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J.Neurol.Sci.[Turk] Journal of Neurological Sciences [Turkish] 30:(4)# 38; 693-701, 2013 http://www.jns.dergisi.org/text.php3?id=717 Research Article The Evaluation of Sexual Functions and Sex Hormones in Male and Female Epilepsy Patients Taking Valproic Acid and Carbamazepine Monotherapy Abidin ERDAL, Gülnihal KUTLU, Yasemin Biçer GÖMCELI, Levent Ertuğrul İNAN T.C.S.B. Ankara Eğitim ve Araştırma Hastanesi, Nöroloji Kliniği, Ankara, Türkiye Summary Objective: In patients with epilepsy, sexual dysfunction is seen at an higher incidence than in patients with other chronic neurologic disorders. In this study, we examined sex hormone levels and sexual dysfunction in patients with epilepsy who took carbamazepine (CBZ) and valproic acid (VPA) monotheraphy. Method: Female and male patients in reproductive period who had sexual partners within the last three months referring to Neurology Department Epilepsy Clinic of Ankara Hospital between December 2009 – November 2010 and who have been followed for at least one year with CBZ or VPA monotherapy were included in the study. There were 35 patients in the study; 18 patients who took VPA and 17 patients who took CBZ. These patients' medical history, epilepsy history, sex hormone levels, drug blood levels, Hamilton Depression Rating Scale (HAM-D), Hamilton Anxiety Rating Scale (HAM-A) and Arizona Sexual Experience Scale (ASEX) levels were examined. Results: The rate of sexual dysfunction was found statistically significant to be higher in women patients with epilepsy than men irrespective of drugs, anxiety and depression. Dehydroepiandrostenedionesulphate (DHEAS) and progesterone (PG) levels were found statistically significant to be higher in male patients who took VPA. The number of pregnancies was statistically significant lower in female patients using VPA and it was associated with VPA induced hyperandrogenism. Conclusion: Sexual dysfunction and alterations in sex hormones may occur frequently in epilepsy patients. The most significant finding of our study was high rates of sexual dysfunction in women. Further studies are necessary to support our findings. Key words: Sexual Antiepileptic drugs dysfunction, Dehydroepiandrostenedionesulphate, Progesterone, Valproik Asit ve Karbamazepin Monoterapili Kadın ve Erkek Epilepsi Hastalarında Cinsel Fonksiyonların ve Seks Hormonlarının Değerlendirilmesi Özet Amaç: Epilepsi hastalarında, diğer kronik nörolojik hastalığı olanlara göre daha yüksek bir insidansta cinsel disfonksiyon görülmektedir. Bu çalışmada, karbamazepin (CBZ) ve valproik asit (VPA) monoterapisi alan epilepsi hastalarında seks hormon seviyelerini ve seksüel disfonksiyonu araştırdık. Yöntem: Çalışmaya S. B. Ankara Eğitim ve Araştırma Hastane'si Nöroloji Kliniği epilepsi polikliniğine Aralık 2009 – Kasım 2010 tarihleri arasında başvuran en az bir yıldır takip edilmekte olan CBZ ve VPA monoterapisi alan reprodüktif çağdaki, son üç ay içinde cinsel partneri olan kadın ve erkek hastalar alınmıştır. VPA kullanan 18 hasta, CBZ kullanan 17 hasta olmak üzere toplam 35 hasta çalışmamızda yer almıştır. Bu hastaların medikal 693 J.Neurol.Sci.[Turk] özgeçmişleri, epilepsi özgeçmişleri, seks hormon seviyeleri, ilaç kan düzeyleri, Hamilton Depresyonu Derecelendirme Ölçeği (HAM-D), Hamilton Anksiye Değerlendirme Ölçeği (HAM-A) ve Arizona Cinsel Yaşam Ölçeği (ASEX) değerleri incelenmiştir. Bulgular: Epilepsili kadın hastalarda, epilepsili erkek hastalara göre seksüel disfonksiyon oranı ilaçlar, anksiyete ve depresyondan bağımsız, istatistiksel olarak anlamlı yüksek bulunmuştur. Çalışmamızda VPA kullanan erkek hastalarda, dihidroksiepiandrostenedionsülfat (DHEAS) ve progesteron (PG) seviyesi istatistiksel olarak anlamlı yüksek tespit edilmiştir. VPA kullanan kadın hastalarda gebelik sayısı istatistiksel olarak anlamlı düşük bulunmuştur ve bu da VPA' nın oluşturduğu hiperandrojenizmle ilişkili olabilir. Sonuç: Epilepsi hastalarında, seksüel disfonksiyon ve seks hormon seviyelerinde değişiklikler sık oluşabilir. Çalışmamızın en önemli bulgusu kadınlarda cinsel disfonksiyon oranının yüksek olmasıdır. Bizim bulgularımızı desteklemek için daha fazla çalışma gereklidir. Anahtar Kelimeler: Seksüel disfonksiyon, dihidroepiandrostenedionsülfat, progesteron, antiepileptik ilaçlar with the ethical standards laid down in the 2008 revision of Declaration of Helsinki. Female and male patients in reproductive period who had sexual partners within the last three months referring to Neurology Department Epilepsy Clinic of Ankara Hospital between December 2009 – November 2010 and who have been followed for at least one year with CBZ or VPA monotherapy were included in the study. Informed consent was obtained from the patients. Pregnant patients and patients with endocrinopathies were excluded from the study. INTRODUCTION Sexual dysfunction occurs more commonly in men and women with epilepsy compared to normal individuals at the same ages.(16,18) The etiology of sexual dysfunction in epilepsy is multifactorial, i.e. endocrinological, neurological, psychological and social factors all play role.(16) The impact of epilepsy on reproductive system was related to complex partial seizures, particularly temporal lobe seizures. Complex partial seizures are associated with hippocampus and amygadala atrophy and it is known that these structures are involved with Sexual reproductive behavior.(20) dysfunction in epilepsy may also be iatrogenic.(4,10) In addition, many psychogenic factors (such as anxiety and depression) may also affect sexuality.(6,25) The aim of the present study was to investigate and compare the prevalence of anxiety, depression, sexual dysfunction and sexuel hormone levels in male and female epilepsy patients who took CBZ and VPA. Demographic data of all patients, medical history, the age of the onset of epilepsy, type and duration of epilepsy, type and frequency of seizures, the age of onset of epilepsy treatment, the dose of antiepileptic drug (AED) used, its duration and blood level, family history of epilepsy, contraceptive methods used, the number of pregnancies and history of menstruation were recorded. In all patients, drug blood level, thyroid stimulating hormone (TSH), free T3, free T4, prolactin (PRL), total testosterone (TT), free testosterone (FT), estradiol (E2), progesterone (PG), luteinizing hormone (LH), follicle stimulating hormone (FSH), human chorionic gonadotropin (HCG), serum biochemistry and complete blood count MATERIAL AND METHODS This study received prior approval from the ethics committee of the Ministry of Health, Ankara Research and Training Hospital and was performed in accordance 694 J.Neurol.Sci.[Turk] was examined. In addition, in male patients DHEAS levels were also measured. In the measurement of hormone levels in patients, blood was drawn from male patients in morning of any day of the month while it was drawn within the first three days of menstruation period in female patients. evaluation of data, descriptive statistical methods (mean, standard deviation) and in the comparison of qualitative data, T test and chi-square test were used. Correlation between parameters was evaluated with Spearman correlation analysis. P value under 0.05 was considered significant. For psychological evaluation, Hamilton Depression Rating Scale (HAM-D) and Hamilton Anxiety Rating Scale (HAM-A) were used.(1,8,23-24) In order to evaluate sexual dysfunction, Arizona Sexual Experience Scale (ASEX), which is a Likert-type self rating scale with male and female forms was used. Likert distinguished between a scale proper, which emerges from collective responses to a set of items (usually eight or more), and the format in which responses are scored along a range.(3) ASEX evaluates sex drive, arousal, vaginal lubrication, penile erection, ability to reach orgasm, and satisfaction from orgasm. Scores at or over 11 are reported to indicate sexual dysfunction in Turkish reliability and validity study.(13,21) Overall 42 patients were included in the study and among them one woman using CBZ became pregnant before hormone analysis and another woman on VPA had high beta-HCG values and they were excluded from the study. Three patients on VPA (one male, two female) withdrew their consent and dropped out from the study. In addition, two women on CBZ were excluded as they could not undergo blood analysis in the first three days of menstruation. RESULTS Hence, overall 35 patients, 18 patients on VPA, and 17 patients on CBZ were included in evaluation. The distribution of drug groups according to epilepsy type and sex is shown in Table 1. Overall mean age was 32.63, mean age in CBZ group 34.82, and that in VPA group 30.56. Drug doses of male and female patients, mean duration of drug use and blood drug levels are shown in Table 2 and 3. Statistical methods Findings of the study were evaluated by SPSS (Statistical Package for Social Sciences) for Windows 17.0. In the Table 1. Distribution of drug groups according to type of epilepsy Type of Epilepsy CBZ VPA (mean age) n / (%) n / (%) 1 / (5,9) 9 / (50,0) 16 /( 94,1) 8 / (44.4) - 1 / (5,6) 17 / (100) 18 / (100) Primary (28.20±2,19) Partial (34,33±1,97) Unclassified (36) Overall (32,63±1,55) *percentages are given for lines 695 J.Neurol.Sci.[Turk] Tablo 2. Mean drug dose and duration and blood drug levels in male and female patients taking CBZ and VPA. CBZ taking♀and♂ (n=17) CBZ taking ♀ (n=8) CBZ taking ♂ (n=9) VPA taking♀and♂ (n=18) VPA taking ♀ (n=7) VPA taking ♂ (n=11) Blood drug level Drug dose Duration of use (mg/day) (month) 608,82±54,61 90,76±22,10 6,88±0,60 643,75±79,86 74,13±18,15 7,01±0,85 577,78±77,78 105,56±39,12 6,76±0,88 958,33±97,45 61,94±13,24 454,90±43,39 821,43±105,14 101,43±27,03 411,45±61,60 1045,45±142,30 36,82±6,84 482,56±59,95 (CBZ mg/L) (VPA µmol/L) Table 3. Mean hormone levels and sexual dysfunction according to drug groups in male and female patients. CBZ VPA (n=17) (n=18) Male (n=9) Female (n=8) Male (n=11) Female (n=7) Sexual Dysfunction (+) 3 8 8 6 Sexual Dysfunction (-) 6 - 3 1 10,23±1,13 9,16±0,91 10,46±1,66 18,08±4,15 TT (ng/dl) 459,39±49,50 40,44±4,85 525,62±55,92 45,06±8,27 FT (pg/ml) 13,13±1,24 1,59±0,28 16,46±1,40 1,83±0,20 E2 (pg/ml) 32,15±6,77 56,58±7,81 31,52±4,84 81,96±31,31 PG (ng/ml) 0,46±0,10 0,65±0,07 1,11±0,21 2,18±1,23 LH (IU/ml) 6,24±0,64 4,65±0,89 5,14±0,64 4,33±0,40 FSH (IU/ml) 5,70±1,06 8,60±1,57 4,40±1,30 5,43±0,98 DHEAS (µg/dl) 83,59±8,16 - 251,85±48,76 - PRL (ng/ml) 696 J.Neurol.Sci.[Turk] (ASEX ≥ 11) and in 28.6% (n=10), it was absent. Sexual dysfunction was found in 93.3% (n=14) of female patients, and in 55% of male patients (n=11), with a statistically significant difference (p<0.05). When comparison was made according to drug group, sexual dysfunction was present in 64.7% (n=11) of CBZ users and 77.8% of (n=14) VPA users. In CBZ group, in patients without sexual dysfunction, FT levels were statistically significant higher (p<0.05). Mean ASEX scores were statistically significant higher in female patients (p<0.05). Of male patients with sexual dysfunction, 8 was in VPA and the remaining 3 in CBZ group. Sexual dysfunction was detected in 8 women in CBZ and 6 women in VPA group with no statistically significant difference (p>0.05). In female patients mean HAM-D scale scores were 5.33±1.10 and HAM-A scores 4.53±0.66 and mean ASEX score was 15.47±1.05. In male patients, the corresponding scores were respectively 3.70±0.45; 2.90±0.40 and 10.70±0.76 (Figure 1). There was no statistically significant difference between male and female patients with regard to mean scores obtained with HAM-D and HAM-A scales (p>0.05). However, ASEX scores were statistically significant higher in female patients (p<0.05). In CBZ using female patients; as the duration of drug use was increased, FT values increased (p<0.05). As the drug dose increased, HAM-D scale values increased and when PRL values increased, ASEX scores decreased (p<0.05, p<0.05). In CBZ using male patients, as drug dose was increased FT values rose and as drug blood level increased PG values rose and as duration of drug use increased, TT values decreased (p<0.05). In VPA using female patients LH values decreased as VPA blood levels increased (p<0.05). In VPA using male patients, as the drug dose increased, FT and TT values rose and as duration of drug use was prolonged, DHEAS values fell (p<0.05). In addition, HAM-D scores increased in parallel to ASEX scores (p<0.05). Although there was no statistically significant difference between drug groups in terms of the number of living healthy children (p>0.05), the number of pregnancies was mean 3.75±0.6 in CBZ group and 1.57±0.6 in VPA group, with a statistically significant difference between groups (p<0.05). PRL, E2, PG levels were respectively 1.97, 1.44 and 3.35 fold higher in female patients in VPA group than those in CBZ group, but the difference was not statistically significant (p>0.05). PG ve DHEAS levels were statistically significant higher in male patients in VPA group than those in CBZ group (p<0.05). Although testesterone levels were within physiological value, patients on CBZ have slightly lower levels than those on VPA. In female and male patients examined separately; there was no statistically significant difference between CBZ and VPA groups in terms of five major global aspects of sexual dysfunction in ASEX: drive, arousal, penile erection/vaginal lubrication, ability to reach orgasm, and satisfaction from orgasm (p>0.05). According to ASEX, in 71.4% of (n=25) all patients sexual dysfunction was present 697 J.Neurol.Sci.[Turk] Figure 1: Mean HAM-D, HAM-A, ASEX scales' ratings comparison by gender lower quality of sexual life.(17) However, even though sexual dysfunction was found to be higher in female patients using CBZ, low number of cases makes interpretation of data more difficult. DISCUSSION The cause of sexual dysfunction is quite complex in both female and male epilepsy patients. AEDs used, epileptic seizures, underlying brain pathology, and psychiatric comorbidity may be considered among these causes.(12) AED give rise to sexual dysfunction by altering metabolism and phramacokinetics of sexual hormones as well as affecting GABAergic and seratonergic neuromodulatory systems as shown in animal studies.(12,22) Herzog stressed that enzyme inducing drugs induce aromatase enzyme, hence the transformation of testesteron to estradiol in the periphery via this enzyme is increased. Estradiol, in turn, increases sex hormonebinding globulin (SHBG) levels and has a negative feedback effect on LH. Herzog also stated that this mechanisms should also be borne in mind when evaluating hormonal changes during CBZ treatment.(5) As to women, enzyme inducing AED's decreases bioactivity of E2, testesteron and other sex steroids by increasing the synthesis SHBG and leads to hyperandrogenism in women with epilepsy.(7) In women who receive long term CBZ treatment, menstrual disorders may occur due to the decrease in bioactive E2.(7,15) In our study, when drug blood level increased in CBZ using patients, ASEX values increased as well. However, low number of patients was a limiting factor for statistical evaluation. In our study, it was found that in male patients using CBZ, FT values rose statistically In our study, no statistically significant difference was found between drug groups with respect to ASEX scores. Nevertheless, mean ASEX scores were found to be statistically significant higher in women than in men, which indicated that sexual dysfunction was experienced at a higher rate in female epilepsy patients than in male epilepsy patients. The causes of this difference may be that in Turkish society male patients have difficulty in expressing themselves regarding dysfunction.(2) Similarly, in the Turkish reliability and validity study of ASEX, higher ASEX scores were obtained by female patients than male patients.(21) In another study, female sex was found to be associated with 698 J.Neurol.Sci.[Turk] In our study, DHEAS level was found to be statistically significant higher in male patients in VPA group than those in CBZ group, which is compatible with the results reported in the literature. And we observed that DHEAS values decreased in male patients using VPA with the duration of use was prolonged. TT and FT levels are normal range of all groups. All of these findings suggest that there is no difference in ASEX scores was found between drug groups. Besides, PG level also was significantly higher in male patients in VPA group. Although PG level was found to be 3.35 fold higher in women patients in VPA group than those in CBZ group, this difference was not found to be statistically significant. In view of the literature, this finding may be interpreted as follows: epilepsy itself decreases pregnelolon and 17 hydroxypregnelolon levels or it increases progesteron levels, being helped by VPA in doing so.(11) significant as drug dose and duration of dose increased, which may be related to adaptation mechanisms. In addition, in male patients using CBZ, TT levels decreased with the duration of drug use. In males with epilepsy receiving VPA, DHEAS and androstenedion concentrations increase. DHEAS is the precursor of androgen in males. This results in increase in androgen load in males, which in turn helps the metabolization of DHEAS to GABAergic steroids.(7,19-20) In our study, although the difference between male and female patients using VPA in terms of duration of use was not statistically significant, duration of VPA use was 2.8 fold higher in women than that in men. However, we observed that DHEAS values decreased in male patients using VPA with the duration of use was prolonged. All of these findings suggest that various adaptation mechanisms may develop in the body as the duration of VPA and CBZ use increases. However, further studies on the issue are required. In patients using CBZ, HAM-D scores increase statistically significant especially with the increase in dose. However, when patients are evaluated individually, diagnosis of depression is not made according to HAM-D scale. This difference may be largely attributed to the fact that majority of patients in CBZ group has partial origin epilepsies. Patients who took high doses of CBZ may generally be considered to be more refractory. In various studies, the rate of sexual dysfunction was reported to vary between 30-60%.(12) Women are more susceptible to endocrinological effects of VPA. In young girls using VPA, hyperandrogenism including weight gain, hirsutism and android obesity occur, while in mature women, it leads to polycystic ovarian syndrome and hyperinsulinism. Menstrual disorders, particularly amenorrhea and oligomenorrhea are common. In women using VPA, sexual dysfunction is not uncommon. Decrease in libido and anorgasmia occur.(7) In our study, FSH and LH levels decreased statistically significant as VPA levels increased. One of the most striking results of the present study was that the rate of sexual dysfunction in women is quite high irrespective of depression and anxiety scores. Since our sample size is small, these findings need to be corroborated by comparative studies including control groups representing general population. Bioactive testesterone correlates with sexual function in men and women, and patients with epilepsy have less bioactive testesterone than others.(9-10,12,14) In our study ASEX values decreased as FT values rose, which emphasizes the importance of FT levels in sexual function in both men and women. Acknowledgment The authors thank Ministry of Health, Ankara Research and Training Hospital' s 699 J.Neurol.Sci.[Turk] biochemistry clinic for their help in blood hormone level analyses. 3. Conflict of interest None of the authors has any conflict of interest to disclose. We confirm that we have read the Journal's position on issues involved in ethical publication and affirm that this report is consistent with those guidelines. 4. 5. 6. Correspondence to: Abidin Erdal E-mail: [email protected] 7. 8. 9. Received by: 21 April 2013 Revised by: 20 October 2013 Accepted: 27 November 2013 10. The Online Journal of Neurological Sciences (Turkish) 1984-2013 This e-journal is run by Ege University Faculty of Medicine, Dept. of Neurological Surgery, Bornova, Izmir-35100TR as part of the Ege Neurological Surgery World Wide Web service. Comments and feedback: E-mail: [email protected] URL: http://www.jns.dergisi.org Journal of Neurological Sciences (Turkish) Abbr: J. Neurol. Sci.[Turk] ISSNe 1302-1664 11. 12. 13. 14. REFERENCES 15. 1. 2. Akdemir A, Örsel SD, Dağ İ, Türkçapar HM, İşcan N, Özbay H. Hamilton depresyon derecelendirme ölçeğinin geçerliliği, güvenilirliği ve klinikte kullanımı. Psikiyatri Psikoloji Psikofarmakoloji Dergisi 1996; 4: 251-259. Bayraktar Z, Atun A. Reasons of Turkish males with erectile dysfunction for not presenting to 16. 700 urology clinics. Türkiye Klinikleri Journal of Medical Sciences 2012; 32(1): 177-183. Carifio J, Rocco J.P. 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