|Year : 2015 | Volume
| Issue : 3 | Page : 113-118
Autistic trait, empathy, and attention-deficit/hyperactivity symptoms in women with idiopathic hirsutism
Ayhan Bilgic1, Özlem Bilgiç2, Sabri Hergüner1, Hilmi Cevdet Altınyazar2
1 Department of Child and Adolescent Psychiatry, Necmettin Erbakan University, Meram School of Medicine, Konya, Turkey
2 Department of Dermatology, Selcuk University, School of Medicine, Konya, Turkey
|Date of Web Publication||19-Oct-2015|
Department of Child and Adolescent Psychiatry, Meram Faculty of Medicine, Necmettin Erbakan University, 42090 Meram, Konya
Source of Support: None, Conflict of Interest: None
| Abstract|| |
Aim: Many psychiatric disorders, including attention-deficit/hyperactivity disorder (ADHD), disruptive behavioral disorders, autism spectrum disorders, and some psychiatric characteristics, such as poor empathizing, are regarded to be related to elevated levels of androgens or androgen sensitivity. Thus, numerous studies have investigated the potential association between androgen-related physical diseases and these psychiatric conditions. Idiopathic hirsutism (IH) is a disease characterized by an increased sensitivity of the pilosebaceous unit to circulating androgens in women. The purpose of this study was to examine whether IH has a relationship with androgen-related psychiatric conditions. Materials and Methods: Totally 37 females with IH and 33 healthy female controls were included in this study. Childhood and present ADHD symptoms of the participants were assessed using the Wender Utah Rating Scale (WURS) and the Adult ADHD Self-Report Scale, respectively. The Autism-spectrum quotient and the interpersonal reactivity index were used to assess autistic traits and different aspects of empathy. Hirsutism severity was measured using the Ferriman–Gallwey scoring system. Results: No significant difference was found between the patients and controls on psychiatric questionnaire scores, except for a trend for subjects with IH to show higher levels of the school-associated problems than controls according to WURS. The severity of hirsutism was strongly correlated with the WURS irritability and behavioral problems/impulsivity subscores and WURS total score, and moderately correlated with the WURS attentional deficit subscore. Conclusions: This study provides preliminary evidence that common etiological factors may be involved in both the severity of IH, ADHD, and coexisting disruptive behavioral problems.
Keywords: Autism, attention deficit hyperactivity disorder, androgen, empathy, hirsutism
|How to cite this article:|
Bilgic A, Bilgiç &, Hergüner S, Altınyazar HC. Autistic trait, empathy, and attention-deficit/hyperactivity symptoms in women with idiopathic hirsutism. Int J Trichol 2015;7:113-8
|How to cite this URL:|
Bilgic A, Bilgiç &, Hergüner S, Altınyazar HC. Autistic trait, empathy, and attention-deficit/hyperactivity symptoms in women with idiopathic hirsutism. Int J Trichol [serial online] 2015 [cited 2020 Sep 23];7:113-8. Available from: http://www.ijtrichology.com/text.asp?2015/7/3/113/167458
| Introduction|| |
Idiopathic hirsutism (IH) is defined as the presence of excessive terminal hair in androgen-dependent areas of a woman's body in conjunction with normal ovulatory function and normal serum androgen levels. The etiology of IH is still not clear. However, an increased sensitivity of the pilosebaceous unit to circulating androgens, due to increased peripheral 5alpha-reductase enzyme activity, and abnormalities of androgen receptor gene polymorphisms have been postulated to explain the pathogenesis of this disorder., Because they share same risk factors, it can be assumed that the rates of other androgen-related disorders are elevated in women with IH. However, few studies have investigated the comorbid conditions of IH.,
Various personality, cognitive, and behavioral traits show sexual dimorphism that are thought to be influenced by androgen exposure that begins prenatally.,, Accordingly, higher androgen levels or androgen sensitivity during early development has powerful programming influences on the brain, and as a consequence, has enduring effects on later behavior.,, Attention deficit hyperactivity disorder (ADHD), disruptive behavioral disorders (DBD); (e.g. oppositional defiant disorder and conduct disorder), and autism spectrum disorders (ASD) are among the neurodevelopmental conditions that occur more frequently in males as compared to females. Some studies have suggested that androgen exposure may play a role in the development of these disorders or their subclinical symptoms., Studies also point to the role of androgens in the development of empathy and pro-social behaviors with the observation that there are lower empathy levels in males than in females. There is also a negative correlation between fetal testosterone levels and empathizing as well as reduced empathetic behaviors in women following testosterone administration.
No studies have specifically investigated the relationship between IH and androgen-related psychiatric variables. However, a study conducted by Ingudomnukul et al. showed that significantly more women with ASD reported hirsutism compared to healthy controls. Furthermore, polycystic ovary syndrome (PCOS) is the most common cause of hirsutism, and recent data provide preliminary evidence that daughters of mothers affected by hyperandrogenic PCOS seem to have a higher risk for autistic traits and lower empathy levels. Although serum androgen levels of patients with IH are within the normal range, the increased androgen sensitivity of these patients may be related to the more prominent androgen-related psychiatric problems.
The objectives of this study were to assess ADHD and DBD symptoms, autistic traits, and empathy in women with IH. We also examined the association between these psychiatric variables and the severity of hirsutism in these patients.
| Materials and Methods|| |
The study sample consisted of patients (aged 18–40 years) with IH, who consecutively applied to the dermatology outpatient clinic at a university hospital in Turkey. Inclusion criteria were: Between 18 and 40 years of age and a diagnosis of IH with an estimated modified FerrimanGallwey (mFG) score of eight or more., Exclusion criteria were: The presence of PCOS, hormonal medication in the six months prior to the initiation of the study, thyroid disorders, diabetes or other endocrinopathies, a significant cognitive problem (enough to impede participation in the study), and a low educational level (less than five years of education). Overall, 69 patients were approached, but 32 patients were disqualified from this study based on the exclusion criteria. The sample finally comprised of 37 patients with IH. The control group consisted of 33 healthy women from the local community who were matched for educational level and had an estimated mFG score of two or under. Other exclusion and inclusion criteria for the control group were similar to the patient group.
All the patients with IH had regular menstrual cycles and a normal hormonal profile including testosterone, dehydroepiandrosterone, luteinizing hormone, follicle stimulating hormone, and thyroid stimulating hormone.
This study was approved by the Ethical Committee of the local university. All participants were given a patient information sheet that outlined the research protocol, and they all provided their written informed consent. Oral assent was also obtained from all subjects. Initially, all patients were assessed by an experienced dermatologist, they then completed the psychiatric questionnaires.
Modified Ferriman–Gallwey scale
The FG scale is a widely used scoring system for determining androgen-dependent hair growth in women. It is a visual method to determine the degree of hirsutism and was originally described by Ferriman and Gallwey, and further modified by Hatch et al. Nine body areas are scored from 0 to 4 (with 4 being extensive terminal hair growth), and the scores in each area are summed for a total hair growth score. The maximum score is 36 and a total score from 8 or higher are generally considered to represent hirsutism. A single examiner performed the scoring assessment on each patient.
The Wender Utah rating scale
The Wender Utah rating scale (WURS) was developed to evaluate retrospectively the symptoms and findings of ADHD and co-existing behavioral problems during childhood., It is a self-report measure with Likert-type 25-item scales including choices from 0 to 4 (0 = None, 4 = Severe). It includes subscales for irritability, depression, school problems, behavioral problems/impulsivity, and attentional deficits that all provide a total score.
The adult attention deficit hyperactivity disorder self-report scale
This instrument was used to assess current ADHD symptoms.,, The Adult ADHD Self-Report Scale (ASRS) is an 18-item self-report inventory where each item is rated on a 5-point Likert scale ranging from "never" to "very often." It consists of 18-item that contain inattention and hyperactivity subscales, and a total score.
The Autism-spectrum quotient
The Autism-spectrum quotient (AQ) is a self-assessment screening instrument for measuring the degree to which an individual of normal intelligence shows autistic traits. It has a 50-item questionnaire probing sub-clinical autistic traits and
organized into 5 domains: Social skills, attention switching, attention to detail, communication, and imagination. Each item is scored with a "0" (non-ASD-like) or a "1" (ASD-like) according to whether the response was "Agree" or "Disagree" to each statement. The higher the score on the AQ, the more autistic traits the individual has. A reliability study using the Turkish version was conducted by Köse.
The interpersonal reactivity index
The interpersonal reactivity index (IRI) is a 5-point Likert-type instrument with 28-item and with four separate subscales evaluating different dimensions of empathy. The "empathic concern" and "personal distress" subscales refer to the two affective empathy dimensions. The "empathic concern" measures a respondent's other-oriented feelings of compassion, warmth, and concerns for unfortunate others. The "personal distress" subscale measures the respondent's tendency to experience distress arising from observing another person's suffering. The subscale of "perspective taking" addresses one's tendency to take another's point-of-view. The "fantasy" subscale measures the tendency to identify with characters in fictional situations, such as movies and novels. Generally, an overall IRI score is calculated as an index of the general capacity to empathize with others. The reliability of the Turkish version of the IRI was evaluated by Engeler in a group of university students.
Data were analyzed using SPSS 21.0 statistical software (Chicago, IL, USA). Descriptive statistics regarding patients' FG scores were calculated. When the normality of the distribution of variables was acceptable, the Student's t-test, or in other cases, the Mann–Whitney U test, were used to analyze differences between groups. The Pearson or Spearman correlation coefficient was calculated to examine the relationship between psychological test scores and FG scores. The significance level was set at 0.05 (two-tailed).
| Results|| |
The mean age did not differ significantly between patient (22.05 ± 3.46 years) and control (23.47 ± 4.43 years) groups (z = −1.33, P = 0.184). The educational level of the participants was also similar in the patients (13.19 ± 3.09 years) and controls (13.75 ± 2.50 years) (z = −0.54, P = 0.590). The mean FG score was 12.00 ± 4.51 (range: 8 to 32) in the patient group.
[Table 1] presents scores on the various scales for patients with IH and controls. The analyzes showed that there were no significant differences among the patient and control groups. However, there was a trend for subjects with IH to show higher levels than controls in the "school problems" factor of the WURS.
|Table 1: Comparisons of psychiatric test scores in clinical and control samples|
Click here to view
Correlations between the severity of hirsutism and psychiatric test scores were evaluated in the patient group. FG scores were strongly correlated with the "attentional deficit" (r = 0.50, P = 0.002) and "behavioral problems/impulsivity" (rs = 0.49, P = 0.002) factors and the total score (r = 0.43, P = 0.009), and moderately correlated with "irritability" (r = 0.33, P = 0.047) factor of the WURS. However, FG scores did not show any significant relationship with the ASRS, AQ, and IRI scores.
| Discussion|| |
This study tested the hypothesis that psychiatric variables that are considered related to androgen exposure, such as ADHD and coexisting behavioral symptoms, autistic traits, and poor empathizing, would show increases in women with IH compared to healthy controls. In addition, we tested to see if these variables would have a relationship with the severity of hirsutism. Contrary to our expectations, the study did not show significant differences among the patient and control groups with respect to psychiatric variables. However, our findings did provide preliminary evidence for a positive relationship between the severity of hirsutism and childhood ADHD and coexisting behavioral symptoms in these patients. A similar relationship was not detected for current ADHD symptoms, autistic traits, and empathizing.
A growing body of research suggests that androgen exposure is related to ADHD and behavioral problems. Gobrogge et al. studied children with ADHD and found fetal androgen exposure, indirectly measured by the second to fourth finger length digit ratio, was associated most strongly with symptoms of inattention as well as hyperactive-impulsive and oppositional-defiant symptoms. Similarly, a recent study by Liu et al. reported that masculinized (i.e., low) finger length ratios are related to attention deficits and aggression in fifth-grade school children. In addition to prenatal androgen exposure, androgen levels in later in life have also shown a relationship with behavioral problems. Wang et al. detected higher salivary levels of dehydroepiandrosterone in children with ADHD compared to controls. There was also an association between salivary testosterone levels in healthy women and reactive aggression, a form of aggression that occurs in response to provocation. In the present study, although all of the mean current and childhood ADHD subscale scores of patients were higher than the controls, they did not reach statistical significance. However, there were significant relationships between the severity of hirsutism and childhood attentional deficit, irritability, and behavioral problems/impulsivity symptoms. These findings seem to be consistent with previous reports regarding an ADHD and androgen relationship, and support the idea that IH, ADHD, and co-existing behavioral problems may share common etiological mechanisms.
The shorter alleles of CAG polymorphisms of the androgen receptor gene cause increased gene expression. Thus, this polymorphism is considered to be related with higher sensitivity to similar levels of circulating androgens. In a previous study, an association between shorter CAG allels and ADHD, conduct disorder and oppositional defiant disorder was reported. Furthermore, though there was a controversial result, a relationship between CAG repeat polymorphisms and hirsutism was also found., Within this context, one could propose the relationship between childhood ADHD scores and hirsutism severity may arise from having shorter CAG repeats in the androgen receptor gene. However, data are very limited, and this hypothesis definitely needs to be validated.
Because ASD is relatively rare, and autistic traits are normally distributed throughout the population, studies have usually evaluated whether patients with androgen-related conditions show increased autistic traits. Knickmeyer et al. observed that females with congenital adrenal hyperplasia, which causes higher intrauterine testosterone levels, had higher autistic traits than controls. Whitehouse et al. showed that the predictor effect of autistic-like traits in childhood for a later menarche age. In line with these findings, a recent study showed a higher risk for autistic traits in daughters of mothers with hyperandrogenic PCOS. However agreement is not universal, a longitudinal pregnancy-cohort study reported no association between perinatal testosterone exposure and autistic-like traits in the general population. Our finding of no relationship between autistic traits and IH can be considered consistent with the results of this previous study.
While empathy may be influenced by psychosocial experiences, it was suggested that prenatal biology also plays an important role in the development of empathy, mediated by androgen effects in the brain. Chapman et al. observed negative correlations between fetal testosterone levels during the second trimester of pregnancy and empathizing in school-age children. A double-blind placebo-controlled study has also suggested a negative impact of androgens on empathy by showing decreased facial mimicry, which is an index of empathy, in women who received a single sublingual administration of testosterone. We hypothesized that, though circulating androgen levels are not elevated in patients with IH, an increased androgen sensitivity may be related to poor empathizing. However, our findings show no relationship among empathy and IH.
The results of our study should be interpreted in light of its limitations. First, the cross-sectional nature of our study means that causality cannot be established. Second, studies that tested the hypothesis that some of the cognitive and behavioral traits is associated with androgen exposure usually had more than fifty patients.,,, Therefore, our small sample size might not allow us to identify some of the group variances. Finally, the self-reported nature of the study is also a concern, because individuals with social cognitive defilcts may have an impaired accuracy in self-awareness.
| Conclusion|| |
This study shows that the severity of hirsutism is related to childhood ADHD and co-existing behavioral symptoms in women with IH. However, no relationship was detected among IH and current ADHD symptoms, autistic traits, and empathizing. These findings suggest that IH, ADHD, and DBD may share common risk factors. Our study will be followed by further studies with larger sample sizes to better identify the relationships between IH and androgen-related psychiatric variables.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Serafini P, Lobo RA. Increased 5 alpha-reductase activity in idiopathic hirsutism. Fertil Steril 1985;43:74-8.
Azziz R, Carmina E, Sawaya ME. Idiopathic hirsutism. Endocr Rev 2000;21:347-62.
Abdel Fattah NS, Darwish YW. Is there a role for insulin resistance in nonobese patients with idiopathic hirsutism? Br J Dermatol 2009;160:1011-5.
Sadat Hosseini M, Ramezani Tehrani F, Azizi F. The lack of association between idiopathic hirsutism and metabolic disturbances: Iranian PCOS Prevalence Study. Gynecol Endocrinol 2013;29:821-5.
Collaer ML, Hines M. Human behavioral sex differences: A role for gonadal hormones during early development? Psychol Bull 1995;118:55-107.
Kimura D. Sex, sexual orientation and sex hormones influence human cognitive function. Curr Opin Neurobiol 1996;6:259-63.
Williams CL, Meck WH. The organizational effects of gonadal steroids on sexually dimorphic spatial ability. Psychoneuroendocrinology 1991;16:155-76.
de Bruin EI, Verheij F, Wiegman T, Ferdinand RF. Differences in finger length ratio between males with autism, pervasive developmental disorder-not otherwise specified, ADHD, and anxiety disorders. Dev Med Child Neurol 2006;48:962-5.
Baron-Cohen S, Knickmeyer RC, Belmonte MK. Sex differences in the brain: Implications for explaining autism. Science 2005;310:819-23.
Chapman E, Baron-Cohen S, Auyeung B, Knickmeyer R, Taylor K, Hackett G. Fetal testosterone and empathy: Evidence from the empathy quotient (EQ) and the "reading the mind in the eyes" test. Soc Neurosci 2006;1:135-48.
Hermans EJ, Putman P, van Honk J. Testosterone administration reduces empathetic behavior: A facial mimicry study. Psychoneuroendocrinology 2006;31:859-66.
Ingudomnukul E, Baron-Cohen S, Wheelwright S, Knickmeyer R. Elevated rates of testosterone-related disorders in women with autism spectrum conditions. Horm Behav 2007;51:597-604.
Palomba S, Marotta R, Di Cello A, Russo T, Falbo A, Orio F, et al.
Pervasive developmental disorders in children of hyperandrogenic women with polycystic ovary syndrome: A longitudinal case-control study. Clin Endocrinol (Oxf) 2012;77:898-904.
Hatch R, Rosenfield RL, Kim MH, Tredway D. Hirsutism: Implications, etiology, and management. Am J Obstet Gynecol 1981;140:815-30.
Yildiz BO, Bolour S, Woods K, Moore A, Azziz R. Visually scoring hirsutism. Hum Reprod Update 2010;16:51-64.
Ferriman D, Gallwey JD. Clinical assessment of body hair growth in women. J Clin Endocrinol Metab 1961;21:1440-7.
Ward MF, Wender PH, Reimherr FW. The Wender Utah Rating Scale: An aid in the retrospective diagnosis of childhood attention deficit hyperactivity disorder. Am J Psychiatry 1993;150:885-90.
Oncü B, Olmez S, Sentürk V. Validity and reliability of the Turkish version of the Wender Utah Rating Scale for attention-deficit/hyperactivity disorder in adults. Turk Psikiyatri Derg 2005;16:252-9.
Adler LA, Spencer T, Faraone SV, Kessler RC, Howes MJ, Biederman J, et al.
Validity of pilot Adult ADHD Self- Report Scale (ASRS) to Rate Adult ADHD symptoms. Ann Clin Psychiatry 2006;18:145-8.
Kessler RC, Adler L, Ames M, Demler O, Faraone S, Hiripi E, et al.
The World Health Organization Adult ADHD Self-Report Scale (ASRS): A short screening scale for use in the general population. Psychol Med 2005;35:245-56.
Dogan SÖ, Saraçoglu GV, Küçükgöncü S. Validity and reliability of the Turkish version of the adult ADHD self-report scale (ASRS-v1.1). Anadolu Psikiyatri Derg 2009;10:77-87.
Baron-Cohen S, Wheelwright S, Skinner R, Martin J, Clubley E. The autism-spectrum quotient (AQ): Evidence from Asperger syndrome/high-functioning autism, males and females, scientists and mathematicians. J Autism Dev Disord 2001;31:5-17.
Köse S, Bora E, Erermis¸ S, Aydın C. Psychometric features of Turkish version of autism-spectrum quotient. Anadolu Psikiyatri Dergisi 2010;11:253-60. [in Turkish].
Davis MH. Measuring individual differences in empathy: Evidence for a multidimensional approach. J Pers Soc Psychol 1983;44:113-26.
Engeler A, Yargiç LI. Interpersonal reactivity index: Measurement of empathy multidimensionaly. New Symp J 2007;45:119-27.
Gobrogge KL, Breedlove SM, Klump KL. Genetic and environmental influences on 2D: 4D finger length ratios: A study of monozygotic and dizygotic male and female twins. Arch Sex Behav 2008;37:112-8.
Liu J, Portnoy J, Raine A. Association between a marker for prenatal testosterone exposure and externalizing behavior problems in children. Dev Psychopathol 2012;24:771-82.
Wang LJ, Huang YS, Hsiao CC, Chiang YL, Wu CC, Shang ZY, et al.
Salivary dehydroepiandrosterone, but not cortisol, is associated with attention deficit hyperactivity disorder. World J Biol Psychiatry 2011;12:99-109.
Denson TF, Mehta PH, Ho Tan D. Endogenous testosterone and cortisol jointly influence reactive aggression in women. Psychoneuroendocrinology 2013;38:416-24.
Lin LH, Baracat MC, Maciel GA, Soares JM Jr, Baracat EC. Androgen receptor gene polymorphism and polycystic ovary syndrome. Int J Gynaecol Obstet 2013;120:115-8.
Comings DE, Chen C, Wu S, Muhleman D. Association of the androgen receptor gene (AR) with ADHD and conduct disorder. Neuroreport 1999;10:1589-92.
Calvo RM, Asunción M, Sancho J, San Millán JL, Escobar-Morreale HF. The role of the CAG repeat polymorphism in the androgen receptor gene and of skewed X-chromosome inactivation, in the pathogenesis of hirsutism. J Clin Endocrinol Metab 2000;85:1735-40.
Sawaya ME, Shalita AR. Androgen receptor polymorphisms (CAG repeat lengths) in androgenetic alopecia, hirsutism, and acne. J Cutan Med Surg 1998;3:9-15.
Van Nieuwerburgh F, Stoop D, Cabri P, Dhont M, Deforce D, De Sutter P. Shorter CAG repeats in the androgen receptor gene may enhance hyperandrogenicity in polycystic ovary syndrome. Gynecol Endocrinol 2008;24:669-73.
Knickmeyer R, Baron-Cohen S, Fane BA, Wheelwright S, Mathews GA, Conway GS, et al.
Androgens and autistic traits: A study of individuals with congenital adrenal hyperplasia. Horm Behav 2006;50:148-53.
Whitehouse AJ, Maybery MT, Hickey M, Sloboda DM. Brief report: Autistic-like traits in childhood predict later age at menarche in girls. J Autism Dev Disord 2011;41:1125-30.
Whitehouse AJ, Mattes E, Maybery MT, Dissanayake C, Sawyer M, Jones RM, et al.
Perinatal testosterone exposure and autistic-like traits in the general population: A longitudinal pregnancy-cohort study. J Neurodev Disord 2012;4:25.
Knickmeyer R, Baron-Cohen S, Raggatt P, Taylor K, Hackett G. Fetal testosterone and empathy. Horm Behav 2006;49:282-92.