Considering BUT, the KS group showed significantly higher uneasiness related to genitals, as compared with the HC after adjusting for age, and TIQ (1.80 ± 2.00 vs ± 0.97, F = 5.81, P = 0.019). Other comparisons on BUT scores were not significant (data not shown). In an ordinal logistic model, adjusted for confounders (age and TIQ), there was a significant relationship between having KS and genital BUT (Wald = 6.033, P = 0.014), which disappears when testis volume was introduced in the model as a further covariate (Wald = 0.46, P = 0.49). Conversely, other body parameters, such as height and weight, did not affect the relationship (not shown). Comparisons between Klinefelter Patients and Healthy Controls: Sexual Orientation and Behaviors Table 3 reports differences in terms of sexual orientation and behaviors between KS and HC after adjusting for age and TIQ. Concerning sexual orientation, no differences were found between groups. Most (91.3%) of the KS subjects reported sexual attraction exclusively toward women. Exclusive homosexuality and bisexuality was reported respectively by 4.3% (n = 2) and 2.2% (n = 1) of KS individuals.
6 6 Fisher et al. Table 2 Psychopathological variables and autistic traits Healthy controls (n = 43) Klinefelter (n = 46) OR 95% CI Adjusted P Axis I disorder, % (n) 7.0 (3) 30.4 (14) 12.68; Anxiety disorders 2.3 (1) 10.9 (5) 5.13; Mood disorders 4.7 (2) 21.7 (10) 7.57; Axis II disorder %, (n) 2.3 (1) 4.7 (2) 6.80; Age- and TIQadjusted Adjusted P d SCL-90-R General symptomatic index 0.31 ± ± ± [ ] [ ] Positive symptom total ± ± ± [ ] [ ] Positive symptom distress index 1.20 ± ± ± [ ] [ ] Obsession-compulsion 0.38 ± ± ± [ ] [ ] Somatization 0.27 ± ± ± [ ] [ ] Interpersonal sensitivity 0.37 ± ± ± [ ] [ ] Depression 0.33 ± ± ± [ ] [ ] Anxiety 0.32 ± ± ± [ ] [ ] Hostility 0.31 ± ± ± [ ] [ ] Phobic anxiety 0.52 ± ± ± [ ] [ ] Paranoid ideation 0.32 ± ± ± [ ] [ ] Psychoticism 0.17 ± ± ± [ ] [ ] RME ± ± ± AQ ± ± ± Data are expressed as mean ± SD when normally distributed, and as percentages and absolute number, reported in round brackets, when categorical. In square brackets are reported the absolute ranges of SCL-90-R scales The multivariate analysis (entering age and TIQ as covariates) has been performed using analysis of covariance for linear variables and binary logistic regression for dummy variables AQ = Autism Spectrum Quotient, RME = Reading the Mind in the Eyes; SCL-90-R = Symptoms Checklist revised; TIQ = total intelligence quotient Considering hypersexuality, the KS group reported significantly higher Sexual Addiction Screening Test (SAST) scores. When paraphilic fantasies and behaviors were assessed, KS subjects showed a higher frequency of voyeuristic fantasies (defined as recurrent and intense sexual arousal from observing an unsuspecting person who is naked, in the process of disrobing, or engaging in sexual activity), during masturbation (52.2% vs. 25.6%). This finding was confirmed when the related VAS was considered. No significant differences between groups were found when paraphilic disorders defined according DSM-5 criteria were considered. Finally, KS individuals reported significantly lower GIDYQ-AA scores. No significant differences were detected in Sexual Orientation and Gender Identity VAS. Finally, no significant differences were detected in terms of IIEF scores. Comparisons between Klinefelter Patients and GD Individuals: GD Levels and Autistic Traits A group of 67 MtF GD (mean ± SD age = ± years, P < vs. KS) referred to Florence Gender Clinic was also included for a secondary analysis. GIDYQ-AA medium scores reported by KS subjects are not at a critical threshold to suggest GD diagnosis (<3 [31],) and are different from scores reported in MtF individuals, diagnosed according to DSM-5 criteria (4.65 ± 0.38 vs ± 0.32, adjusted d = 2.37 ± 0.08, P < after adjustment for age [21,25]). This indicates that levels of GD in KS were significantly lower than in transsexual individuals. In addition, no one in the KS group had a GIDYQ-AA score < 3. Moreover, no one between the KS group met the criteria for GD according to DSM-5 [24]. In addition, KS subjects showed significantly higher AQ and lower RME levels as compared
7 Klinefelter Syndrome, Hypersexuality, Gender Dysphoria 7 Table 3 Sexual Orientation and Behaviors Healthy controls (n = 43) Klinefelter (n = 46) OR 95% CI Adjusted P Male partner 2.3 (1) 4.3 (2) 1.46; Referred Sexual orientation Sexual attraction exclusively toward men 2.3 (1) 4.3 (2) 1.46; Sexual attraction exclusively toward women 90.7 (39) 91.3 (42) 1.12; Sexual attraction toward both men and women 4.7 (2) 2.2 (1) 1.62; Sexual attraction toward no one 2.3 (1) 2.2 (1) 0.14; Age- and TIQadjusted Adjusted P d Sexual orientation VAS (cm) 9.77 ± ± ± Gender identity VAS (cm) 9.66 ± ± ± SAST total score 2.00 ± ± ± GIDYQ-AA 4.99 ± ± ± IEEF Erectile function domain ± ± ± Overall function domain 9.26 ± ± ± Sexual desire domain 8.14 ± ± ± Intercourse satisfaction domain 9.63 ± ± ± Overall satisfaction domain 8.26 ± ± ± Data are expressed as mean ± SD when normally distributed, as median [quartiles in brackets] when not normally distributed, and as percentages and absolute number, reported in brackets, when categorical. Comparisons were performed by means of linear and logistic regression analyses for continuous and categorical variables, respectively, entering age and TIQ as covariates Adjusted d = adjusted mean difference; GIDYQ-AA = Gender Identity/Gender Dysphoria questionnaire for Adolescents and Adults; IEEF = International Index for Erectile Dysfunction; VAS = visual analog scale; SAST = sexual addiction screening test total score with the GD individuals (20.65 ± 5.30 vs ± 6.48, adjusted d = 2.52 ± 1.25, P < 0.05; ± 5.45 vs ± 4.50, adjusted d = 4.12 ± 1.05, P < after adjustment for age, respectively) indicating the presence of higher autistic traits. Mediation Models for Sexual Orientation and Sexual Behaviors Figure 1 and 2 reports the performed mediation models. The relationship between KS and Sexually Compulsive Behaviors (SAST scores) was hypothesized to be an indirect effect that exists due to the influence of obsessive-compulsive symptoms as a mediator. According to the mediation model: (i) group categorization (KS vs. HC) significantly accounted for the variation of the mediator (SCL- 90-R O-C symptoms; β=0.026; P = 0.04); (ii) variation in the mediator significantly accounted for variation in the dependent variable (SAST score, β = 0.307; P = 0.03); and (iii) group categorization significantly accounted for variation in the dependent variable (SAST score, β=0.60; P < ). Furthermore, to test the hypothesized mediation model, PROCESS estimated the indirect effect of Klinefelter on SAST through obsessive symptoms (mediator). Using Sobel s [43] standard error (SE), the indirect effect (unstandardized estimate b = 2.75, SE = 0.43 P < 0.001) was significant. Following recommendations by Edwards and Lambert [44] we also used the bias-corrected bootstrapping method to construct the 95% confidence interval for the indirect effect. The 95% confidence interval for the indirect effect was 0.562; and did not include zero. Therefore, we can conclude that the indirect effect was Figure 1 Indirect effect of Klinefelter on SAST through obsessive symptoms (mediator). SAST = Sexual Addiction Screening Test; SCL-90-R = Symptom Checklist 90 Revised. Figure 2 Indirect effect of Klinefelter on gender dysphoria through autism (mediator).
8 8 Fisher et al. significantly different from zero at α=0.05, confirming the mediation role of obsessive symptoms on the association between Klinefelter and SAST (Figure 1). A similar model was performed for the relationship between Klinefelter s and GD. According to the mediation model: (i) group categorization (KS vs. HC) significantly accounted for variation of the mediator (autism, as measured by Autism Quotient Test, β = 0.26; P < 0.05); (ii) variation in the mediator significantly accounted for variation in the dependent variable (GD, β = 0.31; P = 0.003); and (iii) group categorization significantly accounted for variation in the dependent variable (GD, β= 0.26; P < 0.05).The same PROCESS model was applied to calculate the indirect effect of Klinefelter on GD through autism (mediator). The indirect effect (unstandardized estimate b = 0.019, SE = P = ) was significant. The 95% confidence interval for the indirect effect was 0.235; and did not include zero, confirming the mediation role of autism on the association between Klinefelter and GD (Figure 2). Finally, a moderator analysis was performed to evaluate whether the relationship between GD and autism was present in both KS and GD groups (Figure 3). General linear model revealed a significant interaction between autism and group categorization (KS vs. MtF) on GD score (F = 9.08; t = 3.01, P < 0.005). When the interaction was broken down, it appears that the association between autism and GD was present only in the KS group (β =0.27; P < 0.001), but not in the GD group. All the analyses were adjusted for age and TIQ. Discussion To the best of our knowledge, this is one of the few studies, which attempts to provide a psychopathological explanation of GD and atypical sexual attitudes in a KS population. The main results of the present study are the followings: (i) the KS group showed a higher risk of developing hypersexuality and voyeuristic fantasies during autoeroticism; (ii) hypersexuality in KS seems to be mediated by the presence of relevant obsessive-compulsive (O-C) traits and symptoms; (iii) KS individuals reported higher rates of GD compared with HC; (iv) GD in KS was mediated by the presence of autistic traits. Considering the psychopathological features of KS, this study reports a higher risk of developing a Figure 3 Association between Autism Spectrum Quotient and GIDYQ-AA in GD (Panel A) and in KS (Panel B) groups. Adj. r derived by linear regression analysis are reported. GIDYQ-AA scores were associated with Autism Spectrum Quotient only in KS subjects but not in the GD group. GIDYQ-AA = Gender Identity/Gender Dysphoria Questionnaire for Adolescents and Adults; KS = Klinefelter syndrome; GD = gender dysphoria. compulsive sexual behavior. This result is quite surprising, considering the higher levels of body dissatisfaction reported by KS subjects, when compared with HC, which could theoretically inhibit sexuality, rather than cause a loss of control toward it. In fact, as expected, body satisfaction was significantly affected in relation to body parts related to sexuality such as genitals. We can thus postulate that the higher SAST levels observed are more an expression of intrusive and obsessional thoughts related to sexuality rather than a real hypersexual behavior. We also found that, when compared with HC, KS individuals also had significantly higher scores at SCL- 90-R-PSDI a global index of intensity of psychological distress and SOM, as well as at O-C SCL-90-R scales. The higher levels of SOM
9 Klinefelter Syndrome, Hypersexuality, Gender Dysphoria 9 reflect the distress arising from bodily perception [27] and is in line with the significantly lower levels of body satisfaction previously mentioned. Furthermore, in the present study we also observed that KS patients were at a higher risk for axis I disorders in line with previous studies [7,45,46], confirming a significant psychopathological vulnerability in KS subjects [14]. In fact, consistent with previous reports, a vulnerability in psychopathological domains has been observed in KS In particular, Tartaglia et al. [14], reported that at least 25% of KS subjects endorsed concerns in the areas of anxiety, depression, and somatic complaints, and over 50% reported concerns regarding social withdrawal. To our knowledge, this is the first study reporting that O-C symptoms defined as thoughts, impulses, and actions experienced as irresistible and at the same time unwanted by the individual [27] were significantly increased in a Klinefelter population. Considering the higher scores reported by KS patients as compared with HC in O-C (SCL-90) and paraphilic symptoms (SAST), we found that these differences were almost due to cognitive (e.g., obsessive thoughts and intrusive fantasies related to sexual activity), rather than behavioral items (data not shown). In line with the previous hypothesis, when a mediator model for sexual addiction was applied, we observed that the relative hypersexuality (increased sexual compulsive behaviors or thoughts) observed in KS was mediated by the presence of obsessive traits and by the related ruminative thinking. The same determinant could explain the higher frequency of voyeuristic fantasies during autoeroticism observed in KS subjects. In fact, the presence of sexually intrusive thoughts, together with dissatisfaction for sexual body parts, can eventually lead KS individuals to experience less confidence in behaving as protagonists in a sexual relationship and to activate, consequently, a voyeuristic behavior. Using the RME, beside to Autism Spectrum Quotient (AQ), we here confirmed that KS subjects have significantly less capacity to mentalizing and therefore to predict another person s behavior, when compared with HC [29,30,45,47 50]. Moreover, the fact that both AQ and RME were significantly associated with KS, emphasizes that both measure autistic traits across the notional spectrum [30]. The presence of autistic traits in KS, extensively described in the literature [45,47 50], has found several explanations. Bishop et al. proposed that, in KS individuals, the overexpression of X-linked neuroligin a gene involved in synaptic plasticity may play a significant role in communication impairments and autism spectrum disorder [50,51]. Other authors, using functional magnetic resonance imaging, have observed an increased activation in frontal areas (including Broca s area) during labeling of facial expressions in KS individuals compared with controls [48]. Based on these results, they postulated the presence of an underlying neural mechanism behind autistic traits in 46,XXY individuals [48]. Finally, these results should be considered in the light of the observation that not all KS persons showed impaired intelligence. The relatively surprising results on higher gender dysphoric symptoms in KS may, at first glance, underline the importance of sex chromosome assessment during GD evaluation, not yet routinely recommended [9,10]. However, it has been noted that GIDYQ-AA scores reported by KS subjects studied are not at a critical threshold to suggest GD diagnosis and levels of GD in KS were significantly lower than in transsexual individuals. Indeed, although more evidences regarding this topic are needed, previous researches showed that KS in GD may not be overrepresented [9,10]. Our results should be better considered in the light of the dimensional construct of GD rather than in a dichotomous way. Moreover, moderator analyses demonstrated that gender dysphoric symptoms of KS individuals might be an epiphenomenon of the autistic traits. We can postulate that the rigid thinking, typical of autism traits, observed in KS patients, can cause uneasiness and distress related to gender identity in individuals otherwise not perceiving themselves as a stereotype of alpha-male. In fact, a mediating effect of autistic traits was found for GD in the KS group. A different explanation for the significant higher gender dysphoric symptoms observed in KS individuals can be related to the decreased masculine behavior and gender nonconformity previously reported in this population [52 54]. In particular, it has been observed that KS boys feel more negatively about their male gender role and are judged less masculine by the peer group [54], which can be according to some authors [53,55] a consequence of lower testosterone levels at midpuberty [56]. Despite our finding lower levels of TIQ in KS, in line with previous studies [6], 47,XXY individuals were not, on average, intellectually disabled. However, both verbal and performance IQ were significantly lower than in HC. Even if the majority of studies have reported only VIQ defi-
10 10 Fisher et al. cits in the youngest KS population, significantly lower levels of both VIQ and PIQ have been observed in adulthood, confirming our findings [6]. Some limitations of this study have to be considered. First, the sample size is quite small and the possibility of type II errors should be considered. Second, our findings refer to KS patients seeking treatment and cannot be generalized to the whole population with this condition. Third, KS included in the present study were all on testosterone replacement therapy, which may theoretically contribute in paraphilic interest expression. Fourth, even though all the KS were testosterone-treated since at least 6 months, we cannot exclude an influence of previous hypogonadism on behavior. Given that one of the most important clinical features of KS is a testosterone deficiency starting at midpuberty, an ideal control group would have been a clinical comparison group, as hypogonadal men with normal karyotypes with an exordium of hypogonadism during adolescence (e.g., pituitary tumor or an inflammatory process within the testis with an exordium at midpuberty). Fifth, the control group is not representative of the general population; for example, these men showed a higher than expected IQ, which could be due to the limited sample size. Sixth, data regarding the socioeconomic status were not available. Seventh, no standard measures were adopted for the assessment of obsessive symptoms. Eighth, some of the adopted measures were self-reported. Finally, normative Italian score values of AQ and RME, as well as a validated Italian version of SAST and IIEF are not available. Conclusions In conclusion, our study reports, for the first time, a higher risk in a Klinefelter population to develop hypersexuality, paraphilic behaviors, and GD, which were mediated by O-C and autistic traits. Based on these results, it is important for clinicians to carefully evaluate (and eventually treat) obsessional thoughts and symptoms when hypersexuality and GD are suspected in KS. Acknowledgment We acknowledge the following: Roberta Ribali, MD (ribaliroberta@gmail.com), Urology Unit, IRCCS, Humanitas Research Hospital, Rozzano (MI), Italy; and Federica Pinna, MD (ribaliroberta@gmail.com), Clinica Psichiatrica dell Università di Cagliari, Italy. Corresponding Author: Mario Maggi, MD, PhD, Department of Clinical Physiopathology, University of Florence, Andrology Unit, Florence, Italy. Tel: ; Fax: ; m.maggi@ dfc.unifi.it Statement of Authorship Category 1 (a) Conception and Design Alessandra D. Fisher; Helen Casale; Giovanni Castellini; Mario Maggi; Elisa Bandini (b) Acquisition of Data Beatrice Campone; Naika Ferruccio; Valentina Boddi; Elisa Maseroli; Alessandro Oppo; Giancarlo Balercia; Alessandro Pizzocaro (c) Analysis and Interpretation of Data Alessandra D. Fisher; Giovanni Castellini; Mario Maggi; Helen Casale; Elisa Bandini; Valdo Ricca; Egidia Fanni Category 2 (a) Drafting the Article Alessandra D. Fisher; Giovanni Castellini; Mario Maggi; Valdo Ricca; Valentina Boddi; Elisa Maseroli; Alessandro Oppo; Giancarlo Balercia; Alessandro Pizzocaro (b) Revising It for Intellectual Content Alessandra D. Fisher; Giovanni Castellini; Valdo Ricca; Davide Dèttore; Mario Maggi; Beatrice Campone; Naika Ferruccio Category 3 (a) Final Approval of the Completed Article Alessandra D. Fisher; Giovanni Castellini; Mario Maggi; Valdo Ricca; Elisa Maseroli; Valentina Boddi; Beatrice Campone; Naika Ferruccio; Davide Dèttore References 1 Lee PA, Houk CP, Ahmed SF, Hughes IA, International Consensus Conference on Intersex organized by the Lawson Wilkins Pediatric Endocrine Society and the European Society for Paediatric Endocrinology. Consensus statement on management of intersex disorders. International Consensus Conference on Intersex. Pediatrics 2006;118:e Lanfranco F, Kamischke A, Zitzman M, Nieschag E. Klinefelter s syndrome. Lancet 2004;364: Achermann JC, Hughes IA. Disorders of sex development. In: Kronenberg HM, Melmed S, Polonsky JS, Larsen PR XI, eds. Williams textbook of endocrinology. Vol. 22. Philadelphia: Saunders Elsevier.; 2008: Aksglaede L, Skakkebaek NE, Almstrup K, Juul A. Clinical and biological parameters in 166 boys, adolescents and adults with nonmosaic Klinefelter syndrome: A Copenhagen experience. Acta Paediatr 2011;100: Klinefelter HF, Reifenstein EC, Albright F. Syndrome characterized by gynecomastia, aspermatogenesis without
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