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Early Intervention in Psychiatry 2014; ••: ••–••

doi:10.1111/eip.12194

Original Article Relationship between menarche and psychosis onset in women with first episode of psychosis Elena Rubio-Abadal,1 Judith Usall,1 Anna Barajas,2 Janina Carlson,1 Raquel Iniesta,1 Elena Huerta-Ramos,1 Iris Baños,1 Montserrat Dolz,3 Bernardo Sánchez,3 GENIPE Group* and Susana Ochoa1 Abstract 1

Research Unit, Parc Sanitari Sant Joan de Déu, Sant Boi de Llobregat, Barcelona. CIBERSAM. GTRDSM, 2Research Unit, Centre d’Higiene Mental Les Corts, Barcelona, and 3Psychiatry Department, Hospital Sant Joan de Déu, CIBERSAM, Barcelona, Spain Corresponding author: Dr Elena Rubio-Abadal, Parc Sanitari Sant Joan de Déu, Doctor Antoni Pujadas, 42, 08830 Sant Boi de Llobregat, Barcelona, Spain. Email: [email protected] *GENIPE Group is a multidisciplinary group of researchers: Araya S, Arranz B, Arteaga M, Asensio R, Autonell J, Baños I, Bañuelos M, Barajas A, Barceló M, Blanc M, Borrás M, Busquets E, Carlson J, Carral V, Castro M, Corbacho C, Coromina M, Cuevas J, Dachs I, Dolz M, Domenech MD, Elias M, Espezel I, Falo E, Fargas A, Foix A, Fusté M, Godrid M, Gómez D, González O, Granell L, Gumà L, Haro JM, Herrera S, Huerta-Ramos E, Lacasa F, Mas N, Martí L, Martínez R, Matalí J, Miñambres A, Miquel L, Muñoz D, Muñoz V, Nogueroles R, Ochoa S, Ortiz J, Pardo M, Planella M, Pelaez T, Peruzzi S, Rivero S, Rodriguez MJ, Rubio E, Sammut S, Sánchez M, Sánchez B, Serrano E, Solís C, Stephanotto C, Tabuenca P, Teba S, Torres A, Urbano D, Usall J, Vilaplana M, Villalta V.

Aim: The aim of this study was to explore the relationship between age at menarche and age at first episode of psychosis, as well as clinical severity and outcome, in a population of women with first-episode psychosis. Methods: Clinical and sociodemographical data, age at menarche and at first-episode psychosis, parental history of psychosis and cannabis-use habits were obtained from 42 subjects with a first episode of psychosis. Positive and Negative Syndrome Scale, Clinical Global Impression, Global Assessment Function, Disability Assessment Schedule, Wechsler Adult Intelligence Scale and Wechsler Intelligence Scale for Children, European Quality of Life, and Lewis and Murray Obstetric Complication Scales were administered.

Statistical analysis was performed by means of zero-order correlations and Mann–Whitney U and Kruskal–Wallis tests using SPSS version 17.0. Results: We found no significant correlation between age at menarche and age at first-episode psychosis, or with the clinical scores performed. We observed that subjects with earlier age at menarche had more parental history of psychosis. Conclusions: Our negative results do not support the theory of a possible protective role of oestrogen, which seems to be more complex than previously thought. We would suggest that further research is needed to investigate developmental influences of sex steroids on the onset of psychosis and potentially therapeutic benefits based upon oestrogen.

Key words: age of onset, cannabis, obstetric labour complication, oestrogen, outcome.

Received 22 December 2013; accepted 19 August 2014

INTRODUCTION The existence of gender differences in psychiatric illnesses, and especially in psychosis, has always been of particular interest. As early as 1909, Emil Kräpelin reported that women presented with psychotic illnesses (dementia praecox) later than men, according to their respective ages at first hospital admission. Since then, several research studies have © 2014 Wiley Publishing Asia Pty Ltd

been performed1–3 in order to find these purported gender differences in age at onset of psychosis and to attempt to clarify their causes. Through these studies, it has been confirmed that men show increased incident rates of psychosis between the ages of 20 and 25 years old, whereas women show a more moderate increase between the ages of 30 and 35, exhibiting a second (but lower) peak between the ages of 45 and 49.1 Other studies also found 1

Menarche and age at onset of psychosis lower incidence, later onset and better outcome of the illness in women, at least until the advent of menopause, compared with men.4,5 Various hypotheses have been formulated regarding this issue: one of them is the so-called ‘oestrogen hypothesis’ of schizophrenia, which posits that oestrogen in women who are vulnerable to presenting this illness has a neuroprotective effect,6 which has been shown to decrease or postpone the risk of psychosis among women. To this extent, life periods when oestrogen levels are lower, such as postpartum, menopause or peri-menstrual phases, are related to the beginning or relapse of psychosis and vice versa. This theory was reinforced on finding that, after menopause, women suffering from psychosis needed a higher dose of anti-psychotic medication, probably due to the decrease of the neuroleptic-enhancing property of oestrogen.6 Furthermore, average oestrogen levels in women with schizophrenia have been proven to be lower that than in healthy women.5 Animal research suggests that oestradiol might act as a protective modulator in schizophrenia by enhancing the vulnerability threshold for psychosis through the downward regulation of dopamine neurotransmission.7 According to this hypothesis, several studies have been carried out to prove that an early age for the start of puberty would correlate with a later age at first psychotic episode and with lower severity of psychotic symptoms. Non-conclusive and controversial results have been found. Cohen et al.8 and Galdós et al.9 reported a significant correlation between early puberty and later onset in schizophrenia. On the contrary, the results of similar studies performed by Hochman and Lewine10 and Ruiz et al.11 did not fully support these findings. Genetic predisposition, understood as the familial loading of psychosis, has also been described as a determining factor for age at onset of psychosis. Könnecke et al.12 suggested that this predisposition antagonizes the onset-delaying effect of oestrogen in schizophrenia. In this line of research, several studies have found no significant sex differences in age of onset in cases of familial schizophrenia,13,14 although in the absence of psychotic disorder in first-degree relatives, age of onset is again delayed among women, as the oestrogen protection theory suggests. Other factors that have been reported to bring forward the age of psychosis onset are the presence of obstetric complications and infections during pregnancy,15,16 substance abuse (especially the use of cannabis) and the disturbance of early neuromotor and cognitive development.17,18 Most of the previous research that has studied the interaction of age at onset and age at menarche has 2

dealt with medium- and long-term diagnosed and treated psychotic patients. In our study, only patients with first-episode psychosis were included, presuming that the age of onset of psychosis (first symptoms, first treatment and first hospital admission), age at menarche and other variables collected are less likely to be biased. In addition, the patients in our study had either not received any treatment or only for a short period of time before being recruited, which reduces the presence of possible confounding variables. Aims of the study The aim of this study is to explore the relationship between the age at menarche (as a measure of onset of puberty) and the age at first psychotic episode in a population of first-episode psychotic women. We also aim to correlate the age at menarche with the episode’s clinical severity and outcome. We hypothesized that women with early puberty should develop psychotic episodes later and present lower severity of psychotic symptoms, as well as a better outcome, than patients with later onset of puberty.

METHODS Patients included in this study were recruited as they attended the adult or child and adolescent mental health services at Parc Sanitari Sant Joan de Déu (both hospital and community services), in Barcelona and surrounding areas, from January 2006 until December 2011. The inclusion criteria were as follows: female aged between 10 and 65 years old with two or more psychotic symptoms (delusions, hallucinations, disorganized speech, catatonic or disorganized behaviour and negative symptoms) who attended our services for the first time with a duration of untreated psychosis of less than 1 year and with no more than 6 months of psychological or psychopharmacological treatment. The exclusion criteria were as follows: intellectual disability, previous brain injury or dementia. The present study has been approved by the Ethics Committee of Sant Joan de Déu Foundation (Barcelona) and it conforms to the provisions of the Declaration of Helsinki. Subjects Forty-seven subjects fulfilling inclusion criteria were finally recruited, although five of them, for © 2014 Wiley Publishing Asia Pty Ltd

E. Rubio-Abadal et al. TABLE 1. Age descriptive data (years, n = 42)

Age at inclusion in the study Age at menarche Age at first psychotic symptoms Age at first psychiatry contact Age at first hospital admission†

TABLE 2. Sample diagnoses (n = 42)

Mean

SD

Median

Range

Diagnosis group

19.81

6.142

17.00

14–38

12.24 19.26

1.100 6.332

12.00 17.00

10–15 12–38

19.43

6.236

17.00

12–38

Psychotic disorder NOS Schizophreniform disorder Schizophrenia, paranoid type Schizoaffective disorder Bipolar I disorder Drug-induced psychotic disorder Brief psychotic disorder

19.33

6.028

17.00

13–38

Subjects (%) 10 (23.8) 8 (19.0) 6 (14.3) 4 (9.5) 8 (19.0) 2 (4.8) 4 (9.5)

NOS, not otherwise specified.

†Three patients in the sample did not require any hospital admission.

Explanatory scales whom the age at puberty was unknown, were also excluded. As such, the final size of our sample was 42 women, who provided written informed consent following the description of the study. Twenty-six patients (61.9%) of the sample were recruited from child and adolescent mental health services and 16 patients (38.1%) from adult mental health services. All the subjects of the sample were receiving anti-psychotic treatment with risperidone (35.7%), olanzapine (40.5%), quetiapine (16.7%) or aripiprazole (7.1%) at time of inclusion. A total of 17 subjects out of 41 (41.4%) presented use of cannabis by the time of their first episode of psychosis, 18 subjects (43.9%) presented use of alcohol, 6 subjects of cocaine (14.6%), 3 subjects of stimulating drugs (7.3%) and 1 subject of sedative drugs (2.4%), according to DSM-IV (Diagnostic and Statistical Manual of Mental Disorders, Fourth Edition) criteria for abuse or dependence. No other substances were used by the participants of the study.

Data gathered We obtained retrospective data regarding their age on recruitment, age at menarche,19 first psychotic symptoms, first psychiatry contact and first hospital admission through clinical and socio-demographic interviews with the patient and one relative (Table 1). In order to investigate the age at menarche of our patients, we used the retrospective recall method, which is usually used among the studies that include age at menarche as a variable and correlates highly with original age at menarche.20 We interviewed the patient as well as a first-degree family member in order to minimize a recall bias. Diagnoses made one year after their first psychiatry contact were collected according to the DSM-IV criteria (Table 2) to confirm the original diagnoses. © 2014 Wiley Publishing Asia Pty Ltd

Positive and Negative Syndrome Scale (PANSS) and Clinical Global Impression–Schizophrenia Scale (ICG-ESQ) were taken as a measure of clinical severity. PANSS consists of positive, negative and general sub-scales and measures 30 symptoms on a scale of 1–7, with higher scores indicating higher psychopathology.21,22 ICG-ESQ determines the severity of the episode also in a scale of 1–7 in four groups of schizophrenia symptoms (positive, negative, cognitive and depressive).23 Both evaluations were carried out scoring the episode’s most severe symptoms and were performed between onset of psychosis and 2 weeks after. The assessment was performed by two trained psychologists. The evaluators scored over 0.70 in the intra-class correlation coefficient of the instruments before the start of the study. The Global Assessment of Functioning (GAF)24 score was employed as a measure of outcome. This score is used to measure global functioning (clinical/social), where 1 represents severe dysfunction and 100 represents best functioning. Social functioning was assessed by the Disability Assessment Schedule, short version (DAS-sv), where higher scores indicate greater disability.25 Obstetric complications were measured using the Lewis and Murray Obstetric Complication Scale,26 yielding scores on an ordinal scale (as the number of complications). The scale was administered to the mother of the patient to assess the presence of several obstetric complications. The complications included were syphilis and rubella during the pregnancy, pre-eclampsia, haemorrhage, gestational age under 37 or over 42 weeks, more than 36 hours of labour, Caesarean section, abnormal presentation of the fetus, twins, use of forceps, prolapse of umbilical cord, weight under 2000 g and more than 4 weeks in an incubator.27 Family history of psychosis through the Andreasen interview with the patient and her relative28 and cannabis use (abuse or dependence 3

Menarche and age at onset of psychosis according to DSM-IV) prior to first psychotic symptoms were also assessed and recorded as binary variables (yes/no). Cognitive assessment was performed through the Wechsler Adult Intelligence Scale, 3rd Edition (WAIS-III)29 and Wechsler Intelligence Scale for Children, 4th Edition (WISC-IV).30 The estimated IQ was calculated by vocabulary subtest as suggested previously by several authors.31 Finally, EuroQoL 5D (EQ-5D) was used to assess quality of life. Social tariffs for EQ-5D health states were used, which are obtained based on self-rated health and the rating of hypothetical health states (using visual analogue scale and time trade-off techniques). Tariffs also discriminate between healthy and non-healthy subjects, and are a valid of preferences for health states.32 Statistical analyses Power analyses were conducted and indicated that, in order to detect a linear correlation of 0.5 with a statistical power of 80% and a confidence of 95%, we needed a sample of at least 35 women. Linear correlations between quantitative and normal distributed dependent variables were performed by means of a Pearson coefficient. Spearman coefficient was used when correlation analyses involved ordinal variables. Mann–Whitney U and Kruskal–Wallis tests were applied to assess association between non-normal variables and categorical measures. All analyses were carried out with 17th version of SPSS (SPSS Inc., Chicago, IL, USA). The chosen significance level was P < 0.05. RESULTS In our series, we found no significant correlation between the age at menarche and age at first psychotic symptoms, psychiatry services contact or hospital admission, most severe PANSS score, most severe ICG-ESQ score, GAF score, DAS total score or EuroQoL score (Table 3). The estimated IQ was not significantly related with age at menarche (0.163, P 0.391), age at first psychotic symptoms (−0.063, P 0.742) or family antecedents of psychosis (−0.105, P 0.580). Possible confounding variables were subsequently taken into consideration, such as parental loading of psychosis, antecedents of obstetric complications (by using the Lewis–Murray Scale) and regular use of cannabis by the time of the first episode of psychosis. Regarding the obstetric complication variable, data of 10 subjects were missing. We found that 28 4

TABLE 3. Pearson correlations between age at menarche and age at psychosis onset, PANSS, ICG-ESQ, GAF, DAS and EuroQoL scores (n) Pearson correlations with the age at menarche Age at first psychotic symptoms (42) Age at first psychiatry contact (42) Age at first hospital admission (39) PANSS total score (42) PANSS positive subscale (42) PANSS negative subscale (42) PANSS general subscale (42) ICG-ESQ total score (37) GAF (41) DAS total score (33) EuroQoL (32)

P

0.061

0.702

0.059 −0.036 0.054 −0.063 0.016 0.129 −0.230 0.128 −0.046 −0.016

0.709 0.827 0.733 0.693 0.918 0.414 0.170 0.426 0.800 0.932

DAS, Disability Assessment Schedule; EuroQoL, European Quality of Life; GAF, Global Assessment Function; ICG-ESQ, Clinical Global Impression– Schizophrenia Scale; PANSS, Positive and Negative Syndrome Scale.

out of 32 subjects had suffered from at least one obstetric complication (20 had suffered from one obstetric complication, 4 cases from 2 complications and 4 cases from 3 complications). A total of 17 subjects out of 41 presented regular use of cannabis by the time of their first episode of psychosis and 4 subjects out of 42 reported antecedents of parental psychosis. We created an ordinal variable, adding these three predisposing factors for earlier age of psychosis together, and carried out a Spearman correlation test between them and the age at menarche. We obtained significant results (Spearman coefficient = −0.412, P = 0.021), showing that patients with earlier menarche in our sample had more psychosis anticipating factors. To detect which of these factors could be related to an earlier age at menarche, and thus could have affected our results, Kruskal–Wallis and Mann–Whitney U-tests were carried out. Only the presence of parental psychosis antecedents yielded statistically significant results (P = 0.010). Hormonal contraceptive treatment was also taken into consideration. Six patients (14.3%) were using contraceptive treatment when included in the study but we found no differences in age at onset of psychosis between women who were taking contraceptive treatment and women who were not (P = 0.228). In order to detect differences between the two age groups of our sample, we compared the relationship between age at menarche and age at onset of psychosis separately for the paediatric sample and the adult one. The correlation was not statistically significant in either group (Pearson’s correlation = 0.223 © 2014 Wiley Publishing Asia Pty Ltd

E. Rubio-Abadal et al. P = 0.306, Pearson’s correlation =−0.051 P = 0.835, respectively) and no differences were found in PANSS score (P = 0.236), age at menarche (P = 0.188), presence of obstetric complications (P = 0.098), use of cannabis (P = 0.813) or parental history of psychosis (P = 0.841) between the two age groups. DISCUSSION Our results do not support the hypothesis that women with early puberty would develop psychotic episodes later and present less severe symptoms of psychosis and better outcome. As mentioned earlier, previous studies produced variable results on the relationship between age at puberty and age at first episode of psychosis. Whereas Cohen et al.8 and Galdós et al.9 did report a significant difference working with samples of 32 and 35 women, respectively, other studies’ findings, such as those performed by Ruiz et al.11 and Hochman and Lewine,10 are similar to our results and did not show significant differences, although they worked with larger samples (of 105 and 68 women, respectively). In our study, associations between age at menarche and clinical severity or outcome were not found. Hochman and Lewine10 did report higher negative symptom scores and greater functional impairment in subjects reporting a later age of menarche by using similar measuring instruments (GAF, SANS). Other studies previously mentioned did not find differences in this aspect. Previously described confounding influences, including parental psychosis antecedents, cannabis use and obstetric complications, were more frequent in subjects with an earlier age at menarche, although only the first one reached statistical significance. These factors could have brought forward the age at onset of psychosis of those patients with earlier age at menarche, although we did not find statistical proof that this fact could be affecting the results that were expected. Könnecke et al.12 previously described a lower age at onset of psychosis among patients with at least one first-degree relative suffering from schizophrenia and in cases of pre- and peri-natal complications, although this second result was not statistically significant. Cohen et al.8 also studied substance use, brain injury, obstetric complications and family history of schizophrenia as possible confounders, but concluded that none of them was interfering in the interaction of puberty and onset of illness. In conclusion, our results do not support those findings in which an earlier commencement of © 2014 Wiley Publishing Asia Pty Ltd

puberty is associated with a later age of psychosis onset and lower symptom severity. This negative result, rather than providing evidence against the oestrogen theory of schizophrenia, may indicate that oestrogen theory is more complex than previously thought, with psychosocial and biological factors involved. For instance, coupled to the differences in oestrogen levels and hormonal fluctuations, differences in the specific genotypes of the oestrogen–receptor binding sequences could also explain gender differences in psychosis as has been observed in bipolar disorder and schizophrenia.33,34 A limitation of the present study is the relatively small sample size (n = 42), although some of the previous studies that used similar sample sizes did find statistically significant results. Another limitation to our results is that obstetric complication data were not available for 10 patients due to not being able to contact the patient’s mother and, unfortunately, paediatric reports were not available for these patients. Mothers’ age at menarche was unfortunately not collected, which has been found to correlate well with the age at menarche in daughters.35 Also, since women with first-episode psychosis were recruited in our study, axis-I diagnoses were more heterogeneous than in previous studies, including bipolar disorder and not otherwise specified psychotic disorder. We collected the diagnoses given after 1 year of the first psychotic episode aiming to avoid unspecific diagnoses usually given to first-episode psychosis patients in daily clinical practice. This fact becomes more evident in the child and adolescent group, who are known to present with less specific psychotic symptoms in schizophrenia.36,37 In our sample, subjects who had received a diagnosis of bipolar disorder and druginduced psychotic disorder were indeed mainly children and adolescents (87.5% and 100%, respectively). However, we can anticipate that some of the subjects in our sample might not develop a schizophrenic disorder, which could have affected the external validity of our study. Also, the fact that 61.9% of the sample came from the Child and Adolescent Mental Health Service could represent a bias to the sample since the adult women with first psychotic episode could be underrepresented. Finally, another possible factor to take into account is that menarche could be a non-precise measure for age at onset of puberty and could be recalled differently depending upon the age of each subject. One recommendation for further studies might be to determine the age of puberty by using other characteristics, such as sexual development signs available in scales for pubertal development,38 which were not available in our study, as well as 5

Menarche and age at onset of psychosis genetic and environmental factors that can influence age at menarche. The timing of puberty is clearly not a simple function of chronological age, participating a substantial heritability (considered to be from 0.50 to 0.74),39,40 but also internal and external factors such as growth, body fat/ composition, diet, stress, annual change in photoperiod, circadian time, gonadal steroids, energy expenditure in locomotor activity and others,41 which should be taken into account. Also, should we consider the possible menstrual alterations (such as anovulatory cycles, luteal defects or periods of amenorrhea), as well as onset of puberty, which can present with psychosis (menstrual psychosis). It has been described that this psychosis can initiate even before time of menarche due to secretion of gonadal hormones.42 We suggest that further research in this area is needed, which is of increasing interest as it may provide a better understanding of psychosis aetiopathogenesis and also since potentially therapeutic benefits based upon the oestrogen protection theory have been recently demonstrated.43–45 ACKNOWLEDGEMENTS This project received financial help from the Fondo de Investigaciones Sanitarias de España (FIS PI05/ 1115), the Instituto de Salud Carlos III de España, Centro de Investigación en Red de Salud Mental (CIBERSAM) and Caja Navarra. Special thanks to Csaba Fehér and Stephen Kelly. REFERENCES 1. Hafner H, an der Heiden W, Behrens S et al. Causes and consequences of the gender difference in age at onset of schizophrenia. Schizophr Bull 1998; 24: 99–113. 2. Häfner H, Maurer K, Löffler W, an der Heiden W, Hambrecht M, Schultze-Lutter F. Modeling the early course of schizophrenia. Schizophr Bull 2003; 29: 325–40. 3. Segarra R, Ojeda N, Zabala A et al. Similarities in early course among men and women with a first episode of schizophrenia and schizophreniform disorder. Eur Arch Psychiatry Clin Neurosci 2012; 262: 95–105. 4. Usall J, Busquets E, Araya S, Ochoa S, Gost A. Gender differences in schizophrenia. A literature review. Actas Esp Psiquiatr 2000; 28: 178–85. 5. Riecher-Rössler A, Seeman MV. Oestrogens and schizophrenia – introduction. Arch Womens Ment Health 2002; 5: 91–2. 6. Seeman MV, Lang M. The role of estrogens in schizophrenia gender differences. Schizophr Bull 1990; 16: 185–94. 7. Hafner H, Behrens S, De Vry J, Gattaz WF. An animal model for the effects of estradiol on dopamine-mediated behavior: implications for sex differences in schizophrenia. Psychiatry Res 1991; 38: 125–34. 8. Cohen RZ, Seeman MV, Gotowiec A, Kopala L. Earlier puberty as a predictor of later onset of schizophrenia in women. Am J Psychiatry 1999; 156: 1059–64.

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39. Palmert MR, Hirschhorn JN. Genetic approaches to stature, pubertal timing, and other complex traits [Review]. Mol Genet Metab 2003; 80 (1–2): 1–10. 40. Jahanfar S, Lye MS, Krishnarajah IS. Genetic and environmental effects on age at menarche, and its relationship with reproductive health in twins. Indian J Hum Genet 2013; 19: 245–50. 41. Ebling FJ. The neuroendocrine timing of puberty [Review]. Reproduction 2005; 129: 675–83. 42. Brockington IF. Menstrual psychosis: a bipolar disorder with a link to the hypothalamus. Curr Psychiatry Rep 2011; 13: 193–7. 43. Kulkarni J, Fitzgerald PB, Bailey M. Estrogen in severe mental illness: a potential new treatment approach. Arch Gen Psychiatry 2008; 65: 955–60. 44. Kulkarni J, Gurvich C, Lee SJ et al. Piloting the effective therapeutic dose of adjunctive selective estrogen receptor modulator treatment in postmenopausal women with schizophrenia. Psychoneuroendocrinology 2010; 35: 1142–7. 45. Usall J, Huerta-Ramos E, Iniesta R et al. Raloxifene as an adjunctive treatment for postmenopausal women with schizophrenia: a double-blind, randomized, placebocontrolled trial. J Clin Psychiatry 2011; 72: 1552–7.

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Relationship between menarche and psychosis onset in women with first episode of psychosis.

The aim of this study was to explore the relationship between age at menarche and age at first episode of psychosis, as well as clinical severity and ...
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