It is important to determine the consequences of age-related changes in all aspects of life in order to develop new strategies to help older individuals cope with sleep-wake cycle regularity challenges.
The commonality of sleep problems among older adults is now well established. According to the National Sleep Foundation Survey conducted in 1991, 36% of the population reported a current sleep problem, with those over the age of 65 suffering more from chronic insomnia than any other age group.1 In 1995, a National Institute on Aging study of more than 9,000 individuals aged 65 years and older showed that more than half of the men and women reported at least one chronic sleep complaint.2 Many factors may interfere with optimal sleep and wakefulness in older adults and explain a significant proportion of this age-related increase in sleep difficulties. Acute and chronic illness, the side effects of medication, mental health conditions, primary sleep disorders, and abrupt, uncontrollable changes in social and personal life may all contribute to the development of sleep difficulties in the elderly. Considerable modifications of the sleep-wake cycle also occur in “optimal aging” (in individuals free of any medical or psychiatric condition and who do not present with specific sleep disorders). The literature now shows that some of these age-related changes occur as early as the middle years of life.3
Fundamental and clinical research on sleep in aging has grown rapidly over the past decades, with important progress in the development of descriptive studies that characterize age-related sleep modifications over the life span; however, research on sleep in aging still faces important challenges. First, a better understanding of the mechanisms underlying age-related sleep modifications is necessary and it requires a greater investment of research time and energy. This line of inquiry should involve fundamental human and animal research. Second, it is important to identify factors that may increase the vulnerability of the aging sleep-wake system to disturbances. These factors might include gender, menopause, stress, stimulant consumption, and psychiatric disorders. In addition, the consequences of age-related modifications to the sleep-wake cycle demand more thorough evaluation. These should include not only vigilance but also all functions to which evidence suggests that sleep makes a significant contribution (cognition, immune functions, mood regulation, and hormonal regulation). Finally, the development of preventive and therapeutic strategies to help the aging population cope with their sleep-wake cycle difficulties ought to be a research priority.
Sleep in Normal Aging
Many objective measures of habitual sleep patterns and polysomnographic recordings support the notion that a number of subjective sleep and alertness complaints are more frequent in the elderly than in younger individuals. Thus, empirical data comply with reports in common folklore that elderly individuals go to bed and get up earlier than they did when they were young.4 Their bedtime and wake time are advanced by about 1 hour, which is a common complaint among the elderly. Their sleep is also less consolidated than that of the young. They experience more nighttime awakenings, especially in the second half of the night,5 along with an increased number of microarousals.6 An increase in daytime sleep episodes accompanies this reduction in nighttime sleep duration. The sleep-wake cycle of elderly persons is thus fragmented, with interrupted nighttime sleep and naps intruding on daytime wakefulness. Furthermore, polysomnographic recordings indicate a reduction in slow wave sleep (SWS)—stages 3 and 4, also referred to as deep sleep—and in slow wave activity (SWA)—spectral power between 0.75 Hz and 4.75 Hz. Rapid eye movement (REM) sleep seems to be preserved with age, although in greater proportions in the first half of the night among elderly individuals than among young ones.
The mechanisms underlying normal age-related sleep modifications are still unknown. With the ever-increasing proportion of the population advancing in age and suffering from the potentially crippling impact of sleep difficulties, this issue is of more than academic importance. The model of sleep-wake regulation first elaborated by Borbely in 1982 is one of the most widely accepted.7 This model of sleep regulation incorporates two interacting processes: a homeostatic process (process S) and a circadian process (process C). A precise interaction between these two processes is essential for optimal wakefulness and consolidated sleep episodes. Process S represents the accumulation of sleep pressure with increasing time awake, followed by its dissipation during a sleep episode. The intensity and the dynamics of SWA during non-REM sleep evaluate the time course of Process S. Both SWS and SWA have been shown to increase after an extension of prior wakefulness.8 Using different wake duration intervals prior to a sleep episode, it was established that SWA increases in relation to the number of hours of wakefulness accumulated according to a saturating exponential function. Process C represents the rhythmic variation of the wake and sleep propensity over a 24-hour period. This rhythmic variation might be controlled by an endogenous biological clock located in the suprachiasmatic nucleus of the hypothalamus. There is a strong association between the signal from the biological clock and sleep. For example, circadian sleep propensity rises on the falling limb of core body temperature (in the late evening) and circadian wake propensity gradually intensifies on the rising limb of core body temperature (in the early morning hours).
A number of hypotheses using the Two-Process sleep regulation model have been proposed to explain the sleep-wake modifications that occur with aging. These hypotheses include a phase advance or a diminution of the strength of the signal from the biological clock, a reduction of the endogenous period of the biological clock, alterations to the homeostatic regulation of sleep, increased vulnerability to a phase angle disturbance between the biological clock and the sleep-wake cycle, higher rigidity of the circadian system to phase shift, and reduction in the strength of zeitgebers. Of course, these hypotheses are not mutually exclusive and more than one of these processes may be responsible for age-related deterioration of the sleep-wake cycle.
Although contemporary studies are now testing many of these hypotheses, much more research is needed to confirm or rule out propositions of this nature as well as to understand underlying mechanisms. For example, the phase advance hypothesis of the circadian signal has been able to predict age-related changes in the timing of the sleep-wake cycle. According to this hypothesis, the phase advance would produce an earlier timing of the episode of high sleep propensity in the evening and an earlier circadian wake signal in the morning. Although many studies9,10 have demonstrated a phase advance in the circadian system, the underlying mechanisms have yet to be clarified. Other authors have suggested that the sleep of older subjects might be particularly vulnerable to circadian phases of high wake propensity, which means that it would be more difficult for older people to sleep at the “wrong” circadian phase. Even though the increasing number of complaints among elderly people concerning shift work and jet lag subjectively confirms this idea, some objective studies in the laboratory also confirm that elderly and middle-aged subjects have more problems maintaining sleep when the biological clock sends a strong wake signal, as it does during daytime.11 The results of studies of sleep deprivation in older subjects have indicated that despite an increase in SWS during the recuperative sleep episode, the rebound of SWS is usually less intense than in young subjects.12,13 This may represent an alteration of the buildup function of the homeostatic sleep pressure. Although no evaluation of a changed buildup function is available, it is possible that the buildup function of the homeostatic sleep process is attenuated with increasing age.
In conclusion, the mechanisms that spur the major age-related decrease in sleep consolidation, the marked diminution of SWS and SWA during baseline sleep, the lower rebound of SWS and SWA following an acute sleep deprivation, and the lower tolerance to a phase angle misalignment between sleep and the circadian signal are still unknown. Future animal and human research must focus on these mechanisms in order to define a new target for prevention and intervention.
Factors of Vulnerability
Many variables have been proposed as potentially significant contributors to the increase in vulnerability of the aging sleep-wake system to disturbances. These include gender, menopause, stress, stimulant consumption, and medical or psychiatric conditions. Much more research is needed to understand their actual role in the sleep problems that accompany aging and their potential mutual interactions. For example, caffeine is the most widely used central nervous system stimulant in North America and older individuals regularly consume it; however, very few studies have investigated its effects on sleep in aging. Some studies suggest that caffeine may lead to more important disruption of sleep in elderly than in young subjects.14,15 Furthermore, although the effects of caffeine on habitual sleep in young subjects are well documented, there is a paucity of available information about the interaction between sleep deprivation, circadian timing, and caffeine administration.
The interrelationships between health and sleep are of great importance for the elderly. Yet the extent to which declining physical and mental health has an impact on sleep quality in older individuals is unclear and has been for many years.16 Primary sleep disorders such as sleep-disordered breathing, periodic leg movement disorder, and restless legs syndrome are more common in the elderly than in younger persons; however, acute and chronic illnesses, other than primary sleep disorders, may also precipitate sleep disruption. In fact, older subjects with newly identified significant illnesses are 80% to 100% more likely to have an emergent complaint of chronic insomnia within 3 years than are older individuals who do not develop such medical illnesses.17 Cardiovascular diseases, pulmonary diseases, and chronic pain conditions are all associated with morning fatigue and/or daytime sleepiness and are also a cause of poor nocturnal sleep quality. Psychiatric disorders also have acute symptoms that might contribute to sleep difficulties. For example, the association between major depression and insomnia is now well established. Finally, elderly individuals frequently take medication. Advanced age and frailty may increase their susceptibility to the adverse effects of medication.
Henceforth, gender and menopausal status are factors that impact sleep parameters and need to become the focus of studies instead of being controlled or ignored. Many researchers have tried to find answers to various sleep questions but mostly studied young, healthy males. In the attempt to extend the literature to include both genders, the sleep research community must face methodological challenges presented by factors unique to women. In their willful blindness to these factors, researchers have studied women in different phases of their menstrual cycle; women who were taking contraceptive pills, along with those who were not; pre-, peri-, and post-menopausal women; and women receiving hormonal replacement therapy, as well as those who were not—all without any methodological or theoretical distinction. This has led to inconsistent findings. Although the literature on gender differences in the later years of life is scarce, subjective complaints sometimes differ significantly between older men and women. Compared to older men, older women seek more medical help for their sleep problems and report poorer sleep quality, more difficulty falling asleep, more nighttime awakenings, less frequent napping, and more frequent use of sedative-hypnotic drugs. In a recent study of women that featured a 24-year follow-up, sleep decreased in all cohorts between the ages of 38 and 66 and sleep problems increased with age, reaching 50% in 84-year-old women18; however, explanations for the preponderance of subjective sleep complaints in elderly women (compared to elderly men) have still not been conclusive. In fact, objective assessments of healthy older women indicate more SWS and fewer awakenings relative to older men, which would imply fewer sleep difficulties. It is not clear when these polysomnographic gender differences appear in the aging process. A study of 100 men and women between the ages of 20 and 60 showed no significant interaction between age and gender, suggesting that aging has no differential effect on men and women in this age range.3 More controlled studies are needed to establish these differences and to understand the influence of hormonal status on gender differences.
Between 47% and 64% of menopausal women complain about their sleep and half of them complain about significant fatigue during daytime hours.19 Peri- and post-menopausal women are twice as inclined as premenopausal women are to use sleeping pills, as they sleep less and suffer more often from insomnia symptoms.20 However, very few studies have evaluated the effect of menopausal status on objective sleep parameters and others have shown inconsistent results. Evidently, more studies are needed to define and understand the factors associated with sleep quality in peri- and post-menopausal women. The importance of vasomotor symptoms such as night sweats and hot flashes remains undetermined, but they also seem to play a role in the subjective complaints of women. Finally, the effects of hormonal therapy in menopausal women on polysomnographic sleep parameters require clarification.
Several other factors, such as stress and socioeconomic status, have been proposed to significantly increase the vulnerability of the sleep-wake cycle to the effects of aging. Future theoretical models of the effects of age on sleep should incorporate these factors as well as their interactions with sleep-wake cycle regulatory processes.
It is fundamental to know if age-related changes in sleep reflect a reduction in need for sleep or a reduction in sleep ability (the inability to generate sleep). Age-related modifications may or may not have negative consequences for the elderly. It is possible that aging is associated with a reduced need for sleep. Stated differently, less sleep would be necessary as the person increases in age. To test this hypothesis, we must evaluate the consequences of age-related modifications to the sleep-wake cycle on all physical and psychological functions in which sleep plays a significant role (vigilance, cognition, brain plasticity, mood regulation, hormonal regulation, and immune system).
It is also possible that age-related changes in the sleep-wake cycle have negative effects on the daily lives of elderly individuals. A recent study demonstrated a strong association between reports of frequent sleep difficulties and a decrease in health-related quality of life.21 The elderly participants who reported the greatest number of sleep complaints also reported less energy, more physical or emotional health problems that forced them to limit their work or leisure activities, and more bodily pain. Furthermore, the effects of age-related attenuation of SWS/SWA on diurnal cognitive performance is still unclear. Although a strong inverse relation has been found between SWS and subsequent diurnal reaction time in young subjects,22 the restorative role of SWS (at least in simple neurocognitive functions such as reaction time) may diminish across the life span.23 On the other hand, a recent study demonstrated a close relation between an objective good night’s sleep and good cognitive performance in elderly individuals who regularly slept well.24 A better understanding of the effects of age-related changes in sleep parameters is important not only for a more solid comprehension of the interrelation itself, but also in terms of treatment planning, implementation, and evaluation. A multidisciplinary collaboration between experts in the field of sleep, psychology, neuropsychology, psychiatry, endocrinology, and neurology is necessary to achieve this goal.
Preventive and Therapeutic Strategies
According to epidemiological studies, 12% to 25% of individuals aged 65 and over complain of insomnia on a regular basis25 and pharmacotherapy—mostly sedative medications such as benzodiazepines (BZs)—remains the most frequently used treatment for elderly sufferers of insomnia. BZs are administered because, in the short term, they reduce sleep latency as well as the frequency and length of awakenings during the night. They also increase total sleep time and its quality; however, they lighten sleep (more time spent in stage 2) and reduce the time spent in REM sleep and deep sleep, which is counterintuitive in terms of sleep characteristics in the older population. They also have undesirable side effects such as dependence, daytime sleepiness, sedation, and anterograde amnesia.26 It is now crucial to question the actual efficacy of BZs in improving sleep and daytime performance. It will be necessary to compare the efficacy for older individuals of pharmacological and nonpharmacological treatments of insomnia, along with their potential side effects. Even though BZs may be effective for short-term treatment of insomnia, cognitive-behavioral sleep interventions (including sleep restriction and modification of bad sleeping habits and of false beliefs surrounding sleep) are also effective for older adults and are less likely to have undesirable effects. A newly formed behavioral sleep medicine section of the American Academy of Sleep Medicine will most certainly improve knowledge about nonpharmacological treatments and expand the understanding and appreciation of behavioral approaches to medical diseases.
Based on our novel understanding of some of the mechanisms underlying age-related changes in the sleep-wake cycle, some experimental therapeutic measures have been developed that target these age-altered mechanisms specifically. For example, evening phototherapy (timed bright light exposure) appears to have probable therapeutic efficacy in the treatment of age-dependent modifications to the sleep-wake cycle, especially early morning awakenings and sleep fragmentation. Bright light exposure in the evening has been shown to phase delay the circadian signal in older subjects.27 Furthermore, the results of a study of elderly subjects with sleep maintenance insomnia pointed out that evening bright light exposure increases polysomnographic sleep efficiency and enhances daytime performance.28 While light may have a significant therapeutic effect, many variables still need further elucidation. These include the optimal duration and intensity of effective light treatment, the population for whom it will be most beneficial, the long-term efficacy of this treatment, and the possibility of tolerance. Some have suggested melatonin replacement therapy for the improvement of nighttime sleep in older individuals following the finding of a decrease in melatonin levels with increasing age.29 Although there is evidence that melatonin administration decreases sleep latency, its effect on polysomnographic sleep efficiency is still ambiguous. The factors associated with the efficacy of this treatment in the later years of life are still obscure and many theoretical questions remain. Other therapeutic interventions that target directly the mechanisms underlying age-related sleep-wake modifications are also in experimental development. For example, preliminary work to test the ability of a pharmacological agent to increase SWS in older populations (SWS boosters) is under way.
Finally, prevention is an essentially unexplored territory in the sleep domain; however, preventive efforts may be beneficial when implemented soon after elderly persons receive the diagnosis of a medical condition or a psychological disorder known to affect sleep. Preventive efforts could take the form of early education and training in behavioral sleep techniques such as stimulus control, relaxation, sleep hygiene, and sleep restriction. It may also be important to offer in-home treatment for this population.30
Conclusion
Important age-related modifications to the sleep-wake cycle are now well described in the literature; however, much needs to be done to comprehend the underlying mechanisms that introduce these changes across the life span. The elaboration of effective preventive and therapeutic strategies for the older population depends on our understanding of these mechanisms. Future research will need to help identify vulnerability factors that put older individuals at risk of suffering from sleep-wake cycle disturbances. It is also crucial to determine the consequences of these age-related changes on all aspects of life, with the ultimate goals of developing new strategies to help older individuals cope with sleep-wake cycle regularity challenges and identifying new pharmacological and nonpharmacological treatments for insomnia in this age range.
Caroline Drapeau, BSc, is a doctoral candidate and Julie Carrier, PhD, is assistant professor, Department of Psychology, University of Montreal, and the Centre d’etude du sommeil et des rythmes biologiques, Hopital du Sacre-Coeur de Montreal, Quebec, Canada.
References
1. Ancoli-Israel S, Roth T. Characteristics of insomnia in the United States: results of the 1991 National Sleep Foundation survey. Sleep. 1999;22:S347-S353.
2. Foley DJ, Monjan AA, Brown SL, Simonsick EM, Wallace RB, Blazer DG. Sleep complaints among elderly persons: an epidemiologic study of three communities. Sleep. 1995;18:425-432.
3. Carrier J, Monk TH, Buysse DJ, Kupfer DJ. Sleep and morningness-eveningness in the “middle” years of life (20-59 y). J Sleep Res. 1997;6:230-237.
4. Weitzman ED, Moline ML, Czeisler CA, Zimmerman JC. Chronobiology of aging: temperature, sleep-wake rhythms and entrainment. Neurobiol Aging. 1982;3:299-309.
5. Feinberg I. Changes in sleep cycle patterns with age. J Psychiatr Res. 1974;10:283-306.
6. Boselli M, Parrino L, Smerieri A, Terzano MG. Effect of age on EEG arousal on normal sleep. Sleep. 1998;21:531-357.
7. Borbely AA. A two-process model of sleep regulation. Hum Neurobiol. 1982;1:195-204.
8. Achermann P, Dijk DJ, Brunner DP, Borbely AA. A model of human sleep homeostasis based on EEG slow-wave activity: quantitative comparison of data and simulations. Brain Res Bull. 1993;31:97-113.
9. Myers BL, Badia P. Changes in circadian rhythms and sleep quality with aging: mechanisms and interventions. Neurosci Biobehav Rev. 1995;19:553-571.
10. Brock MA. Chronobiology and aging. J Am Geriatr Soc. 1991;39:74-91.
11. Dijk DJ, Duffy JF, Czeisler CA. Age-related increase in awakenings: impaired consolidation of nonREM sleep at all circadian phases. Sleep. 2001;24:565-577.
12. Bonnet MH, Rosa RR. Sleep and performance in young adults and older normals and insomniacs during acute sleep loss and recovery. Biol Psychol. 1987;25:153-172.
13. Carskadon MA, Dement WC. Sleep loss in elderly volunteers. Sleep. 1985;8:207-221.
14. Brezinova V. Effects of caffeine on sleep: EEG study in late middle age people. Br J Clin Pharmacol. 1974;1:203-208.
15. Swift CG, Tiplady B. The effects of age on the response to caffeine. Psychopharmacology. 1988;94:29-31.
16. Vitiello MV, Moe KE, Prinz PN. Sleep complaints cosegregate with illness in older adults. Clinical research informed by and informing epidemiological studies of sleep. J Psychosom Res. 2002;53:555-559.
17. Foley DJ, Monjan AA, Brown SL, Simonsick EM, Walace RB, Blazer DG. Sleep complaints among older persons: an epidemiological study of three communities. Sleep. 1995;18:425-432.
18. Björkelund C, Bengtsson C, Lissner L, Rödström K. Women’s sleep: longitudinal changes and secular trends in a 24-year perspective. Results of the population study of women in Gothenburg, Sweden. Sleep. 2002;25:53-55.
19. Ledesert B, Ringa V, Breart G. Menopause and perceived health status among the women of the French GAZEL cohort. Maturitas. 1995;20:113-120.
20. Women and Sleep Poll. Washington, DC: National Sleep Foundation; 1998.
21. Shubert CR, Cruickshanks KJ, Dalton DS, Klein BEK, Klein R, Nondahl DM. Prevalence of sleep problems and quality of life in an older population. Sleep. 2002;25:48-52.
22. Jurado JL, Luna Villegas G, Buela-Casal G. Normal human subjects with slow reaction times and larger time estimations after waking have diminished delta sleep. Electroencephalogr Clin Neurophysiol. 1989;73:124-128.
23. Edinger JD, Glenn DM, Bastian LA, Marsh GR. Slow-wave sleep and waking cognitive performance II: findings among middle-aged adults with and without insomnia complaints. Physiol Behav. 2000;70:127-134.
24. Bastien CH, Fortier-Brochu E, Rioux I, LeBlanc M, Daley M, Morin CM. Cognitive performance and sleep quality in the elderly suffering from chronic insomnia. Relationship between objective and subjective measures. J Psychosom Res. 2003;54:39-49.
25. Mellinger GD, Balter MB, Uhlenhuth EH. Insomnia and its treatment. Prevalence and correlates. Arch Gen Psychiatry. 1995;42:225-232.
26. Buysse DJ, Reynolds CF. Pharmacological treatment. In: Lichstein KL, Morin CM, eds. Treatment of Late-Life Insomnia. Thousand Oaks, Calif: Sage Publications; 2000:231-267.
27. Campbell SS, Terman M, Lewy AJ, Dijk DJ, Eastman CI, Boulos Z. Light treatment for sleep disorders: consensus report. V. Age-related disturbances. J Biol Rhythms. 1995;10:151-154.
28. Murphy PJ, Campbell SS. Enhanced performance in elderly subjects following bright light treatment of sleep maintenance insomnia. J Sleep Res. 1996;5:165-172.
29. Sack RL, Lewy AJ, Erb DL, Vollmer WM, Singer CM. Human melatonin production decreases with age. J Pineal Res. 1986;3:379-388.
30. McCrae C, Wilson NM, Lichstein KL, et al. Young, old, and old poor sleepers with and without insomnia complaints. J Psychosom Res. 2003;54:11-19.
