GENDER DIFFERENCES IN MORNINGNESS EVENINGNESS PREFERENCE

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1 CHRONOBIOLOGY INTERNATIONAL, 19(4), (2002) GENDER DIFFERENCES IN MORNINGNESS EVENINGNESS PREFERENCE Ana Adan 1 and Vincenzo Natale 2, * 1 Department of Psychiatry and Clinical Psychobiology, University of Barcelona, Barcelona, Spain 2 Department of Psychology, University of Bologna, Viale Berti Pichat 5, Bologna, Italy ABSTRACT Morningness eveningness preference (morning-, intermediate-, eveningtype) or circadian typology is the individual difference that most clearly explains the variations in the rhythmic expression of biological or behavioral patterns. The aim of this study was to analyze gender difference in morningness eveningness preference using the Horne and Östberg questionnaire in the largest university student population selected so far ðn ¼ 2135Þ; with an age range yr. Morningness eveningness questionnaire (MEQ) score distribution closely correlated to the normal curve ðrange ¼ 17 78; mean ¼ 48:25; SD ¼ 10:11Þ; with 338 (15.84%) morning-types, 1273 (59.62%) intermediate-types, and 524 (24.54%) evening-types. The men and women differed significantly in their mean scores ðp, 0:0001Þ and distribution per circadian typology ðp, 0:00001Þ; with the men presenting a more pronounced eveningness preference. Three factors were identified by factor analysis: time of greatest efficiency (I), sleep time/sleep phase (II), awakening time/sleep inertia (III). The MEQ items sensitive to gender differences were essentially those included in factor I and factor II. The results are discussed in relation to recent models of circadian regulation of the sleep wake cycle. (Chronobiology International, 19(4), , 2002) Key Words: Circadian rhythm; Gender differences; Morningness eveningness; Sleep wake cycle; Time of day *Corresponding author. Fax: ; natale@psibo.unibo.it 709 Copyright q 2002 by Marcel Dekker, Inc.

2 710 ADAN AND NATALE INTRODUCTION Most biological and behavioral parameters present circadian rhythmicity (24h period) synchronized with the light dark cycle, though of endogenous origin to the extent that they follow the same behavioral patterns even when there is no environmental input. [1,2] It has been shown that there are individual differences that affect the expression of circadian rhythms people living under the same environmental conditions and with similar daily activities present rhythmic variations that differ according to the parameters considered. One of the most marked individual differences is the morningness eveningness preference or circadian typology (morning-, intermediate-, and evening-type), which seems to be based on endogenous rhythmic control. [3] In general terms, the circadian functions of morning-type individuals present a phase advance vs. evening-type subjects, the intermediate-type being in an intermediate position. [4,5] Several self-evaluation instruments have been developed to help identify individual circadian typology, the reliability and validity of which have been proved using psychological and biological parameters. The first such instance was the morningness eveningness questionnaire (MEQ) developed by Horne and Östberg. [6] It consists of 19 mixed-format questions regarding the time individuals get up and go to bed, preferred times for physical and mental activity, and subjective alertness. Although it has been criticized for not just collecting information on morningness, but on other domains too, [7,8] and for having low sensitivity in subjects on shift or night work, [9,10] it has proven to be a valid and reliable instrument for subjects with daytime work schedules. [11,12] The MEQ has been translated into many languages, and is still today the most frequently used self-evaluation instrument, on account of which we decided to use it in this study. There is keen interest in the study of relationships between morningness eveningness preference and other individual differences. The closest correlation is that between age and morningness; with advancing age MEQ scores tend to highlight greater morningness. [5,13,14] However, it is not yet clear whether such a relationship is the result of changes in the biology of the circadian pacemaker (CP) or changes in work, and/or domestic arrangements. [15] As regards the relationship between gender and circadian typology the conclusions are not yet univocal. The Kerkhof review [4] concludes that the rhythmic differences between men and women are few and inconsistent, while some authors have found no significant differences in MEQ score distribution between women and men. [8,16 18] However, studies involving larger samples have indicated that women tend to score significantly more towards morningness than men. [12] The same studies have found a phase advance in women s circadian rhythms compared to those of men, even though this advance is less pronounced [14,19 21] than the one that can be seen comparing morning and evening-types. Recently, Natale and Adan [22] showed that the season of birth modulates the morningness preference in men but not in women.

3 GENDER AND MORNINGNESS 711 We believe that gender differences in morningness eveningness preference should be studied further. The aim of the present survey was to examine, in a much broader-based sample of participants than before, the gender preferences in the sleep wake cycle (SWC) using the MEQ. In particular, we analyzed gender differences in: (1) the MEQ score distribution and its descriptive statistics, (2) circadian typology distribution, and (3) distribution and mean score of the answers in each single MEQ item. METHOD A sample of 2135 university students, 1256 Italian (616 men and 640 women), and 879 Spanish (425 men and 454 women), answered the MEQ in its Italian [23] and Spanish [24] version, respectively. The subjects age ranged from 18 to 30 yr ðmean ¼ 22:17 ^ 2:85; median ¼ 21; mode ¼ 20Þðmen ¼ 22:07 ^ 2:95; women ¼ 22:20 ^ 3:36Þ: All participants were tested in groups ranging in size from 10 to 100 students, their participation was voluntary and they were not paid. The MEQ score ranged from 16 to 86, with scores above 58 classifying individuals as morning-type and scores below 41 as evening-types. As suggested by Horne and Östberg, [6] morning-types with scores below 70 were classified as moderate while the rest were classified as definitely morning-types. Evening-types with scores below 31 were classified as definitely evening-types and the rest as moderately evening-types. Internal consistency or reliability of the questionnaire was analyzed using Cronbach s alpha correlation coefficient, values between 0.7 and 0.9 being considered to be very good. [25] The distribution of scores was tested for normality by the Kolmogorov Smirnov test both for the whole sample and for each gender. Descriptive statistics were obtained for the total score of each sex. In order to investigate the dimensions of the MEQ, factor analysis was performed. Gender differences in mean scores were explored using Student s t-test and distribution in circadian typologies using Chi-squared test. In order to evaluate better the gender differences, we ran two supplementary nonparametric item-by-item MEQ analyses: the Mann Whitney test for mean scores and the Chi-squared test for answer distribution. In view of the subjective nature of the data, we decided to consider as significant only those items that proved to be significant in both tests. In view of the large size of the sample, we also decided to consider values of p, 0:005 as cut-off for significant results. Such precautionary measures were taken to minimize possible methodological bias. RESULTS The full scale alpha Cronbach coefficient of the MEQ for the present sample was 0.83 (internal consistency) (0.83 in the Italian sample and 0.84 in the Spanish sample). The average inter-item correlation (homogeneity) was a little lower, with a value of

4 712 ADAN AND NATALE 0.22 (0.22 in the Italian sample and 0.25 in the Spanish sample) ranging between 0.02 and The split-half reliability (even items vs. uneven items) was The MEQ score range was ðmean ¼ 48:25 ^ 10:11; median ¼ 49; mode ¼ 48Þ: The frequency distribution of MEQ scores correlated closely to normal curve as shown by the Kolmogorov Smirnov test ðd ¼ 0:02; p ¼ n:s:þðskewness ¼ 20:18; kurtosis ¼ 20:17Þ: The MEQ score range for men was ðmean ¼ 46:81 ^ 10:34; median ¼ 47; mode ¼ 45Þ and for women ðmean ¼ 49:61 ^ 9:71; median ¼ 50; mode ¼ 48Þ: The mean score for men was significantly lower than that for women ðt 2133 ¼ 6:44; p, 0:0001Þ; a result that was replicated when Italian ðt 1254 ¼ 5:19; p, 0:0001Þ and Spanish ðt 877 ¼ 3:92; p, 0:0001Þ samples were considered separately. With regard to MEQ scores, we performed a supplementary analysis (ANOVA) of two factors: gender (male and female) and sample (Italian and Spanish). The first factor was significant ðf 1;2131 ¼ 41:12; p, 0:00001Þ; confirming that MEQ scores highest in females, as too was the second factor ðf 1;2131 ¼ 17:13; p, 0:00001Þ with the Italian sample scoring higher on MEQ (48.96 ^ 10.08) than the Spanish one (47.14 ^ 10.07). The interaction between the two factors, however, was not significant: females presented MEQ scores higher than males in both Italian ðfemale ¼ 50:42 ^ 10:02; male ¼ 47:49 ^ 9:93Þ; and Spanish ðfemale ¼ 48:46 ^ 9:13; male ¼ 45:82 ^ 10:84Þ samples, proving that the gender effect on MEQ score is the same irrespective of nationality. The frequency distributions of MEQ scores between males ðskewness ¼ 20:16; kurtosis ¼ 20:28Þ and females ðskewness ¼ 20:16; kurtosis ¼ 20:08Þ were also significantly different (Kolmogorov Smirnov p, 0.001), with the distribution shifting towards morningness in women (Fig. 1). The result was the same when Italian ðp, 0:001Þ and Spanish ðp, 0:005Þ samples were considered separately. Figure 1. Frequency distribution of MEQ scores for men and women in the whole sample.

5 GENDER AND MORNINGNESS 713 According to MEQ responses, out of 2135 participants, 338 (15.83%) were morning-type (18.23% in Italian sample and 12.29% in Spanish), 1273 (59.62%) were intermediate-type (59.39% in Italian sample and 59.95% in Spanish), and 524 (24.54%) were evening-type (22.37% in Italian sample and in Spanish). The Chi-squared test that was carried out provided significant results, indicating that there is a relationship between gender and circadian typology, taking into account both the three ðx 2 2 ¼ 23:16; p, 0:00001Þ and the five ðx2 4 ¼ 31:96; p, 0:00001Þ typologies. In the Italian sample, the results were, respectively, x 2 2 ¼ 11:94 ðp, 0:005Þ and x2 4 ¼ 14:27 ðp, 0:005Þ; in the Spanish x2 2 ¼ 16:68 ðp, 0:0005Þ and x 2 4 ¼ 28:10; ðp, 0:00001Þ: As shown in Table 1, the percentage of evening-type men was greater than that of women, while the percentage of morning-type women was greater than that of men. The percentage of intermediate-type men was slightly lower than that of women. At this point, on the basis of the results obtained, we assume that gender differences as regards MEQ score are the same in both Italian and Spanish samples and so will consider the two samples together. In order to investigate the MEQ dimensions, we used the principal component extraction method, [26] a method in which all the variance of the variables measured contributes to the solution. The most unambiguous and psychologically meaningful factor structure was obtained with varimax rotation. Firstly, data for males and females were analyzed separately in case this important variable influenced factor structure. However, congruency test [27] comparing each factor across sex showed that the factors were essentially the same for both groups. Then considering the whole sample, three factors were extracted based on the eigenvalue-greater-than-one-criterion. The percentage of the variance explained by each factor was as follows: 27.39, 9.00, and 7.04%. According to Comrey, [28] variables with loading higher than 0.71 are considered excellent measures of the factor, 0.63: very good, 0.55: good, 0.45: fair, and 0.32: poor. Only item 8 had a loading below According to Table 2, items 6, 11, 15, 17, 18 ( at what time of day do you think that you reach your feeling best peak? ), and 19, loaded on Factor I. Items 1, 2, 10 ( at what time in the evening do you feel tired and as a result in need of sleep? ), 12, 14, and 16 loaded on Factor II. Items Table 1. Number and Percentage of Men and Women as Function of Circadian Typology Assessed by MEQ in the Whole Sample Circadian Typology Men Women Morning-type 142 (13.64%) 196 (17.91%) Definitely 7 (0.67%) 15 (1.37%) Moderately 135 (12.97%) 181 (16.54%) Neither-type 599 (57.54%) 674 (61.61%) Evening-type 300 (28.82%) 224 (20.47%) Moderately 228 (21.90%) 193 (17.64%) Definitely 72 (6.92%) 31 (2.83%)

6 714 ADAN AND NATALE Table 2. Pattern Matrix of the MEQ with Varimax Rotation in the Whole Sample I II III Item Item Item Item Item Item Item Item Item Item Item Item Item Item Item Item Item Item Item , 4 ( assuming adequate environmental conditions, how easy do you find getting up in the morning? ), 5, 7, 8, 9, and 13 loaded on Factor III. These results are generally in line with previous data. [29,30] We labeled Factor I as time of greatest efficiency, Factor II as sleep time or sleep phase, Factor III as awakening time or sleep inertia. Differences in mean values of answers in each of the items analyzed by the Mann Whitney test and differences in answer distribution analyzed by the Chisquared test are presented in Tables 3 and 4, respectively. As can be seen, 12 of the 19 MEQ items differentiate men from women in both analyses and should therefore be considered more sensitive as regards gender differences. Four of them (4/6 ¼ 66.66%) refer to Factor I (time of greatest efficiency), five (5/6 ¼ 83.33%) to Factor II (sleep time/sleep phase), and only two (3/7 ¼ 42.86%) to Factor III (awakening time/sleep inertia). Women prefer to wake up (item 1) and go to bed (item 2) earlier, since they feel the need for sleep in the evening (item 10) earlier than men and feel more tired at 23:00h. (item 12). Men prefer to go to bed 1 2, or more, hours later (item 8) and wake up later (item 13) when they do not have an engagement the next day, feeling less alert after awakening (item 5). Women also report having an earlier peak time for mental performance (item 11) and time of day for feeling best (item 18), with a lower propensity for physical exercise at 22:00h 23:00h (item 16). They consider themselves to be more morning-types than men (item 19), and locate the five consecutive preferred working hours (item 17) at an earlier juncture than men.

7 GENDER AND MORNINGNESS 715 Table 3. Gender Differences in Mean Values for Each MEQ Item Mean Items of MEQ Men Women Mann Whitney Z ( p, ) 1. Preferred waking hour (0.005) 2. Preferred go-to-bed hour ( ) 3. Dependence on alarm clock (ns) 4. Ease in getting up (ns) 5. Alertness after waking up (0.001) 6. Appetite after waking up (ns) 7. Tiredness after waking up (ns) 8. Difference preferred/usual time to go to bed (0.0005) 9. Desire for physical exercise at 07:00 08:00h (ns) 10. Time in the evening when one needs to sleep ( ) 11. Time of mental performance ( ) 12. Level of tiredness at 23:00h (0.001) 13. Sleep length when going to bed several hours later (0.005) 14. Sleep when remaining awake between 04:00 and 06:00h (ns) 15. Preferred time for hard physical work (0.005) 16. Desire for physical exercise at 22:00 23:00h ( ) 17. Five consecutive preferred working hours (0.001) 18. Time of day of feeling best peak (0.0005) 19. Self-assessment of morning/evening-type ( ) Only four MEQ items proved not to be sensitive to gender differences in the analyses performed. Of these, all of them regarded waking phase or sleep inertia (Factor III). Between 50 and 60% of the subjects claimed to be alarm clock-dependent (item 3), to have little appetite after waking up (item 6), to feel less tired after waking up (item 7), and to have little desire for physical exercise at 07:00 08:00h. (item 9), with no differences between male and female. DISCUSSION We confirm the solid consistency and reliability of MEQ in students with daytime work schedules. [11,12] The distribution of subjects in the different circadian typologies presented in this study is in line with previous population data. [4,5,22] While the Spanish sample displayed a slight bias towards the eveningness category compared to the Italian one, gender differences in the present study proved to be the same in both samples. We consider this a very significant result and therefore feel it right to consider the two samples together in the final discussion on gender differences and circadian typology. The men and women in our study presented different global MEQ scores as well as different circadian typology distributions. Men had lower mean scores

8 716 ADAN AND NATALE Table 4. Gender Distribution per Answer to Each MEQ Item (The Items Have IV or V Possible Response Levels, the Lower Levels Indicating Eveningness and the Higher Ones Morningness) I II III IV V Items of Morningness Eveningness Questionnaire Men Women Men Women Men Women Men Women Men Women Chi-Square ( p, ) 1. Preferred waking hour ( ) 2. Preferred go-to-bed hour ( ) 3. Dependence on alarm clock (ns) 4. Ease in getting up (0.001) 5. Alertness after waking up (0.0005) 6. Appetite after waking up (ns) 7. Tiredness after waking up (ns) 8. Difference preferred/usual time to go to bed (0.001) 9. Desire for physical exercise at 07:00 08:00h (ns) 10. Time in the evening when one needs to sleep ( ) 11. Time of mental performance ( ) 12. Level of tiredness at 23:00h (0.001) 13. Sleep length when going to bed several hours later (0.005) 14. Sleep when remaining awake between 04:00 and 06:00h (0.0001) 15. Preferred time for hard physical work (ns) 16. Desire for physical exercise at 22:00 23:00h ( ) 17. Five consecutive preferred working hours (0.001) 18. Time of day of feeling best peak (0.001) 19. Self-assessment of morning/evening-type ( )

9 GENDER AND MORNINGNESS 717 (more eveningness) as well as a higher percentage of evening-types. These results are similar to those reported by Chelminski et al. [12] and Natale and Adan, [22] although both sets of authors did not study the sensitivity of MEQ items. In the case of Chelminski, the high age range (18 53 yr) made it impossible to discard the effects of this variable. An item by item analysis allowed us to ascertain that 12 items are sensitive to gender difference referring essentially to Factor I (time of greatest efficiency) and Factor II (sleep time/sleep phase). The items that showed no sensitivity to gender difference are prevalently grouped in Factor III (awakening time/sleep inertia). In particular, items 6 and 7 refer to the phenomena of sleep inertia and indicate that men wake up later than women but are not sleepier when they awaken (with the exception of item 5). The differences in the SWC therefore are prevalently in the phase relationship, which was confirmed by cognitive and physical performance items. The existence of gender differences in circadian rhythms has been sometimes interpreted as a product of social cultural influences. [20,21,31] Data have been presented, however, that would seem to be inconsistent with such a hypothesis, pointing to differences under conditions where subjects have been isolated from environmental input. [19] In these conditions, males normally present internal desynchronization earlier than women as though they felt or adapted to the new environmental conditions faster than females. Our results indirectly support the existence of different synchronization patterns for men and women with the environment, as suggested by Natale and Adan. [22] Furthermore, it has been suggested that the phase advance of circadian rhythms in morning-type subjects [14,30 32] and older individuals [5,13,14,33] reflects more sensitivity to the environmental Zeitgeber. Our findings are significant also with reference to the multi-oscillatory model framework. The more recently proposed chronobiological models claim that the circadian system in humans essentially involves two basic endogenous processes: [34] a self-sustained CP, and a SWC homeostatic controller. It is currently thought that neither of the two processes on their own can account for the rhythmic variations in SWC, suggesting a mixture of CP and SWC influences. To improve on this model, [35,36] a third process has been introduced, a process of inertia with regard to the transition from sleep to waking conditions. Our data seem to suggest that men and women do not differ as regards to the inertia process but they do not provide an understanding of whether gender differences are prevalently loaded with CP or SWC process. It has, however, been posited that the interplay of CP and SWC processes would ensure the circadian system has flexibility in the timing of sleep and other rhythmic parameters. From an adaptive point of view, this feature explains the capacity of adjustment to changes in environmental conditions. We believe that the different circadian systems according to gender could stem from a different interplay between CP and SWC processes, which could in turn help make the circadian system in males more flexible and more able to adapt to

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12 720 ADAN AND NATALE 36. Jewett, M.E.; Kronauer, R.E. Interactive Mathematical Models of Subjective Alertness and Cognitive Throughput in Humans. J. Biol. Rhythms 1999, 14, Received September 18, 2001 Returned for revision December 10, 2001 Accepted February 18, 2002