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2000 Martin Dunitz Ltd

International Journal of Psychiatry in Clinical Practice 2000 Volume 4 Pages 63 ± 67

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The relationship between objective sleep variables and subjective sleep estimation in schizophrenia VS ROTENBERG, P INDURSKI, R KIMHI, J HADJEZ, Y GUTMAN, E SHAMIR, Y BARAK AND A ELIZUR Abarbanel Mental Health Center, Tel-Aviv University, Israel

Correspondence Address V.S. Rotenberg, MD, PhD, Senior Lecturer of Tel-Aviv University, The Y. Abarbanel Mental Health Center, 15 Keren Kayemet Str., Bat-Yam, Israel. Tel: 972-3-555263 4 Fax: 972-3-658995 2

Received 15 June 1998; revised 26 March 1999; accepted for publication 26 April 1999

Few investigations of sleep structure in schizophrenia have concentrated on the relationship between objective and subjective sleep variables. The aim of this study was to assess objective sleep variables and subjective estimation of sleep duration and sleep quality. METHODS: Polysomnogr aphy was performed in 20 chronic patients with schizophrenia during three consecutive nights. After final awakenings subjects answered questions concerning subjective estimations of sleep duration, sleep latency, number of awakenings , and sleep depth. Pearson correlations between ranged subjective reports and objective sleep variables were performed. RESULTS: The results showed a high positive correlation between objective sleep latency and its subjective estimation; a positive correlation between subjective estimation of sleep depth and percentage of slow wave sleep (SWS%); a positive correlation between eye movement (EM) density and subjective estimation of wakefulness during the night; and a negative correlation between EM density and dream reports. CONCLUSION: We concluded that objective sleep variables are related to subjective sleep estimation in schizophrenic patients. In these patients, EM activity in REM sleep is related to the subjective feeling of wakefulness. (Int J Psych Clin Pract 2000; 4: 63 ± 67) AIM:

Keywords sleep variables

INTRODUCTION

C

omplaints of sleep disturbance are common in patients with schizophren ia and may relate to the peculiaritie s of their sleep structure. Such relationship s may help to elucidate the functional meaning of different objective sleep alterations in schizophrenia . If some subjective complaints are strongly determined by definite objective sleep variables, such complaints may be used in future as markers of sleep structure. Although there have been several investigation s of sleep structure in schizophrenia, 1 ± 7 only a few included the patient’s subjective estimation of sleep,5 ,6 and even in these investigation s the relationships between objective and subjective sleep variables have not been analysed in a systematic way. Investigation s of relations between subjective and objective (physiologic al) sleep variables in healthy subjects and insomniac patients8 ± 1 0 suggest that subjective sleep estimation is mainly determined by objective sleep latency and wakefulnes s after sleep onset. The role of

subjective estimation

schizophrenia

sleep stages in sleep estimation is less definite. Only a few studies have found subjective sleep quality to be directly related to slow wave sleep (SWS) or rapid eye movement (REM) sleep.8 ,1 0,1 1 A recent systematic investigatio n which used short sleep episodes1 2 showed, by mean of multiple regressio n analysis, that in healthy subjects subjective sleep quality was predicted by total sleep time and slow wave sleep. It was also shown that, although objective sleep latency correlated with subjective ease of falling asleep, when subjective sleep latency is measured in minutes it is an overestimate of physiologica l sleep latency. It is unknown whether the same relationship s between the objective and subjective sleep variables are relevant in patients with schizophreni a. The aim of the present investigatio n was to assess objective sleep variables and subjective estimation of sleep duration and sleep quality. Our preliminar y hypothesi s predicted that subjective estimation of depth of sleep in patients with schizophreni a would be determined by the amount of SWS, while

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subjective estimation of sleep duration correlates negatively with awakenings during sleep.

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MATERIAL AND METHOD We investigated 20 patients with chronic schizophren ia (13 men, 7 women; mean age 45.8, range 28 ± 72 years). The diagnosi s was based on DSM-IV criteria: 11 patients had paranoid type, five had residual type, three had disorganize d type, and one had the schizo-affec tive type. The duration of illness ranged from 11 to 39 years (mean 21.6). Evaluation with the PANSS rating scale was performed to evaluate the severity of positive and negative features.1 3 The mean level of positive symptoms for the group was 17.116 7.5 while the mean score for negative symptoms was 28.756 5.2. All patients were free from medical problems, and were taking neuroleptic medication (equivalen t to haloperidol 15 mg/ day), treatment being unchanged during 60 days prior to polysomnogr aphy. Hypnotic medication was stopped at least 2 weeks before polysomnogr aphy. The control group contained 10 healthy subjects (six men, four women; mean age 43.3 years) without any complaints of sleep disturbance, and without medical problems. All patients gave informed consent to participate in the study. Sleep data were collected from all patients on three consecutive nights and from control subjects on two consecutive nights in a sleep laboratory. Lights were usually turned off between 10.00 and 10.30 pm and turned on between 6.00 and 6.30 am, according to the typical schedule in the ward. Electroencephalograms (EEG), submental electromyogr ams (EMG) and electro-oculograms (EOG) for EM registration were recorded using an electroenceph alograph Neurofax EEG-4400. The EEG and EOG were recorded at a low filter setting of 0.3 Hz. Polysomnogr ams were analysed according to international criteria.1 4 Sleep onset was defined as the first minute of stage I followed by at least 10 min of this stage, not interrupted by awakenings . REM sleep latency was defined as the time from onset of sleep until onset of the first REM sleep period, including intervening awake time. Eye movements (EM) in REM sleep were counted visually. The criterion for EM detection was a minimum of 25 mV.4 EM density was counted as EM frequency per minute of stage REM. Fragments of wakefulnes s or non-REM sleep occurring within a single REM period were not analysed for EM activity, and were not included in the REM period length when we computed a net EM/REM period variability . The minimum of REM sleep duration was defined as being 1 minute. Each morning, every subject, after final awakening in the laboratory, was requested to answer questions concerning their subjective feelings about sleep duration, sleep latency, number of awakenings , sleep depth and the state after sleep (mood, refreshment ); the possible answers were ranged, in order to compute correlations between subjective and objective variables (see Appendix). This questionnair e was used in our investigatio n of patients with major depres-

sion, 1 5 ,1 6 in which we found that in patients with the `first night’ effect (who are sensitive to antidepressan ts), SWS determined positive estimation of sleep duration, and also a feeling of being refreshed after sleep. Thus, the results of our investigatio n while using this questionnair e are similar to the results of earlier investigatio ns (a positive role of SWS in sleep estimation), and confirm the validit y of the questionnair e.

STATISTICAL ANALYSIS One-way analysis of variance (ANOVA) was used for sleep variables in patients and controls. If the ANOVA was found to be significan t (at the 0.05 level), it was followed by the paired Student’s t-test in order to compare sleep variables in both groups. Pearson product ± moment correlations have been used for estimation of relationship s between objective and subjective sleep variables. We selected those objective sleep variables which, according to the previous investigations, 1 1 ,1 2 seemed to correspond to subjective variables. Thus, we correlated the subjective estimation of sleep duration with the objective sleep duration, with sleep efficiency , with SWS%, REM%, sleep latency and number of awakenings . Subjective sleep latency was correlated with objective sleep latency, total sleep duration, SWS and REM sleep in the first cycle, REM latency, and with EM density in the first REM sleep period. Subjective estimation of sleep depth was correlated with objective sleep duration, sleep efficiency , SWS%, REM%, SWS and REM duration and EM density in all cycles. Subjective estimation of awakenings during the night was correlated with the objective number of awakenings , EM density, REM sleep duration in different cycles, and sleep efficiency . In order to increase the importance of the selected correlations , an additional procedure was performed: a) selection of the extreme (minimal and maximal) indices of subjective sleep variables (sleep latency, depth of sleep etc.); b) calculation of mean data and standard deviation of objective sleep variables (sleep latency, SWS% etc.) which correspond to the extreme indices of subjective sleep variables; c) the mean data of objective sleep variables which correspond to the minimal and maximal indices of the subjective sleep variables were compared using Student’s ttest, and if a differenc e was significan t (P > 0.05), the correlation between the correspondin g subjective and objective sleep variables was used for discussion .

RESULTS Sleep variables for patients with schizophreni a and healthy subjects are presented in Table 1. The main difference between the groups is in sleep latency and its deviation (which are relatively higher in the patients) and in REM sleep variables (duration of first REM sleep period and eye movement density in the first two cycles are greater in the patients) (Figure 1).

Sleep in schizophrenia

ESTIMATION OF SLEEP LATENCY The positive correlation between objective sleep latency and its subjective estimation was high in patients, being 0.83 (P < 0.01): in healthy subjects this correlation was absent. In patients, subjective estimation of

sleep latency correlated negatively with objective sleep duration (for all nights this correlation was Ð 0.72; P < 0.02), which confirms the correlation mentioned above, because increased sleep latency decreases total duration of sleep if the time of final awakening is fixed.

Table 1 Sleep variables in healthy controls and schizophrenic patients Controls (n=10)

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Groups No. of nights Total sleep time, min Sleep efficiency, % Sleep latency, min

20 412 (43) 98 (3) 3.3 (2.1)***

Patients (n=20) 58 413 (74) 92 (11) 32 (69)***

Slow wave sleep, % SWS, cycle 1, min SWS, cycle 2, min SWS, cycle 3, min SWS, cycle 4, min

14.5 26.2 22.6 6.6 4.8

(6.8) (12.3) (13.2) (8.7) (8.6)

16.3 23.7 23.7 9.7 7.1

(10.1) (18.8) (18.4) (12.7) (11.7)

REM sleep latency, min REM sleep, % REM, cycle 1, min REM, cycle 2, min REM, cycle 3, min REM, cycle 4, min

89.4 19.3 7.9 19.7 22.4 23.0

(33.7) (3.7) (4.5)**** (9.5) (11.5) (12.3)

93.4 22.7 19.2 28.3 23.7 24.7

(6.10) (8.0) (14.0)**** (19.2) (16.0) (14.6)

2.0 3.8 5.1 5.4

(2.3)**** (1.9)** (2.6) (3.2)

5.2 5.4 5.1 4.7

(4.8)**** (3.5)** (2.9) (2.6)

EM EM EM EM

density, density, density, density,

Awakening

cycle cycle cycle cycle

1 2 3 4

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1.0 (1.0)*

****P < 0.001; ***P < 0.01; **P < 0.02; *P < 0.05 (in brackets ± standard deviations)

Figure 1 A typical sleep structure of the schizophrenic patient, a) comparison with normal sleep variables, b) sleep structure

1.8 (2.0)*

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ESTIMATION OF SLEEP DEPTH The estimation by patients of sleep depth in the first half of the night correlated in all nights with the duration of slow wave sleep in the first cycle (0.42, P < 0.05) and in the third cycle (0.33, P < 0.05). The positive role of slow wave sleep in estimation of sleep depth was indirectly confirmed by a positive correlation between the feeling of being refreshed and SWS in the third cycle (0.30, P < 0.05). In healthy subjects SWS does not correlate with sleep depth (possibly because the deviation of sleep depth reports in healthy subjets was small), but SWS in the second cycle correlated positively with the estimation of sleep duration (0.57, P < 0.05), and SWS% correlated negatively with the subjective estimation of sleep delay ( Ð 0.59, P < 0.05).

ESTIMATION OF THE DURATION OF WAKEFULNESS Patients display a positive correlation between estimation of the duration of wakefulnes s during the night and EM density in the fourth cycle (0.60, P < 0.01). In healthy subjects, subjective estimation of the duration of wakefulness incorporated in sleep correlates negatively with sleep efficiency ( Ð 0.66, P < 0.05) and positivel y with objective duration of wakefulnes s (0.57, P < 0.05).

the type of mental disorder. In patients with chronic schizophreni a subjective estimation of the duration of wakefulnes s in sleep correlated with eye movement density in REM sleep. The same correlation was found in depresse d patients.1 6 High eye movement density reflects physiologica l arousal,1 7 ,1 8 which might be subjectivel y estimated as wakefulness . However, in healthy subjects such correlatio n is absent. According to previous investigation s in healthy subjects,1 9,2 0 eye movement density correlates with some features of dream reports. As there are fewer reports of dreams in REM sleep in mentally ill patients than in healthy subjects,2 0 ,21 it is possible to suggest that psychiatric patients perceive mental activity in REM sleep as wakefulness ; this suggestio n is indirectly confirmed by the negative correlation between EM density and dream reports. If dream experience is related to psychologica l adaptation,2 1 ± 2 3 our findings may be interpreted as a sign of the functional insufficienc y of REM sleep in patients.2 0 Healthy subjects, according to the present investigation , are able to perceive correctly the duration of wakefulnes s incorporated in sleep. While SWS plays the same role in sleep in schizophrenic patients as in other patients and healthy subjects, the estimation of sleep quality and eye movement activity in REM sleep in schizophreni a is related to the subjective feeling of wakefulness .

DISCUSSION An unexpected result of the present investigatio n is the ability of patients with schizophreni a to estimate correctly the duration of wakefulnes s before sleep onset. The correlation between objective and subjective sleep latency in these patients is higher than in healthy subjects. 1 2 Correct estimation of sleep delay is absent in our healthy subjects, as well as in patients with major depression.1 6 In healthy subjects and patients with mood disorder s the duration of wakefulnes s before sleep onset is possibly overestimated, because sleep delay causes emotional tension, which may interfere with the subject’s ability to estimate it correctly: in chronic schizophren ic patients with blunted affect, alteration of sleep onset does not cause any emotional reaction and its subjective estimation is not distorted. The positive correlation between SWS% and subjective estimation of sleep depth confirms an earlier investigatio n1 2 and our previous findings in neurotic patients;1 1 SWS determines the subjective evaluation of sleep regardless of

KEY POINTS

· · · ·

Complaints of schizophreni c patients about sleep delay have usually objective confirmation in the increased sleep latency Complaints of schizophreni c patients about insufficien t sleep depth have objective confirmation in SWS deficiency . In most cases such complaints must not be dismisse d as the `absence of the sleep sense’ or as a delusion In patients with schizophreni a, complaints about awakenings in sleep are often determined by the functional deficiency of REM sleep, and can be used as an indirect sign of the REM sleep quality Subjective estimation of sleep by schizophren ic patients may be used as a sign of objective alteration of sleep structure in the course of illness and in the process of treatment

REFERENCES 1. Tandon R, Shipley JE, Taylor J et al (1992) Electroencephalographic sleep abnormalities in schizophrenia. Relationships to positive/negative symptoms and prior neuroleptic treatment. Arch Gen Psychiatry 49: 185 ± 194.

2. Neylan TC, VanKammen DP, Kelley ME, Peters JL (1992) Sleep in schizophrenic patients on and off haloperidol therapy. Arch Gen Psychiatry 49: 643 ± 9.

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Sleep in schizophrenia

3. Hudson JI, Lipinsky JF, Keck PE et al (1993) Polysomnographic characteristics of schizophrenia in comparison with mania and depression. Biol Psychiatry 34: 191 ± 3. 4. Benson KL, Zarcone VP (1993) Rapid eye movement sleep eye movements in schizophrenia and depression. Arch Gen Psychiatry 50: 474 ± 82. 5. Kajimura N, Kato M, Okuma T, Onuma T (1994) Effects of Zopiclone on sleep and symptoms in schizophrenia: comparison with benzodiazepine hypnotics. Prog Neuropsychoph armacol Biol Psychiatry 18: 477 ± 90. 6. Kajimura N, Kato M, Okuma T et al (1995) A quantitative sleep EEG study on the effects of benzodiazepine and Zopiclone in schizophrenic patients. Schizophr Res 15: 303 ± 312. 7. Keshavan MS, Pettegrew JW, Reynolds CF et al (1995) Biological correlates of slow wave sleep deficits in functional psychoses: 31-P magnetic resonance spectroscopy. Psychiatry Res 57: 91 ± 100. 8. Mendelson WB, Garnett D, Gillin JC, Weingartner H (1984) The experience of insomnia and daytime and nighttime functioning. Psychiatry Res 12: 235 ± 50. 9. Baekeland F, Hoy P (1971) Reported vs. recorded sleep characteristics. Arch Gen Psychiatry 24: 548 ± 51. 10. Kryger MH, Steltjes D, Pouliot Z et al (1991) Subjective vs. objective evaluation of hypnotic efficacy: experience with Zolpidem. Sleep 14: 399 ± 407. 11. Rotenberg VS (1993) The estimation of sleep quality in different stages and sleep cycles. J Sleep Res 2: 17 ± 20. 12. Akerstedt T, Hume K, Minors D, Waterhouse J (1997) Good sleep ± its timing and physiological sleep characteristics. J Sleep Res 6: 221 ± 9. 13. Kay SR, Fiszbein A, Opler IA (1987) The positive and negative syndrome scale (PANSS) for schizophrenia. Schizophr Bull 13: 261 ± 76.

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14. Rechtschaffen A, Kales A (ed) (1968) A manual of standardized terminology, techniques and scoring system for sleep stages of human subjects, 204. National Institute of Health, N.I.H. Public, Washington, DC. 15. Rotenberg VS, Kayumov L, Indursky P et al (1997) REM sleep in depressed patients: Different attempts to achieve adaptation. J Psychosom Res 42: 565 ± 75. 16. Rotenberg VS, Kobrin V, Indursky P et al (1997) Subjective ± objective relationships in sleep (abstracts). 14th World Congress on Psychosomatic Medicine, Cairns, Australia. 17. Perlis ML, Giles DE, Fleming GM et al (1995) Sustained facial muscle activity during REM sleep and its correlation with depression. J Affect Disord 35: 163 ± 71. 18. Perlis ML, Giles DE, Buysse DJ et al (1997) Which depressive symptoms are related to which sleep electroencephalographic variables? Biol Psychiatr 42: 904 ± 13. 19. Herman JH, Erman M, Boys R et al (1984) Evidence for a directional correspondence between eye movements and dream imagery in REM sleep. Sleep 7: 52 ± 63. 20. Rotenberg VS (1988) Functional deficiency of REM sleep and its role in the pathogenesis of neurotic and psychosomatic disturbances. Pavlov J Biol Sci 23: 1 ± 3. 21. Greenberg R, Pearlman Ch (1974) Cutting the REM sleep nerve: an approach to the adaptive role of REM sleep. Persp Biol Med 17: 513 ± 21. 22. Rotenberg VS (1993) REM sleep and dreams as mechanisms of the recovery of search activity. In The functions of dreaming (ed A Moffitt, M Kramer, R Hoffmann) 261 ± 262. State University of New York Press, New York, NY. 23. Rotenberg VS (1992) Sleep and memory II: Investigations on humans. Neurosci Biobehavioral Rev 16: 503 ± 5.

Appendix: Sleep questionnaire 1. How long have you slept?

> 9 hours; 8‰ hours; 8 hours; 7‰ hours; 7 hours; 6‰ hours; 6 hours; 5‰ hours; 5 hours; < 5 hours; no sleep at all

2. How long did it take you to fall asleep?

> 1 hour; 1 hour; 50 min; 40 min; 30 min; 20 min; 10 min; 5 min; < 5 min

3. How many awakenings have you during sleep?

0; 1; 2; 3; more than 3

4. How long did it take you to go back to sleep after each awakening?

< 1 min; 1 ± 5 min; 6 ± 10 min; 11 ± 20 min; > 20 min (Please specify to which awakening ± first, second, etc ± the duration of wakefulness belongs)

5. Are you refreshed after sleep?

Totally; partly; not refreshed

6. Was your sleep in the first part of the night:

Deep? moderate? superficial?

7. Was your sleep in the second part of the night:

Deep? moderate? superficial?

8. Have you experienced dreams during your sleep?

Yes; No

9. Do you remember some of your dreams?

Yes; No

10. Your dreams were predominantly:

Pleasant? neutral? unpleasant? frightening?

The relationship between objective sleep variables and subjective sleep estimation in schizophrenia.

Few investigations of sleep structure in schizophrenia have concentrated on the relationship between objective and subjective sleep variables. The aim...
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