Journal of Affective Disorders 175 (2015) 256–259
Contents lists available at ScienceDirect
Journal of Affective Disorders journal homepage: www.elsevier.com/locate/jad
Brief report
Relationships between chronotypes and affective temperaments in healthy young adults Chun Il Park a,b, Suk Kyoon An a,b, Hae Won Kim a,b, Min Jung Koh a,b, Kee Namkoong a,b, Jee In Kang a,b,n, Se Joo Kim a,b,n a b
Department of Psychiatry, Yonsei University College of Medicine, Seoul, South Korea Institute of Behavioral Science in Medicine, Yonsei University College of Medicine, Seoul, South Korea
art ic l e i nf o
a b s t r a c t
Article history: Received 10 October 2014 Received in revised form 8 January 2015 Accepted 8 January 2015 Available online 15 January 2015
Background: Chronotype, an individual's preferred time for activity and sleep, has been known to be associated with affective disorders. Affective temperaments may be subclinical manifestations that represent a biological diathesis for affective disorders. Therefore, the aim of this study is to investigate the relationships between circadian preferences and affective temperaments. Methods: Six hundred and forty one healthy young adults (376 male, 265 female) completed the Korean Translation of Composite Scale of Morningness to measure diurnal preferences and the Temperament Scale of Memphis, Pisa, Paris and San Diego - Autoquestionnaire (TEMPS-A) to measure cyclothymic, depressive, hyperthymic, irritable, and anxious affective temperaments. Multivariate analyses of covariance were computed with the five affective temperaments as dependent variables, chronotype and gender as an independent variable, and age as a covariate. Results: One hundred and sixteen subjects were classified as having morning-type (18.1%), 402 as intermediate-type (62.7%), and 123 as evening-type (19.2%) circadian preferences. Evening-type was significantly associated with greater depressive, cyclothymic, irritable, and anxious temperaments, while morning-type was significantly associated with hyperthymic temperament. Limitations: The present study only used self-report questionnaires to measure diurnal preference. Conclusions: Evening-type subjects were more likely to have depressive, cyclothymic, irritable and anxious temperaments, whereas morning-types were more likely to have hyperthymic temperament. This relationship between chronotype and affective temperament might be important for vulnerability to affective disorders. & 2015 Elsevier B.V. All rights reserved.
Keywords: Affective temperaments TEMPS-A Chronotype Morning-type Evening-type
1. Introduction Circadian rhythm refers to the cycle with oscillations of close to 24 h of biochemical, physiological, and behavioral processes that generate an organism's dynamic internal milieu (Czeisler et al., 1999; Othmer et al., 1969). The internally derived circadian systems are entrained by external cues called zeitgebers such as day–night cycles (Jewett et al., 1991). Optimal coordination of circadian rhythms in the internal milieu and external world is essential for an organism's fundamental adaptation and optimal functioning. Desynchronization of human circadian rhythms may play a critical role in the development of health problems including psychiatric disorders (Evans and Davidson, 2013). n Correspondence to: Department of Psychiatry, Yonsei University College of Medicine 50-1 Yonsei-Ro, Seodaemun-gu, Seoul 120-752, South Korea. Tel.: þ 82 2 2228 1620; fax: þ82 2 313 0891. E-mail addresses: [email protected] (J.I. Kang), [email protected] (S.J. Kim).
http://dx.doi.org/10.1016/j.jad.2015.01.004 0165-0327/& 2015 Elsevier B.V. All rights reserved.
Over the past several decades, there has been growing interest in disrupted circadian rhythms in affective disorders (Adan et al., 2012). Several studies have reported sleep problems and circadian rhythm disruptions in euthymic states (Millar et al., 2004; Sitaram et al., 1982) as well as in manic and depressive episodes (Harvey, 2008). These findings suggest that disturbances in the circadian timing system might be not only a core symptom, but also a fundamental pathophysiological element in affective disorders. Circadian preference indicating an individual's preferred time for activity and sleep has been known to account for substantial variation in circadian rhythm (Giannotti et al., 2002). Several studies have shown relationships between circadian preferences and affective disorders (Ahn et al., 2008; Gaspar-Barba et al., 2009; Selvi et al., 2010). A Korean study of euthymic patients with bipolar disorder reported an association between evening preference and bipolar disorder (Ahn et al., 2008), consistent with other studies (Wood et al., 2009). Evening preference is related to severe depressive symptoms in both depressive patients and nonclinical populations (Selvi et al.,
C.I. Park et al. / Journal of Affective Disorders 175 (2015) 256–259
2010). These findings suggest that evening-type individuals may be particularly vulnerable to affective disorders (Adan et al., 2012). Affective temperaments may be subclinical manifestations that represent a biological diathesis for affective disorders (Akiskal et al., 1995; Kochman et al., 2005). Several previous studies using the Temperament Scale of Memphis, Pisa, Paris and San Diego - Autoquestionnaire (TEMPS-A) or similar instruments showed that healthy firstdegree relatives of bipolar I patients were more likely to have cyclothymic temperament than normal controls (Chiaroni et al., 2005; Kesebir et al., 2005). Other studies revealed that patients with bipolar disorder had higher cyclothymic, depressive, irritable, and anxious temperament scores compared to normal subjects (Evans et al., 2005; Mendlowicz et al., 2005). Therefore, affective temperament may reflect a fundamental predisposition for affective disorders (Rihmer et al., 2010). However, until recently there has been little research examining direct relationships between affective temperament and circadian preference. A web-based survey in a Brazilian sample using the Circadian Energy Scale (CIRENS) and the 52-item Affective and Emotional Composite Temperament Scale (AFECTS) showed that apathetic, cyclothymic, dysphoric, and disinhibited temperaments were associated with an evening preference (Ottoni et al., 2012). This suggests that evening preference might be associated with affective temperaments. Studies using more popular comprehensive measurements of circadian preference and affective temperaments are needed to elucidate the relationship between them. Therefore, the present study aimed to investigate relationships between circadian preference and affective temperaments measured by the TEMPS-A. We hypothesized that cyclothymic, irritable, anxious, and depressive temperaments, which have been reported to be related to affective disorders, would be more associated with evening preference.
2. Methods 2.1. Participants Six hundred and seventy nine Korean volunteers (404 male, 275 female) aged 19 years or older were recruited by advertisement. All participants were interviewed by psychiatrists and subjects with any current or past psychiatric disorder according to Diagnostic and Statistical Manual of Mental Disorders, 4th Edition (DSM-IV), family history of psychiatric disorders, or neurologic disorders were excluded. Thirty eight subjects were excluded for these reasons, leaving 641 subjects (376 male, 265 female) aged 18–47 years (22.773.71) who participated in the study. All subjects provided informed consent before the study. The study protocol was approved by the Institutional Review Board of Severance Mental Health Hospital. 2.2. Materials and procedures Chronotype was assessed with the Korean Translation of Composite Scale of Morning-type (CSM) that was standardized for the Korean population (Yoon et al., 1997). The test has 13 items taken from the Morning-type-Evening-type Questionnaire and Diurnal Type Scale. The CSM is a reliable measure that shows high sensitivity in classifying subjects as morning-type or evening-type (Caci et al., 2005; Smith et al., 1989), and the internal reliability was high in the present sample (Cronbach's α ¼0.83). Total scores ranged from 13 to 55, with higher scores indicating more morning preference, and lower scores indicating more evening preference. In this study, participants in the top 20th percentile of CSM scores were classified as morning-type, the bottom 20th percentile were classified as evening-type, and the middle 60% were classified as intermediate-type (Prat and Adan, 2013).
257
Affective temperaments were measured by the TEMPS-A, which was developed as a self-report temperament scale to evaluate various affective temperament dimensions (Akiskal et al., 2005b). This yes-or-no type questionnaire consists of 110 items (109 for male subjects) that pertain to depressive (items 1–21), cyclothymic (items 22–42), hyperthymic (items 43–63), irritable (items 64–84 for female, 64–83 for male), and anxious (items 85–110) temperaments. Each of the subscale is made up of sections on mood, cognitive, psychomotor, and socially adaptive traits. The TEMPS-A is thought to be a suitable description of the affective temperaments in both clinical and non-clinical samples (Di Florio et al., 2010; Rózsa et al., 2008), while not being influenced by current mood state (Akiskal et al., 2005a). 2.3. Data analysis Partial correlations controlling for age were conducted between the five affective temperaments and total CSM scores. Reliability of the applied scales was assessed using Cronbach's α. Multiple analyses of covariance (MANCOVA) with Bonferroni corrections were performed using the total scores for each TEMPS-A dimension as dependent variables and circadian typology and gender as fixed factors. Age was entered as a covariate to control for possible effects. Partial eta squared (η2p) was calculated as a measure of effect size. Data analysis was performed using SPSS statistics (version 20.0), and statistical tests were bilateral with Type I error set at 5%.
3. Results The number of subjects in each chronotype group was as follows: morning-type 116 (18.1%; 57 male, 59 female), intermediate-type 402 (62.7%; 252 male, 150 female), and evening-type 123 (19.2%; 67 male, 56 female). There was a significant difference in sex between chronotype groups (χ2 ¼7.915, do¼ 2, p¼0.019), such that eveningtypes were more prevalent in male than in female. The partial correlation matrix for the five TEMPS-A dimensions and total CSM scores controlling for age is shown in Table 1. There was a significant negative correlation between total CSM score and depressive, cyclothymic, irritable, and anxious temperaments, whereas there was a significant positive correlation between total CSM score and hyperthymic temperament. The pattern of correlations was similar in male and female subjects. The MANCOVA results are shown in Table 2. There were significant overall effects of chronotype (Wilks λ ¼ 0.90, F(10, 1260) ¼ 7.11, p o0.001) and gender (Wilks λ ¼0.96, F(5, 630) ¼5.97, po 0.001) on these results, although no effects of chronotype x sex interaction (Wilks λ ¼0.99, F(10, 1260) ¼ 0.74, p ¼0.68) were found on TEMPS-A dimensions. Female subjects had significantly higher depressive (F¼ 13.66, po 0.001, η2p ¼ 0.021), cyclothymic (F¼ 8.39, p¼ 0.004, η2p ¼ 0.013), and anxious temperament scores (F¼12.46, Table 1 Partial correlation coefficients (age controlled) between the TEMPS-A dimensions and total CSM scores. CSM (Total) DEP CYC HYP IRR ANX
†
0.207 0.195† 0.192† 0.254† 0.200†
CSM (Male) †
0.178 0.160* 0.200† 0.214† 0.181†
CSM (Female) 0.244† 0.241† 0.183* 0.301† 0.226†
Abbreviations: DEP¼depressive, CYC¼ cyclothymic, HYP¼ hyperthymic, IRR¼ irritable, ANX¼ anxious. n
†
p o 0.01. p o 0.001.
258
C.I. Park et al. / Journal of Affective Disorders 175 (2015) 256–259
Table 2 Multivariate analysis comparing scores for each affective temperament dimension for each chronotype (mean 7 SEM) after controlling age. Total (N ¼ 641)a
DEP CYC HYP IRR ANX
E (N¼ 123)
I (N ¼402)
M (N¼ 116)
8.34 7 0.28 9.29 7 0.43 10.007 0.43 5.53 7 0.31 8.497 0.48
7.117 0.16 7.26 7 0.24 10.84 7 0.25 3.517 0.17 6.26 7 0.28
6.28 7 0.28 6.36 7 0.44 12.93 7 0.44 3.007 0.31 5.337 0.50
F
p
ηp2
Post-hoc*
13.98 12.72 12.27 20.65 11.69
o 0.001 o 0.001 o 0.001 o 0.001 o 0.001
0.042 0.039 0.037 0.061 0.036
E 4M, E 4M, E oM, E 4M, E 4M,
E 4 I, I 4M E 4 I, I ¼M E ¼ I, I oM E 4 I, I ¼M E 4 I, I ¼M
Abbreviations: E ¼ Evening-type, I ¼ Intermediate-type, M ¼Morning-type, DEP ¼depressive, CYC ¼ cyclothymic, HYP ¼hyperthymic, IRR¼ irritable, ANX ¼anxious. a n
Chronotype - Wilks λ ¼0.90, F(10, 1260) ¼ 7.11, p o 0.001, gender - Wilks λ¼ 0.96, F(5, po 0.05, Bonferroni-corrected.
p o0.001, η2p ¼ 0.019), while males scored higher in hyperthymic temperament (F¼6.63, p ¼0.01, η2p ¼0.010). There was no difference of irritable temperament between male and female subjects (F¼ 0.11, p ¼0.74, η2p ¼0.010). In comparing chronotypes, eveningtype subjects showed significantly higher depressive, cyclothymic, irritable, and anxious temperament scores and significantly lower hyperthymic temperament scores than morning-type subjects.
4. Discussion The present study investigated the associations between affective temperaments and circadian preference in healthy young adults. To our knowledge, this is the first study that investigated direct relationships between circadian typologies and affective temperaments using the TEMPS-A. As hypothesized, evening-type subjects had significantly higher depressive, cyclothymic, irritable, and anxious temperament scores than morning-type subjects. In addition, there were more morning-types with hyperthymic temperament. The main results of the present study are consistent with a previous study that used the CIRENS and AFECTS in a Brazilian sample. The depressive, apathetic, cyclothymic, volatile, disinhibited, and euphoric temperaments of the AFECTS had higher energy in the evening, which suggests an evening preference (Ottoni et al., 2012). When considering that the depressive, cyclothymic, and irritable temperaments of the TEMPS-A have several common features with the depressive/apathetic, cyclothymic, and euphoric temperaments of the AFECTS, respectively, these findings were compatible with our results of association between evening preference and affective temperaments. Furthermore, similar to our results, Ottoni et al. found an association between hyperthymic temperament and an earlier circadian rhythm (Ottoni et al., 2012). Some researchers suggested that the hyperthymic temperament is extroverted yet stable (low sensitivity, high control, and coping) (Lara et al., 2012), has a favorable sleep profile (Ottoni et al., 2011), and is thus protective against psychopathology (Lara et al., 2012). Other studies also reported that the hyperthymic temperament was related to resilience to depressive disorder (Kesebir et al., 2013), less suicidal ideation, and less hopelessness (Pompili et al., 2012). These findings suggest that a hyperthymic temperament combined with a morning preference may be an overall positive trait and protective factor for various mental illnesses, especially affective disorders. However, these results should be interpreted with caution, as some studies have reported an association between a hyperthymic temperament and bipolar spectrum psychopathology in young adults at risk for bipolar disorders (DeGeorge et al., 2014). Contrary to our results that indicate higher irritable and anxious temperaments in evening-type subjects, Ottoni et al. found no associations between them (Ottoni et al., 2012). One possible reason for this discrepancy is the difference of scales used to measure circadian
630) ¼ 5.97,
p o 0.001, chronotype x gender - Wilks λ¼ 0.99, F(10, 1260) ¼0.74, p¼ 0.68.
preference (CIREN vs. CSM) and affective temperament (AFECTS vs. TEMPS-A). The AFECTS uses only a short description of each putative affective temperament with a 5-likert scale, whereas TEMPS-A has multiple (21–26) items with a yes-or-no type for each temperament. In addition, the CIRENS consists of two simple questions based on energy level, whereas the CSM has 13 questions regarding how much the respondent prefers a particular time of the day to be active. Previous research supports the relationship between evening preference and various psychiatric conditions. Depressive, cyclothymic, irritable, and anxious temperaments of the TEMPS-A have been found to be positively associated with 12-month prevalence of various DSMIV diagnoses including mood disorders, while the hyperthymic temperament is negatively associated (Karam et al., 2010). Many studies have found that bipolar patients are more likely to be evening-type than the normal population (Wood et al., 2009). A Korean study also reported an association between evening preference and euthymic bipolar disorder (Ahn et al., 2008). Patients with mood disorders (Aguiar Ferreira et al., 2013) and relatives of bipolar patients (Chiaroni et al., 2005) tend to have greater depressive and cyclothymic temperaments. These findings suggest that circadian typology (i.e., evening-type) mediates affective temperaments (depressive, cyclothymic, irritable, and anxious) that might be a predisposition to affective disorders. Although the mechanism is unclear, social rhythm disturbance in evening-type individuals (Bouwkamp et al., 2013; Frank et al., 2000) or molecular clock genes (Lamont et al., 2007) may be related to proneness to affective disorders. Our results indicating the association between circadian preference and affective temperament may not only be relevant for understanding the affective disorders but also have potential clinical implications. It may be possible to prevent affective disorders by stabilizing vulnerable affective temperaments via circadian rhythmic organizations such as increased lifestyle regularity or daytime light exposure. This study has some limitations. First, chronotype classification was only based on a self-report questionnaire. The use of objective tools including polysomnography, actigraphy, or serum melatonin level may be helpful for overcoming this limitation and evaluating individual circadian rhythms. Second, the Korean version of the TEMPS-A has not been standardized in a Korean population. However, the five TEMPS-A subscales showed acceptable internal consistency in our sample (Cronbach's α ¼0.67–0.88 for each temperament). Third, we could not control factors such as menstrual cycle, shift work schedule, amount of activity, and body mass index that might influence circadian rhythms. Fourth, we excluded only subjects with substance-related disorders according to the DSM-IV and did not consider substance consumption, which does not meet the DSM-IV criteria. Considering that there may be some associations between substance consumption and circadian typology (Adan, 2013), we cannot completely rule out potential influences of subclinical substance use on the present results. Future studies are needed to take both threshold and subthreshold
C.I. Park et al. / Journal of Affective Disorders 175 (2015) 256–259
substance use into consideration when analyzing subject characteristics. Finally, because the present study used a cross-sectional design, the direction of the interaction between chronotype and affective temperaments could not be determined. In conclusion, the present results showed an obvious association between affective temperament and chronotype. Eveningtype subjects had more depressive, cyclothymic, irritable and anxious temperaments, whereas morning-types had more hyperthymic temperaments. This relationship between chronotype and affective temperament might be crucial for assessing vulnerability to affective disorders. Role of funding source The funding source did not give any influences on the study design, data collection, analysis, interpretation of data, the writing of the report, and the decision to submit the paper for publication.
Conflict of interest All authors declare that they have no conflicts of interest.
Acknowledgments This work was supported by grants from the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science, and Technology (2010-0022363).
References Adan, A., 2013. A chronobiological approach to addiction. J. Subst. Use 18, 171–183. Adan, A., Archer, S.N., Hidalgo, M.P., Di Milia, L., Natale, V., Randler, C., 2012. Circadian typology: a comprehensive review. Chronobiol. Int. 29, 1153–1175. Aguiar Ferreira, A., Vasconcelos, A.G., Neves, F.S., Laks, J., Correa, H., 2013. Affective temperaments: familiality and clinical use in mood disorders. J. Affect. Disord. 148, 53–56. Ahn, Y.M., Chang, J., Joo, Y.H., Kim, S.C., Lee, K.Y., Kim, Y.S., 2008. Chronotype distribution in bipolar I disorder and schizophrenia in a Korean sample. Bipolar Disord. 10, 271–275. Akiskal, H.S., Akiskal, K.K., Haykal, R.F., Manning, J.S., Connor, P.D., 2005a. TEMPS-A: progress towards validation of a self-rated clinical version of the temperament evaluation of the Memphis, Pisa, Paris, and San Diego autoquestionnaire. J. Affect. Disord. 85, 3–16. Akiskal, H.S., Maser, J.D., Zeller, P.J., Endicott, J., Coryell, W., Keller, M., Warshaw, M., Clayton, P., Goodwin, F., 1995. Switching from ‘unipolar’ to bipolar II. An 11-year prospective study of clinical and temperamental predictors in 559 patients. Arch. Gen. Psychiatry 52, 114–123. Akiskal, H.S., Mendlowicz, M.V., Jean-Louis, G., Rapaport, M.H., Kelsoe, J.R., Gillin, J.C., Smith, T.L., 2005b. TEMPS-A: validation of a short version of a self-rated instrument designed to measure variations in temperament. J. Affect. Disord. 85, 45–52. Bouwkamp, C.G., de Kruiff, M.E., van Troost, T.M., Snippe, D., Blom, M.J., de Winter, R.F., Judith Haffmans, P.M., 2013. Interpersonal and social rhythm group therapy for patients with bipolar disorder. Int. J. Group Psychother. 63, 97–115. Caci, H., Adan, A., Bohle, P., Natale, V., Pornpitakpan, C., Tilley, A., 2005. Transcultural properties of the composite scale of morningness: the relevance of the “morning affect” factor. Chronobiol. Int. 22, 523–540. Chiaroni, P., Hantouche, E.G., Gouvernet, J., Azorin, J.M., Akiskal, H.S., 2005. The cyclothymic temperament in healthy controls and familially at risk individuals for mood disorder: endophenotype for genetic studies. J. Affect. Disord. 85, 135–145. Czeisler, C.A., Duffy, J.F., Shanahan, T.L., Brown, E.N., Mitchell, J.F., Rimmer, D.W., Ronda, J.M., Silva, E.J., Allan, J.S., Emens, J.S., Dijk, D.J., Kronauer, R.E., 1999. Stability, precision, and near-24 h period of the human circadian pacemaker. Science 284, 2177–2181. DeGeorge, D.P., Walsh, M.A., Barrantes-Vidal, N., Kwapil, T.R., 2014. A three-year longitudinal study of affective temperaments and risk for psychopathology. J. Affect. Disord. 164, 94–100. Di Florio, A., Hamshere, M., Forty, L., Green, E.K., Grozeva, D., Jones, I., Caesar, S., Fraser, C., Gordon-Smith, K., Jones, L., Craddock, N., Smith, D.J., 2010. Affective temperaments across the bipolar-unipolar spectrum: examination of the TEMPS-A in 927 patients and controls. J. Affect. Disord. 123, 42–51.
259
Evans, J.A., Davidson, A.J., 2013. Health consequences of circadian disruption in humans and animal models. Prog. Mol. Biol. Transl. Sci. 119, 283–323. Evans, L., Akiskal, H.S., Keck Jr, P.E., McElroy, S.L., Sadovnick, A.D., Remick, R.A., Kelsoe, J.R., 2005. Familiality of temperament in bipolar disorder: support for a genetic spectrum. J. Affect. Disord. 85, 153–168. Frank, E., Swartz, H.A., Kupfer, D.J., 2000. Interpersonal and social rhythm therapy: managing the chaos of bipolar disorder. Biol. Psychiatry 48, 593–604. Gaspar-Barba, E., Calati, R., Cruz-Fuentes, C.S., Ontiveros-Uribe, M.P., Natale, V., De Ronchi, D., Serretti, A., 2009. Depressive symptomatology is influenced by chronotypes. J. Affect. Disord. 119, 100–106. Giannotti, F., Cortesi, F., Sebastiani, T., Ottaviano, S., 2002. Circadian preference, sleep and daytime behaviour in adolescence. J. Sleep Res. 11, 191–199. Harvey, A.G., 2008. Sleep and circadian rhythms in bipolar disorder: seeking synchrony, harmony, and regulation. Am. J. Psychiatry 165, 820–829. Jewett, M.E., Kronauer, R.E., Czeisler, C.A., 1991. Light-induced suppression of endogenous circadian amplitude in humans. Nature 350, 59–62. Karam, E.G., Salamoun, M.M., Yeretzian, J.S., Mneimneh, Z.N., Karam, A.N., Fayyad, J., Hantouche, E., Akiskal, K., Akiskal, H.S., 2010. The role of anxious and hyperthymic temperaments in mental disorders: a national epidemiologic study. World Psychiatry 9, 103–110. Kesebir, S., Gundogar, D., Kucuksubasi, Y., Tatlidil Yaylaci, E., 2013. The relation between affective temperament and resilience in depression: a controlled study. J. Affect. Disord. 148, 352–356. Kesebir, S., Vahip, S., Akdeniz, F., Yüncü, Z., Alkan, M., Akiskal, H., 2005. Affective temperaments as measured by TEMPS-A in patients with bipolar I disorder and their first-degree relatives: a controlled study. J. Affect. Disord. 85, 127–133. Kochman, F.J., Hantouche, E.G., Ferrari, P., Lancrenon, S., Bayart, D., Akiskal, H.S., 2005. Cyclothymic temperament as a prospective predictor of bipolarity and suicidality in children and adolescents with major depressive disorder. J. Affect. Disord. 85, 181–189. Lamont, E.W., Legault-Coutu, D., Cermakian, N., Boivin, D.B., 2007. The role of circadian clock genes in mental disorders. Dialogues Clin. Neurosci. 9, 333–342. Lara, D.R., Bisol, L.W., Brunstein, M.G., Reppold, C.T., de Carvalho, H.W., Ottoni, G.L., 2012. The Affective and Emotional Composite Temperament (AFECT) model and scale: a system-based integrative approach. J. Affect. Disord. 140, 14–37. Mendlowicz, M.V., Jean-Louis, G., Kelsoe, J.R., Akiskal, H.S., 2005. A comparison of recovered bipolar patients, healthy relatives of bipolar probands, and normal controls using the short TEMPS-A. J. Affect. Disord. 85, 147–151. Millar, A., Espie, C.A., Scott, J., 2004. The sleep of remitted bipolar outpatients: a controlled naturalistic study using actigraphy. J. Affect. Disord. 80, 145–153. Othmer, E., Hayden, M.P., Segelbaum, R., 1969. Encephalic cycles during sleep and wakefulness in humans: a 24 h pattern. Science 164, 447–449. Ottoni, G.L., Antoniolli, E., Lara, D.R., 2012. Circadian preference is associated with emotional and affective temperaments. Chronobiol. Int. 29, 786–793. Ottoni, G.L., Lorenzi, T.M., Lara, D.R., 2011. Association of temperament with subjective sleep patterns. J. Affect. Disord. 128, 120–127. Pompili, M., Innamorati, M., Rihmer, Z., Gonda, X., Serafini, G., Akiskal, H., Amore, M., Niolu, C., Sher, L., Tatarelli, R., Perugi, G., Girardi, P., 2012. Cyclothymicdepressive-anxious temperament pattern is related to suicide risk in 346 patients with major mood disorders. J. Affect. Disord. 136, 405–411. Prat, G., Adan, A., 2013. Relationships among circadian typology, psychological symptoms, and sensation seeking. Chronobiol. Int. 30, 942–949. Rózsa, S., Rihmer, Z., Gonda, X., Szili, I., Rihmer, A., Kő, N., Németh, A., Pestality, P., Bagdy, G., Alhassoon, O., 2008. A study of affective temperaments in Hungary: internal consistency and concurrent validity of the TEMPS-A against the TCI and NEO-PI-R. J. Affect. Disord. 106, 45–53. Rihmer, Z., Akiskal, K.K., Rihmer, A., Akiskal, H.S., 2010. Current research on affective temperaments. Curr. Opin. Psychiatr. 23, 12–18. Selvi, Y., Aydin, A., Boysan, M., Atli, A., Agargun, M.Y., Besiroglu, L., 2010. Associations between chronotype, sleep quality, suicidality, and depressive symptoms in patients with major depression and healthy controls. Chronobiol. Int. 27, 1813–1828. Sitaram, N., Nurnberger Jr., J.I., Gershon, E.S., Gillin, J.C., 1982. Cholinergic regulation of mood and REM sleep: potential model and marker of vulnerability to affective disorder. Am. J. Psychiatry 139, 571–576. Smith, C.S., Reilly, C., Midkiff, K., 1989. Evaluation of three circadian rhythm questionnaires with suggestions for an improved measure of morningness. J. Appl. Psychol. 74, 728–738. Wood, J., Birmaher, B., Axelson, D., Ehmann, M., Kalas, C., Monk, K., Turkin, S., Kupfer, D.J., Brent, D., Monk, T.H., 2009. Replicable differences in preferred circadian phase between bipolar disorder patients and control individuals. Psychiatry Res. 166, 201–209. Yoon, J.S., Shin, S.M., Kook, S.H., Lee, H.Y., 1997. A Preliminary Study on the Korean Translation of Composite Scale(KtCS) to Measure Morningness-eveningness. J. Korean Neuropsychiatr. Assoc. 36, 122–134.
Contents lists available at ScienceDirect
Journal of Affective Disorders journal homepage: www.elsevier.com/locate/jad
Brief report
Relationships between chronotypes and affective temperaments in healthy young adults Chun Il Park a,b, Suk Kyoon An a,b, Hae Won Kim a,b, Min Jung Koh a,b, Kee Namkoong a,b, Jee In Kang a,b,n, Se Joo Kim a,b,n a b
Department of Psychiatry, Yonsei University College of Medicine, Seoul, South Korea Institute of Behavioral Science in Medicine, Yonsei University College of Medicine, Seoul, South Korea
art ic l e i nf o
a b s t r a c t
Article history: Received 10 October 2014 Received in revised form 8 January 2015 Accepted 8 January 2015 Available online 15 January 2015
Background: Chronotype, an individual's preferred time for activity and sleep, has been known to be associated with affective disorders. Affective temperaments may be subclinical manifestations that represent a biological diathesis for affective disorders. Therefore, the aim of this study is to investigate the relationships between circadian preferences and affective temperaments. Methods: Six hundred and forty one healthy young adults (376 male, 265 female) completed the Korean Translation of Composite Scale of Morningness to measure diurnal preferences and the Temperament Scale of Memphis, Pisa, Paris and San Diego - Autoquestionnaire (TEMPS-A) to measure cyclothymic, depressive, hyperthymic, irritable, and anxious affective temperaments. Multivariate analyses of covariance were computed with the five affective temperaments as dependent variables, chronotype and gender as an independent variable, and age as a covariate. Results: One hundred and sixteen subjects were classified as having morning-type (18.1%), 402 as intermediate-type (62.7%), and 123 as evening-type (19.2%) circadian preferences. Evening-type was significantly associated with greater depressive, cyclothymic, irritable, and anxious temperaments, while morning-type was significantly associated with hyperthymic temperament. Limitations: The present study only used self-report questionnaires to measure diurnal preference. Conclusions: Evening-type subjects were more likely to have depressive, cyclothymic, irritable and anxious temperaments, whereas morning-types were more likely to have hyperthymic temperament. This relationship between chronotype and affective temperament might be important for vulnerability to affective disorders. & 2015 Elsevier B.V. All rights reserved.
Keywords: Affective temperaments TEMPS-A Chronotype Morning-type Evening-type
1. Introduction Circadian rhythm refers to the cycle with oscillations of close to 24 h of biochemical, physiological, and behavioral processes that generate an organism's dynamic internal milieu (Czeisler et al., 1999; Othmer et al., 1969). The internally derived circadian systems are entrained by external cues called zeitgebers such as day–night cycles (Jewett et al., 1991). Optimal coordination of circadian rhythms in the internal milieu and external world is essential for an organism's fundamental adaptation and optimal functioning. Desynchronization of human circadian rhythms may play a critical role in the development of health problems including psychiatric disorders (Evans and Davidson, 2013). n Correspondence to: Department of Psychiatry, Yonsei University College of Medicine 50-1 Yonsei-Ro, Seodaemun-gu, Seoul 120-752, South Korea. Tel.: þ 82 2 2228 1620; fax: þ82 2 313 0891. E-mail addresses: [email protected] (J.I. Kang), [email protected] (S.J. Kim).
http://dx.doi.org/10.1016/j.jad.2015.01.004 0165-0327/& 2015 Elsevier B.V. All rights reserved.
Over the past several decades, there has been growing interest in disrupted circadian rhythms in affective disorders (Adan et al., 2012). Several studies have reported sleep problems and circadian rhythm disruptions in euthymic states (Millar et al., 2004; Sitaram et al., 1982) as well as in manic and depressive episodes (Harvey, 2008). These findings suggest that disturbances in the circadian timing system might be not only a core symptom, but also a fundamental pathophysiological element in affective disorders. Circadian preference indicating an individual's preferred time for activity and sleep has been known to account for substantial variation in circadian rhythm (Giannotti et al., 2002). Several studies have shown relationships between circadian preferences and affective disorders (Ahn et al., 2008; Gaspar-Barba et al., 2009; Selvi et al., 2010). A Korean study of euthymic patients with bipolar disorder reported an association between evening preference and bipolar disorder (Ahn et al., 2008), consistent with other studies (Wood et al., 2009). Evening preference is related to severe depressive symptoms in both depressive patients and nonclinical populations (Selvi et al.,
C.I. Park et al. / Journal of Affective Disorders 175 (2015) 256–259
2010). These findings suggest that evening-type individuals may be particularly vulnerable to affective disorders (Adan et al., 2012). Affective temperaments may be subclinical manifestations that represent a biological diathesis for affective disorders (Akiskal et al., 1995; Kochman et al., 2005). Several previous studies using the Temperament Scale of Memphis, Pisa, Paris and San Diego - Autoquestionnaire (TEMPS-A) or similar instruments showed that healthy firstdegree relatives of bipolar I patients were more likely to have cyclothymic temperament than normal controls (Chiaroni et al., 2005; Kesebir et al., 2005). Other studies revealed that patients with bipolar disorder had higher cyclothymic, depressive, irritable, and anxious temperament scores compared to normal subjects (Evans et al., 2005; Mendlowicz et al., 2005). Therefore, affective temperament may reflect a fundamental predisposition for affective disorders (Rihmer et al., 2010). However, until recently there has been little research examining direct relationships between affective temperament and circadian preference. A web-based survey in a Brazilian sample using the Circadian Energy Scale (CIRENS) and the 52-item Affective and Emotional Composite Temperament Scale (AFECTS) showed that apathetic, cyclothymic, dysphoric, and disinhibited temperaments were associated with an evening preference (Ottoni et al., 2012). This suggests that evening preference might be associated with affective temperaments. Studies using more popular comprehensive measurements of circadian preference and affective temperaments are needed to elucidate the relationship between them. Therefore, the present study aimed to investigate relationships between circadian preference and affective temperaments measured by the TEMPS-A. We hypothesized that cyclothymic, irritable, anxious, and depressive temperaments, which have been reported to be related to affective disorders, would be more associated with evening preference.
2. Methods 2.1. Participants Six hundred and seventy nine Korean volunteers (404 male, 275 female) aged 19 years or older were recruited by advertisement. All participants were interviewed by psychiatrists and subjects with any current or past psychiatric disorder according to Diagnostic and Statistical Manual of Mental Disorders, 4th Edition (DSM-IV), family history of psychiatric disorders, or neurologic disorders were excluded. Thirty eight subjects were excluded for these reasons, leaving 641 subjects (376 male, 265 female) aged 18–47 years (22.773.71) who participated in the study. All subjects provided informed consent before the study. The study protocol was approved by the Institutional Review Board of Severance Mental Health Hospital. 2.2. Materials and procedures Chronotype was assessed with the Korean Translation of Composite Scale of Morning-type (CSM) that was standardized for the Korean population (Yoon et al., 1997). The test has 13 items taken from the Morning-type-Evening-type Questionnaire and Diurnal Type Scale. The CSM is a reliable measure that shows high sensitivity in classifying subjects as morning-type or evening-type (Caci et al., 2005; Smith et al., 1989), and the internal reliability was high in the present sample (Cronbach's α ¼0.83). Total scores ranged from 13 to 55, with higher scores indicating more morning preference, and lower scores indicating more evening preference. In this study, participants in the top 20th percentile of CSM scores were classified as morning-type, the bottom 20th percentile were classified as evening-type, and the middle 60% were classified as intermediate-type (Prat and Adan, 2013).
257
Affective temperaments were measured by the TEMPS-A, which was developed as a self-report temperament scale to evaluate various affective temperament dimensions (Akiskal et al., 2005b). This yes-or-no type questionnaire consists of 110 items (109 for male subjects) that pertain to depressive (items 1–21), cyclothymic (items 22–42), hyperthymic (items 43–63), irritable (items 64–84 for female, 64–83 for male), and anxious (items 85–110) temperaments. Each of the subscale is made up of sections on mood, cognitive, psychomotor, and socially adaptive traits. The TEMPS-A is thought to be a suitable description of the affective temperaments in both clinical and non-clinical samples (Di Florio et al., 2010; Rózsa et al., 2008), while not being influenced by current mood state (Akiskal et al., 2005a). 2.3. Data analysis Partial correlations controlling for age were conducted between the five affective temperaments and total CSM scores. Reliability of the applied scales was assessed using Cronbach's α. Multiple analyses of covariance (MANCOVA) with Bonferroni corrections were performed using the total scores for each TEMPS-A dimension as dependent variables and circadian typology and gender as fixed factors. Age was entered as a covariate to control for possible effects. Partial eta squared (η2p) was calculated as a measure of effect size. Data analysis was performed using SPSS statistics (version 20.0), and statistical tests were bilateral with Type I error set at 5%.
3. Results The number of subjects in each chronotype group was as follows: morning-type 116 (18.1%; 57 male, 59 female), intermediate-type 402 (62.7%; 252 male, 150 female), and evening-type 123 (19.2%; 67 male, 56 female). There was a significant difference in sex between chronotype groups (χ2 ¼7.915, do¼ 2, p¼0.019), such that eveningtypes were more prevalent in male than in female. The partial correlation matrix for the five TEMPS-A dimensions and total CSM scores controlling for age is shown in Table 1. There was a significant negative correlation between total CSM score and depressive, cyclothymic, irritable, and anxious temperaments, whereas there was a significant positive correlation between total CSM score and hyperthymic temperament. The pattern of correlations was similar in male and female subjects. The MANCOVA results are shown in Table 2. There were significant overall effects of chronotype (Wilks λ ¼ 0.90, F(10, 1260) ¼ 7.11, p o0.001) and gender (Wilks λ ¼0.96, F(5, 630) ¼5.97, po 0.001) on these results, although no effects of chronotype x sex interaction (Wilks λ ¼0.99, F(10, 1260) ¼ 0.74, p ¼0.68) were found on TEMPS-A dimensions. Female subjects had significantly higher depressive (F¼ 13.66, po 0.001, η2p ¼ 0.021), cyclothymic (F¼ 8.39, p¼ 0.004, η2p ¼ 0.013), and anxious temperament scores (F¼12.46, Table 1 Partial correlation coefficients (age controlled) between the TEMPS-A dimensions and total CSM scores. CSM (Total) DEP CYC HYP IRR ANX
†
0.207 0.195† 0.192† 0.254† 0.200†
CSM (Male) †
0.178 0.160* 0.200† 0.214† 0.181†
CSM (Female) 0.244† 0.241† 0.183* 0.301† 0.226†
Abbreviations: DEP¼depressive, CYC¼ cyclothymic, HYP¼ hyperthymic, IRR¼ irritable, ANX¼ anxious. n
†
p o 0.01. p o 0.001.
258
C.I. Park et al. / Journal of Affective Disorders 175 (2015) 256–259
Table 2 Multivariate analysis comparing scores for each affective temperament dimension for each chronotype (mean 7 SEM) after controlling age. Total (N ¼ 641)a
DEP CYC HYP IRR ANX
E (N¼ 123)
I (N ¼402)
M (N¼ 116)
8.34 7 0.28 9.29 7 0.43 10.007 0.43 5.53 7 0.31 8.497 0.48
7.117 0.16 7.26 7 0.24 10.84 7 0.25 3.517 0.17 6.26 7 0.28
6.28 7 0.28 6.36 7 0.44 12.93 7 0.44 3.007 0.31 5.337 0.50
F
p
ηp2
Post-hoc*
13.98 12.72 12.27 20.65 11.69
o 0.001 o 0.001 o 0.001 o 0.001 o 0.001
0.042 0.039 0.037 0.061 0.036
E 4M, E 4M, E oM, E 4M, E 4M,
E 4 I, I 4M E 4 I, I ¼M E ¼ I, I oM E 4 I, I ¼M E 4 I, I ¼M
Abbreviations: E ¼ Evening-type, I ¼ Intermediate-type, M ¼Morning-type, DEP ¼depressive, CYC ¼ cyclothymic, HYP ¼hyperthymic, IRR¼ irritable, ANX ¼anxious. a n
Chronotype - Wilks λ ¼0.90, F(10, 1260) ¼ 7.11, p o 0.001, gender - Wilks λ¼ 0.96, F(5, po 0.05, Bonferroni-corrected.
p o0.001, η2p ¼ 0.019), while males scored higher in hyperthymic temperament (F¼6.63, p ¼0.01, η2p ¼0.010). There was no difference of irritable temperament between male and female subjects (F¼ 0.11, p ¼0.74, η2p ¼0.010). In comparing chronotypes, eveningtype subjects showed significantly higher depressive, cyclothymic, irritable, and anxious temperament scores and significantly lower hyperthymic temperament scores than morning-type subjects.
4. Discussion The present study investigated the associations between affective temperaments and circadian preference in healthy young adults. To our knowledge, this is the first study that investigated direct relationships between circadian typologies and affective temperaments using the TEMPS-A. As hypothesized, evening-type subjects had significantly higher depressive, cyclothymic, irritable, and anxious temperament scores than morning-type subjects. In addition, there were more morning-types with hyperthymic temperament. The main results of the present study are consistent with a previous study that used the CIRENS and AFECTS in a Brazilian sample. The depressive, apathetic, cyclothymic, volatile, disinhibited, and euphoric temperaments of the AFECTS had higher energy in the evening, which suggests an evening preference (Ottoni et al., 2012). When considering that the depressive, cyclothymic, and irritable temperaments of the TEMPS-A have several common features with the depressive/apathetic, cyclothymic, and euphoric temperaments of the AFECTS, respectively, these findings were compatible with our results of association between evening preference and affective temperaments. Furthermore, similar to our results, Ottoni et al. found an association between hyperthymic temperament and an earlier circadian rhythm (Ottoni et al., 2012). Some researchers suggested that the hyperthymic temperament is extroverted yet stable (low sensitivity, high control, and coping) (Lara et al., 2012), has a favorable sleep profile (Ottoni et al., 2011), and is thus protective against psychopathology (Lara et al., 2012). Other studies also reported that the hyperthymic temperament was related to resilience to depressive disorder (Kesebir et al., 2013), less suicidal ideation, and less hopelessness (Pompili et al., 2012). These findings suggest that a hyperthymic temperament combined with a morning preference may be an overall positive trait and protective factor for various mental illnesses, especially affective disorders. However, these results should be interpreted with caution, as some studies have reported an association between a hyperthymic temperament and bipolar spectrum psychopathology in young adults at risk for bipolar disorders (DeGeorge et al., 2014). Contrary to our results that indicate higher irritable and anxious temperaments in evening-type subjects, Ottoni et al. found no associations between them (Ottoni et al., 2012). One possible reason for this discrepancy is the difference of scales used to measure circadian
630) ¼ 5.97,
p o 0.001, chronotype x gender - Wilks λ¼ 0.99, F(10, 1260) ¼0.74, p¼ 0.68.
preference (CIREN vs. CSM) and affective temperament (AFECTS vs. TEMPS-A). The AFECTS uses only a short description of each putative affective temperament with a 5-likert scale, whereas TEMPS-A has multiple (21–26) items with a yes-or-no type for each temperament. In addition, the CIRENS consists of two simple questions based on energy level, whereas the CSM has 13 questions regarding how much the respondent prefers a particular time of the day to be active. Previous research supports the relationship between evening preference and various psychiatric conditions. Depressive, cyclothymic, irritable, and anxious temperaments of the TEMPS-A have been found to be positively associated with 12-month prevalence of various DSMIV diagnoses including mood disorders, while the hyperthymic temperament is negatively associated (Karam et al., 2010). Many studies have found that bipolar patients are more likely to be evening-type than the normal population (Wood et al., 2009). A Korean study also reported an association between evening preference and euthymic bipolar disorder (Ahn et al., 2008). Patients with mood disorders (Aguiar Ferreira et al., 2013) and relatives of bipolar patients (Chiaroni et al., 2005) tend to have greater depressive and cyclothymic temperaments. These findings suggest that circadian typology (i.e., evening-type) mediates affective temperaments (depressive, cyclothymic, irritable, and anxious) that might be a predisposition to affective disorders. Although the mechanism is unclear, social rhythm disturbance in evening-type individuals (Bouwkamp et al., 2013; Frank et al., 2000) or molecular clock genes (Lamont et al., 2007) may be related to proneness to affective disorders. Our results indicating the association between circadian preference and affective temperament may not only be relevant for understanding the affective disorders but also have potential clinical implications. It may be possible to prevent affective disorders by stabilizing vulnerable affective temperaments via circadian rhythmic organizations such as increased lifestyle regularity or daytime light exposure. This study has some limitations. First, chronotype classification was only based on a self-report questionnaire. The use of objective tools including polysomnography, actigraphy, or serum melatonin level may be helpful for overcoming this limitation and evaluating individual circadian rhythms. Second, the Korean version of the TEMPS-A has not been standardized in a Korean population. However, the five TEMPS-A subscales showed acceptable internal consistency in our sample (Cronbach's α ¼0.67–0.88 for each temperament). Third, we could not control factors such as menstrual cycle, shift work schedule, amount of activity, and body mass index that might influence circadian rhythms. Fourth, we excluded only subjects with substance-related disorders according to the DSM-IV and did not consider substance consumption, which does not meet the DSM-IV criteria. Considering that there may be some associations between substance consumption and circadian typology (Adan, 2013), we cannot completely rule out potential influences of subclinical substance use on the present results. Future studies are needed to take both threshold and subthreshold
C.I. Park et al. / Journal of Affective Disorders 175 (2015) 256–259
substance use into consideration when analyzing subject characteristics. Finally, because the present study used a cross-sectional design, the direction of the interaction between chronotype and affective temperaments could not be determined. In conclusion, the present results showed an obvious association between affective temperament and chronotype. Eveningtype subjects had more depressive, cyclothymic, irritable and anxious temperaments, whereas morning-types had more hyperthymic temperaments. This relationship between chronotype and affective temperament might be crucial for assessing vulnerability to affective disorders. Role of funding source The funding source did not give any influences on the study design, data collection, analysis, interpretation of data, the writing of the report, and the decision to submit the paper for publication.
Conflict of interest All authors declare that they have no conflicts of interest.
Acknowledgments This work was supported by grants from the National Research Foundation of Korea (NRF) funded by the Ministry of Education, Science, and Technology (2010-0022363).
References Adan, A., 2013. A chronobiological approach to addiction. J. Subst. Use 18, 171–183. Adan, A., Archer, S.N., Hidalgo, M.P., Di Milia, L., Natale, V., Randler, C., 2012. Circadian typology: a comprehensive review. Chronobiol. Int. 29, 1153–1175. Aguiar Ferreira, A., Vasconcelos, A.G., Neves, F.S., Laks, J., Correa, H., 2013. Affective temperaments: familiality and clinical use in mood disorders. J. Affect. Disord. 148, 53–56. Ahn, Y.M., Chang, J., Joo, Y.H., Kim, S.C., Lee, K.Y., Kim, Y.S., 2008. Chronotype distribution in bipolar I disorder and schizophrenia in a Korean sample. Bipolar Disord. 10, 271–275. Akiskal, H.S., Akiskal, K.K., Haykal, R.F., Manning, J.S., Connor, P.D., 2005a. TEMPS-A: progress towards validation of a self-rated clinical version of the temperament evaluation of the Memphis, Pisa, Paris, and San Diego autoquestionnaire. J. Affect. Disord. 85, 3–16. Akiskal, H.S., Maser, J.D., Zeller, P.J., Endicott, J., Coryell, W., Keller, M., Warshaw, M., Clayton, P., Goodwin, F., 1995. Switching from ‘unipolar’ to bipolar II. An 11-year prospective study of clinical and temperamental predictors in 559 patients. Arch. Gen. Psychiatry 52, 114–123. Akiskal, H.S., Mendlowicz, M.V., Jean-Louis, G., Rapaport, M.H., Kelsoe, J.R., Gillin, J.C., Smith, T.L., 2005b. TEMPS-A: validation of a short version of a self-rated instrument designed to measure variations in temperament. J. Affect. Disord. 85, 45–52. Bouwkamp, C.G., de Kruiff, M.E., van Troost, T.M., Snippe, D., Blom, M.J., de Winter, R.F., Judith Haffmans, P.M., 2013. Interpersonal and social rhythm group therapy for patients with bipolar disorder. Int. J. Group Psychother. 63, 97–115. Caci, H., Adan, A., Bohle, P., Natale, V., Pornpitakpan, C., Tilley, A., 2005. Transcultural properties of the composite scale of morningness: the relevance of the “morning affect” factor. Chronobiol. Int. 22, 523–540. Chiaroni, P., Hantouche, E.G., Gouvernet, J., Azorin, J.M., Akiskal, H.S., 2005. The cyclothymic temperament in healthy controls and familially at risk individuals for mood disorder: endophenotype for genetic studies. J. Affect. Disord. 85, 135–145. Czeisler, C.A., Duffy, J.F., Shanahan, T.L., Brown, E.N., Mitchell, J.F., Rimmer, D.W., Ronda, J.M., Silva, E.J., Allan, J.S., Emens, J.S., Dijk, D.J., Kronauer, R.E., 1999. Stability, precision, and near-24 h period of the human circadian pacemaker. Science 284, 2177–2181. DeGeorge, D.P., Walsh, M.A., Barrantes-Vidal, N., Kwapil, T.R., 2014. A three-year longitudinal study of affective temperaments and risk for psychopathology. J. Affect. Disord. 164, 94–100. Di Florio, A., Hamshere, M., Forty, L., Green, E.K., Grozeva, D., Jones, I., Caesar, S., Fraser, C., Gordon-Smith, K., Jones, L., Craddock, N., Smith, D.J., 2010. Affective temperaments across the bipolar-unipolar spectrum: examination of the TEMPS-A in 927 patients and controls. J. Affect. Disord. 123, 42–51.
259
Evans, J.A., Davidson, A.J., 2013. Health consequences of circadian disruption in humans and animal models. Prog. Mol. Biol. Transl. Sci. 119, 283–323. Evans, L., Akiskal, H.S., Keck Jr, P.E., McElroy, S.L., Sadovnick, A.D., Remick, R.A., Kelsoe, J.R., 2005. Familiality of temperament in bipolar disorder: support for a genetic spectrum. J. Affect. Disord. 85, 153–168. Frank, E., Swartz, H.A., Kupfer, D.J., 2000. Interpersonal and social rhythm therapy: managing the chaos of bipolar disorder. Biol. Psychiatry 48, 593–604. Gaspar-Barba, E., Calati, R., Cruz-Fuentes, C.S., Ontiveros-Uribe, M.P., Natale, V., De Ronchi, D., Serretti, A., 2009. Depressive symptomatology is influenced by chronotypes. J. Affect. Disord. 119, 100–106. Giannotti, F., Cortesi, F., Sebastiani, T., Ottaviano, S., 2002. Circadian preference, sleep and daytime behaviour in adolescence. J. Sleep Res. 11, 191–199. Harvey, A.G., 2008. Sleep and circadian rhythms in bipolar disorder: seeking synchrony, harmony, and regulation. Am. J. Psychiatry 165, 820–829. Jewett, M.E., Kronauer, R.E., Czeisler, C.A., 1991. Light-induced suppression of endogenous circadian amplitude in humans. Nature 350, 59–62. Karam, E.G., Salamoun, M.M., Yeretzian, J.S., Mneimneh, Z.N., Karam, A.N., Fayyad, J., Hantouche, E., Akiskal, K., Akiskal, H.S., 2010. The role of anxious and hyperthymic temperaments in mental disorders: a national epidemiologic study. World Psychiatry 9, 103–110. Kesebir, S., Gundogar, D., Kucuksubasi, Y., Tatlidil Yaylaci, E., 2013. The relation between affective temperament and resilience in depression: a controlled study. J. Affect. Disord. 148, 352–356. Kesebir, S., Vahip, S., Akdeniz, F., Yüncü, Z., Alkan, M., Akiskal, H., 2005. Affective temperaments as measured by TEMPS-A in patients with bipolar I disorder and their first-degree relatives: a controlled study. J. Affect. Disord. 85, 127–133. Kochman, F.J., Hantouche, E.G., Ferrari, P., Lancrenon, S., Bayart, D., Akiskal, H.S., 2005. Cyclothymic temperament as a prospective predictor of bipolarity and suicidality in children and adolescents with major depressive disorder. J. Affect. Disord. 85, 181–189. Lamont, E.W., Legault-Coutu, D., Cermakian, N., Boivin, D.B., 2007. The role of circadian clock genes in mental disorders. Dialogues Clin. Neurosci. 9, 333–342. Lara, D.R., Bisol, L.W., Brunstein, M.G., Reppold, C.T., de Carvalho, H.W., Ottoni, G.L., 2012. The Affective and Emotional Composite Temperament (AFECT) model and scale: a system-based integrative approach. J. Affect. Disord. 140, 14–37. Mendlowicz, M.V., Jean-Louis, G., Kelsoe, J.R., Akiskal, H.S., 2005. A comparison of recovered bipolar patients, healthy relatives of bipolar probands, and normal controls using the short TEMPS-A. J. Affect. Disord. 85, 147–151. Millar, A., Espie, C.A., Scott, J., 2004. The sleep of remitted bipolar outpatients: a controlled naturalistic study using actigraphy. J. Affect. Disord. 80, 145–153. Othmer, E., Hayden, M.P., Segelbaum, R., 1969. Encephalic cycles during sleep and wakefulness in humans: a 24 h pattern. Science 164, 447–449. Ottoni, G.L., Antoniolli, E., Lara, D.R., 2012. Circadian preference is associated with emotional and affective temperaments. Chronobiol. Int. 29, 786–793. Ottoni, G.L., Lorenzi, T.M., Lara, D.R., 2011. Association of temperament with subjective sleep patterns. J. Affect. Disord. 128, 120–127. Pompili, M., Innamorati, M., Rihmer, Z., Gonda, X., Serafini, G., Akiskal, H., Amore, M., Niolu, C., Sher, L., Tatarelli, R., Perugi, G., Girardi, P., 2012. Cyclothymicdepressive-anxious temperament pattern is related to suicide risk in 346 patients with major mood disorders. J. Affect. Disord. 136, 405–411. Prat, G., Adan, A., 2013. Relationships among circadian typology, psychological symptoms, and sensation seeking. Chronobiol. Int. 30, 942–949. Rózsa, S., Rihmer, Z., Gonda, X., Szili, I., Rihmer, A., Kő, N., Németh, A., Pestality, P., Bagdy, G., Alhassoon, O., 2008. A study of affective temperaments in Hungary: internal consistency and concurrent validity of the TEMPS-A against the TCI and NEO-PI-R. J. Affect. Disord. 106, 45–53. Rihmer, Z., Akiskal, K.K., Rihmer, A., Akiskal, H.S., 2010. Current research on affective temperaments. Curr. Opin. Psychiatr. 23, 12–18. Selvi, Y., Aydin, A., Boysan, M., Atli, A., Agargun, M.Y., Besiroglu, L., 2010. Associations between chronotype, sleep quality, suicidality, and depressive symptoms in patients with major depression and healthy controls. Chronobiol. Int. 27, 1813–1828. Sitaram, N., Nurnberger Jr., J.I., Gershon, E.S., Gillin, J.C., 1982. Cholinergic regulation of mood and REM sleep: potential model and marker of vulnerability to affective disorder. Am. J. Psychiatry 139, 571–576. Smith, C.S., Reilly, C., Midkiff, K., 1989. Evaluation of three circadian rhythm questionnaires with suggestions for an improved measure of morningness. J. Appl. Psychol. 74, 728–738. Wood, J., Birmaher, B., Axelson, D., Ehmann, M., Kalas, C., Monk, K., Turkin, S., Kupfer, D.J., Brent, D., Monk, T.H., 2009. Replicable differences in preferred circadian phase between bipolar disorder patients and control individuals. Psychiatry Res. 166, 201–209. Yoon, J.S., Shin, S.M., Kook, S.H., Lee, H.Y., 1997. A Preliminary Study on the Korean Translation of Composite Scale(KtCS) to Measure Morningness-eveningness. J. Korean Neuropsychiatr. Assoc. 36, 122–134.
