Accepted Manuscript Subjective Short Sleep Duration: What does it mean? A.N. Vgontzas, M. Basta, J. Fernandez-Mendoza PII:
S1087-0792(14)00043-4
DOI:
10.1016/j.smrv.2014.04.002
Reference:
YSMRV 805
To appear in:
Sleep Medicine Reviews
Received Date: 16 April 2014 Accepted Date: 17 April 2014
Please cite this article as: Vgontzas AN, Basta M, Fernandez-Mendoza J, Subjective Short Sleep Duration: What does it mean?, Sleep Medicine Reviews (2014), doi: 10.1016/j.smrv.2014.04.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Subjective Short Sleep Duration: What does it mean?
A.N. Vgontzas1, M. Basta2, J Fernandez-Mendoza1
1
2
RI PT
Sleep Research and Treatment Center, Department of Psychiatry, Pennsylvania State University, College of Medicine, Hershey, PA, USA
Department of Psychiatry, University of Crete, School of Medicine, Heraklion, Crete, Greece
SC
Correspondence: Dr AN Vgontzas, email:[email protected]
M AN U
The results of the study by Xi et al.1 represent the first meta-analysis on the association between sleep duration and risk of metabolic syndrome. They found that subjective short sleep duration was significantly associated with increased risk of Metabolic Syndrome (MS). Several meta-analyses have supported the association between sleep duration and obesity, hypertension, and type 2 diabetes. Since obesity, hypertension and impaired fasting glucose are components of MS, it is not surprising as the authors suggest, that short sleep duration is positively associated with MS.
EP
TE D
It has been about 10 years since the first publications raised the possibility that short sleep duration or sleep loss is a significant modifiable risk factor of the “epidemic” of obesity and its associated metabolic abnormalities.2-3 Also, at the same time small experimental studies showed that short term sleep loss increases appetite and calorie consumption by affecting appetite regulating hormones, .i.e. leptin and ghrelin.4 As it was expected it was suggested implicitly but sometimes explicitly, too, that if people sleep more they would lose weight and the obesity "epidemic" will be controlled. What have we learned in the ensuing 10 years?
AC C
First, subjective short sleep duration does not reflect sleep loss per se but it is strongly influenced by demographic, behavioral and mental health variables.5-6 For example, socioeconomic status, income, education, race and other play a significant role of how people respond to the question “how many hours do you typically sleep?”. Also, behavioral and life-style factors appear to be strongly linked to self-reported short sleep duration. Reporting bias, demand characteristics and social desirability all can influence how an individual responds to a survey. Furthermore, in a report by the Center of Disease Control and Prevention released in May 2008, it was suggested that United States adults who usually report sleeping less than 6 hours, were more likely to engage in certain health risk behaviors (i.e. cigarette smoking, consuming 5 or more alcoholic drinks per day), and not engaging in physical activity during leisure time.7 Also, Stamatakis and Brownson reported that short sleep duration is associated with less physical activity and lower fruit and vegetable consumption. 8 In 2008 in a large general population study we reported (a) self-reported short sleep duration is associated with obesity and (b) importantly, short sleep duration is
ACCEPTED MANUSCRIPT
SC
RI PT
strongly linked to sleep complaints and emotional stress measured with extensive psychological testing (MMPI). 9 We suggested that subjective short sleep duration may be a surrogate marker of emotional stress and poor sleep. In 2013 in the same cohort we examined prospectively the association between short sleep duration and incidence of obesity. 10 Consistent with previous studies, we found that subjective short sleep duration is associated with incident obesity. However, after controlling for complaints of poor sleep, and emotional stress, the significant association between short sleep and incident obesity disappeared. In fact, these two factors of poor sleep and emotional stress were strong predictors of incident obesity and played an additive role between each other. Interestingly, the effects of emotional stress were stronger in the young and middle-aged and in women. We concluded that the longitudinal association between subjective short sleep duration and incident obesity, is mediated by poor sleep and emotional stress. Finally, self-reported short sleep in not only influenced by emotional stress but also by chronic physical conditions, such as pain.
M AN U
How about the association between objective sleep duration and obesity or metabolic syndrome? Few studies, as noted also by the authors, have used objective sleep measures and almost none has reported an association either cross-sectionally or prospectively. 9-12 The findings suggest that objective sleep duration as measured by PSG or actigraphy does not predict obesity or metabolic syndrome. Parenthetically we should note that objective short sleep duration is emerging as a very useful tool in other areas of sleep research i.e. predicting severity of insomnia or influencing significantly and adversely the long term effects of cardiometabolic disorders. 13
AC C
EP
TE D
As far as biologic mechanisms linking sleep loss and obesity, there are more questions than replicated facts. The enthusiasm that sleep curtailment in young men is associated with decreased anorexigenic leptin levels and increased orexigenic ghrelin levels along with increased hunger and appetite was tempered by the fact that several experimental studies that followed failed to replicate these initial findings.14-18 The reported association between sleep loss and increased energy intake by most studies suggests that non-homeostatic (reward/ hedonistic driven feeding behavior), rather than homeostatic mechanisms (i.e. appetite/ satiety hormones) may play a role in the increased food consumption following sleep loss.19 Nevertheless the extrapolation of findings from these small experimental studies to large epidemiological studies is problematic given the severe nature of sleep restriction, i.e. 4 hours of sleep per night, a rarity in “real life” and the short term course of the experiments. Shortly after the first studies on the association of sleep and obesity, it was suggested that you may lose weight by sleeping more. Too good to be true! Although there have not been published reports from studies initiated based on this hypothesis, it is anecdotally known that extending sleep did not lead to weight loss, but rather resulted in gaining weight. In conclusion, in these 10 years we have learned that (a) subjective short sleep duration is a marker of sleep complaints and emotional stress, (b) objective sleep duration does not predict obesity, (c) the biological mechanisms of sleep loss and increased energy intake remain unknown, (d) just sleeping more does not work. Does this mean that sleep is
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
irrelevant to prevention or treatment of obesity or metabolic syndrome? Not at all. Good quality of sleep is very important for health, including weight control. Self-reported sleep duration may be a very useful screening question in the hands of the general practitioner for the detection of sleep complaints and emotional stress. Finally, assessing emotional stress, improving coping mechanisms and enhancing healthy behaviors should be part of our preventive strategies against obesity and the metabolic syndrome.
ACCEPTED MANUSCRIPT References 1. Xi B, He D, Zhang M, J Xue, Zhou D. Short sleep duration predicts risk of metabolic syndrome: A systematic review and meta-analysis. Sleep Med Rev 2014: .doi.org/10.1016/j.smrv.2013.06.001
RI PT
2. Taheri S, Lin L, Austin D, Young T, Mignot E. Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med 2004;1:e62
3. Vorona RD, Winn MP, Babineau TW, Eng BP, Feldman HR, Ware JC. Overweight and obese patients in a primary care population report less sleep than patients with normal body mass index. Arch Intern Med 2005;165:25-30
SC
4. Spiegel K, Knutson K, Leproult R, Tasali E, Van Cauter E. Sleep loss: a novel risk factor for insulin resistance and type 2 diabetes. J Appl Physiol 2005;99:2008-19
M AN U
5. Bliwise DL, Young TB. The Parable of Parabola: What the U-Shaped Curve Can and Cannot Tell Us about Sleep. Sleep 2007;130:1614-15 6. Vgontzas AN, Bixler EO. Short Sleep and Obesity: Are Poor Sleep, Chronic Stress, and Unhealthy Behaviors the Link? Sleep 2008;31:1203
TE D
7. Schoenborn CA, Adams PF. Sleep duration as a correlate of smoking, alcohol use, leisure-time physical inactivity, and obesity among adults: United States, 2004-2006. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics, May, 2008;http://www.cdc.gov/nchs/products/pubs/pubd/hestats/sleep04-06/sleep0406.htm
EP
8. Stamatakis KA, Brownson RC. Sleep duration and obesity-related risk factors in the rural Midwest. Prev Med. 2008 ;46:439-44.
AC C
9. Vgontzas AN, Lin H-M, Papaliaga M, Calhoun S, Vela-Bueno A, Chrousos GP, et al. Short sleep duration and obesity: the role of emotional stress and sleep disturbances. Int J Obes 2008;32:801-9 10. Vgontzas AN, Fenrandez-Mendoza J, Miksiewicz T, Kritikou I, Shaffer M, Liao D et al. Unveiling the longitudinal association between short sleep duration and the incidence of obesity: the Penn State Cohort. Int J Obes 2013 Sep 12. doi: 10.1038/ijo.2013.172. 11. Lauderdale DS, Knutson KL, Rathouz PJ, Yan LL, Hulley SB, Liu K. Cross-sectional and longitudinal associations between objectively measured sleep duration and body mass index: the CARDIA sleep study. Am J Epimediol 2009;170:805-13 12. Appelhans BM, Janssen I, Cursio JF, Matthews KA, Hall M, Gold EB et al. Sleep duration and weight change in midlife women: the SWAN sleep study. Obesity (Silver Spring) 2013;21:77-84
ACCEPTED MANUSCRIPT 13. Vgontzas AN, Fernandez-Mendoza J, Liao D, Bixler EO. Insomnia with objective short sleep duration: the most biologically severe phenotype of the disorder. Sleep Med Rev. 2013;17:241-54. 14. Simpson, N, Banks, S, Dinges, DF. Five nights of partial sleep restriction increased plasma leptin levels in healthy adults. Sleep 2008; 31: A128.
RI PT
15. Schmid SM, Hallschmid M, Jauch-Chara K, Wilms B, Benedict C, Lehnert H et al. Short-term sleep loss decreases physical activity under free-living conditions but does not increase food intake under time-deprived laboratory conditions in healthy men. Am J Clin Nutr. 2009;90:1476-82.
SC
16. Nedeltcheva AV, Kilkus JM, Imperial J, Kasza K, Schoeller DA, Penev PD. Sleep curtailment is accompanied by increased intake of calories from snacks. Am J Clin Nutr 2009; 89: 126-133.
M AN U
17. Nedeltcheva AV, Kilkus JM, Imperial J, Schoeller DA, Penev PD. Insufficient sleep undermines dietary efforts to reduce adiposity. Ann Intern Med 2010;153:435-41. 18. Pejovic S, Vgontzas AN, Basta M, Tsaoussoglou M, Zoumakis E, Vgontzas A, et al. Leptin and hunger levels in young healthy adults after one night of sleep loss. J Sleep Res 2010;19:552-8.
AC C
EP
TE D
19. Penev PD. Update on energy homeostasis and insufficient sleep. J Clin Endocrinol Metab 2012;97:1792-801.
S1087-0792(14)00043-4
DOI:
10.1016/j.smrv.2014.04.002
Reference:
YSMRV 805
To appear in:
Sleep Medicine Reviews
Received Date: 16 April 2014 Accepted Date: 17 April 2014
Please cite this article as: Vgontzas AN, Basta M, Fernandez-Mendoza J, Subjective Short Sleep Duration: What does it mean?, Sleep Medicine Reviews (2014), doi: 10.1016/j.smrv.2014.04.002. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Subjective Short Sleep Duration: What does it mean?
A.N. Vgontzas1, M. Basta2, J Fernandez-Mendoza1
1
2
RI PT
Sleep Research and Treatment Center, Department of Psychiatry, Pennsylvania State University, College of Medicine, Hershey, PA, USA
Department of Psychiatry, University of Crete, School of Medicine, Heraklion, Crete, Greece
SC
Correspondence: Dr AN Vgontzas, email:[email protected]
M AN U
The results of the study by Xi et al.1 represent the first meta-analysis on the association between sleep duration and risk of metabolic syndrome. They found that subjective short sleep duration was significantly associated with increased risk of Metabolic Syndrome (MS). Several meta-analyses have supported the association between sleep duration and obesity, hypertension, and type 2 diabetes. Since obesity, hypertension and impaired fasting glucose are components of MS, it is not surprising as the authors suggest, that short sleep duration is positively associated with MS.
EP
TE D
It has been about 10 years since the first publications raised the possibility that short sleep duration or sleep loss is a significant modifiable risk factor of the “epidemic” of obesity and its associated metabolic abnormalities.2-3 Also, at the same time small experimental studies showed that short term sleep loss increases appetite and calorie consumption by affecting appetite regulating hormones, .i.e. leptin and ghrelin.4 As it was expected it was suggested implicitly but sometimes explicitly, too, that if people sleep more they would lose weight and the obesity "epidemic" will be controlled. What have we learned in the ensuing 10 years?
AC C
First, subjective short sleep duration does not reflect sleep loss per se but it is strongly influenced by demographic, behavioral and mental health variables.5-6 For example, socioeconomic status, income, education, race and other play a significant role of how people respond to the question “how many hours do you typically sleep?”. Also, behavioral and life-style factors appear to be strongly linked to self-reported short sleep duration. Reporting bias, demand characteristics and social desirability all can influence how an individual responds to a survey. Furthermore, in a report by the Center of Disease Control and Prevention released in May 2008, it was suggested that United States adults who usually report sleeping less than 6 hours, were more likely to engage in certain health risk behaviors (i.e. cigarette smoking, consuming 5 or more alcoholic drinks per day), and not engaging in physical activity during leisure time.7 Also, Stamatakis and Brownson reported that short sleep duration is associated with less physical activity and lower fruit and vegetable consumption. 8 In 2008 in a large general population study we reported (a) self-reported short sleep duration is associated with obesity and (b) importantly, short sleep duration is
ACCEPTED MANUSCRIPT
SC
RI PT
strongly linked to sleep complaints and emotional stress measured with extensive psychological testing (MMPI). 9 We suggested that subjective short sleep duration may be a surrogate marker of emotional stress and poor sleep. In 2013 in the same cohort we examined prospectively the association between short sleep duration and incidence of obesity. 10 Consistent with previous studies, we found that subjective short sleep duration is associated with incident obesity. However, after controlling for complaints of poor sleep, and emotional stress, the significant association between short sleep and incident obesity disappeared. In fact, these two factors of poor sleep and emotional stress were strong predictors of incident obesity and played an additive role between each other. Interestingly, the effects of emotional stress were stronger in the young and middle-aged and in women. We concluded that the longitudinal association between subjective short sleep duration and incident obesity, is mediated by poor sleep and emotional stress. Finally, self-reported short sleep in not only influenced by emotional stress but also by chronic physical conditions, such as pain.
M AN U
How about the association between objective sleep duration and obesity or metabolic syndrome? Few studies, as noted also by the authors, have used objective sleep measures and almost none has reported an association either cross-sectionally or prospectively. 9-12 The findings suggest that objective sleep duration as measured by PSG or actigraphy does not predict obesity or metabolic syndrome. Parenthetically we should note that objective short sleep duration is emerging as a very useful tool in other areas of sleep research i.e. predicting severity of insomnia or influencing significantly and adversely the long term effects of cardiometabolic disorders. 13
AC C
EP
TE D
As far as biologic mechanisms linking sleep loss and obesity, there are more questions than replicated facts. The enthusiasm that sleep curtailment in young men is associated with decreased anorexigenic leptin levels and increased orexigenic ghrelin levels along with increased hunger and appetite was tempered by the fact that several experimental studies that followed failed to replicate these initial findings.14-18 The reported association between sleep loss and increased energy intake by most studies suggests that non-homeostatic (reward/ hedonistic driven feeding behavior), rather than homeostatic mechanisms (i.e. appetite/ satiety hormones) may play a role in the increased food consumption following sleep loss.19 Nevertheless the extrapolation of findings from these small experimental studies to large epidemiological studies is problematic given the severe nature of sleep restriction, i.e. 4 hours of sleep per night, a rarity in “real life” and the short term course of the experiments. Shortly after the first studies on the association of sleep and obesity, it was suggested that you may lose weight by sleeping more. Too good to be true! Although there have not been published reports from studies initiated based on this hypothesis, it is anecdotally known that extending sleep did not lead to weight loss, but rather resulted in gaining weight. In conclusion, in these 10 years we have learned that (a) subjective short sleep duration is a marker of sleep complaints and emotional stress, (b) objective sleep duration does not predict obesity, (c) the biological mechanisms of sleep loss and increased energy intake remain unknown, (d) just sleeping more does not work. Does this mean that sleep is
ACCEPTED MANUSCRIPT
AC C
EP
TE D
M AN U
SC
RI PT
irrelevant to prevention or treatment of obesity or metabolic syndrome? Not at all. Good quality of sleep is very important for health, including weight control. Self-reported sleep duration may be a very useful screening question in the hands of the general practitioner for the detection of sleep complaints and emotional stress. Finally, assessing emotional stress, improving coping mechanisms and enhancing healthy behaviors should be part of our preventive strategies against obesity and the metabolic syndrome.
ACCEPTED MANUSCRIPT References 1. Xi B, He D, Zhang M, J Xue, Zhou D. Short sleep duration predicts risk of metabolic syndrome: A systematic review and meta-analysis. Sleep Med Rev 2014: .doi.org/10.1016/j.smrv.2013.06.001
RI PT
2. Taheri S, Lin L, Austin D, Young T, Mignot E. Short sleep duration is associated with reduced leptin, elevated ghrelin, and increased body mass index. PLoS Med 2004;1:e62
3. Vorona RD, Winn MP, Babineau TW, Eng BP, Feldman HR, Ware JC. Overweight and obese patients in a primary care population report less sleep than patients with normal body mass index. Arch Intern Med 2005;165:25-30
SC
4. Spiegel K, Knutson K, Leproult R, Tasali E, Van Cauter E. Sleep loss: a novel risk factor for insulin resistance and type 2 diabetes. J Appl Physiol 2005;99:2008-19
M AN U
5. Bliwise DL, Young TB. The Parable of Parabola: What the U-Shaped Curve Can and Cannot Tell Us about Sleep. Sleep 2007;130:1614-15 6. Vgontzas AN, Bixler EO. Short Sleep and Obesity: Are Poor Sleep, Chronic Stress, and Unhealthy Behaviors the Link? Sleep 2008;31:1203
TE D
7. Schoenborn CA, Adams PF. Sleep duration as a correlate of smoking, alcohol use, leisure-time physical inactivity, and obesity among adults: United States, 2004-2006. Department of Health and Human Services, Centers for Disease Control and Prevention, National Center for Health Statistics, May, 2008;http://www.cdc.gov/nchs/products/pubs/pubd/hestats/sleep04-06/sleep0406.htm
EP
8. Stamatakis KA, Brownson RC. Sleep duration and obesity-related risk factors in the rural Midwest. Prev Med. 2008 ;46:439-44.
AC C
9. Vgontzas AN, Lin H-M, Papaliaga M, Calhoun S, Vela-Bueno A, Chrousos GP, et al. Short sleep duration and obesity: the role of emotional stress and sleep disturbances. Int J Obes 2008;32:801-9 10. Vgontzas AN, Fenrandez-Mendoza J, Miksiewicz T, Kritikou I, Shaffer M, Liao D et al. Unveiling the longitudinal association between short sleep duration and the incidence of obesity: the Penn State Cohort. Int J Obes 2013 Sep 12. doi: 10.1038/ijo.2013.172. 11. Lauderdale DS, Knutson KL, Rathouz PJ, Yan LL, Hulley SB, Liu K. Cross-sectional and longitudinal associations between objectively measured sleep duration and body mass index: the CARDIA sleep study. Am J Epimediol 2009;170:805-13 12. Appelhans BM, Janssen I, Cursio JF, Matthews KA, Hall M, Gold EB et al. Sleep duration and weight change in midlife women: the SWAN sleep study. Obesity (Silver Spring) 2013;21:77-84
ACCEPTED MANUSCRIPT 13. Vgontzas AN, Fernandez-Mendoza J, Liao D, Bixler EO. Insomnia with objective short sleep duration: the most biologically severe phenotype of the disorder. Sleep Med Rev. 2013;17:241-54. 14. Simpson, N, Banks, S, Dinges, DF. Five nights of partial sleep restriction increased plasma leptin levels in healthy adults. Sleep 2008; 31: A128.
RI PT
15. Schmid SM, Hallschmid M, Jauch-Chara K, Wilms B, Benedict C, Lehnert H et al. Short-term sleep loss decreases physical activity under free-living conditions but does not increase food intake under time-deprived laboratory conditions in healthy men. Am J Clin Nutr. 2009;90:1476-82.
SC
16. Nedeltcheva AV, Kilkus JM, Imperial J, Kasza K, Schoeller DA, Penev PD. Sleep curtailment is accompanied by increased intake of calories from snacks. Am J Clin Nutr 2009; 89: 126-133.
M AN U
17. Nedeltcheva AV, Kilkus JM, Imperial J, Schoeller DA, Penev PD. Insufficient sleep undermines dietary efforts to reduce adiposity. Ann Intern Med 2010;153:435-41. 18. Pejovic S, Vgontzas AN, Basta M, Tsaoussoglou M, Zoumakis E, Vgontzas A, et al. Leptin and hunger levels in young healthy adults after one night of sleep loss. J Sleep Res 2010;19:552-8.
AC C
EP
TE D
19. Penev PD. Update on energy homeostasis and insufficient sleep. J Clin Endocrinol Metab 2012;97:1792-801.
