Sleep extension improves neurocognitive functions in chronically sleep-deprived obese individuals

Eliane A Lucassen, Paolo Piaggi, John Dsurney, Lilian de Jonge, Xiong-ce Zhao, Megan S Mattingly, Angela Ramer, Janet Gershengorn, Gyorgy Csako, Giovanni Cizza, Sleep Extension Study Group, Eliane A Lucassen, Paolo Piaggi, John Dsurney, Lilian de Jonge, Xiong-ce Zhao, Megan S Mattingly, Angela Ramer, Janet Gershengorn, Gyorgy Csako, Giovanni Cizza, Sleep Extension Study Group

Abstract

Background: Sleep deprivation and obesity, are associated with neurocognitive impairments. Effects of sleep deprivation and obesity on cognition are unknown, and the cognitive long-term effects of improvement of sleep have not been prospectively assessed in short sleeping, obese individuals.

Objective: To characterize neurocognitive functions and assess its reversibility.

Design: Prospective cohort study.

Setting: Tertiary Referral Research Clinical Center.

Patients: A cohort of 121 short-sleeping (<6.5 h/night) obese (BMI 30-55 kg/m(2)) men and pre-menopausal women.

Intervention: Sleep extension (468±88 days) with life-style modifications.

Measurements: Neurocognitive functions, sleep quality and sleep duration.

Results: At baseline, 44% of the individuals had an impaired global deficit score (t-score 0-39). Impaired global deficit score was associated with worse subjective sleep quality (p = 0.02), and lower urinary dopamine levels (p = 0.001). Memory was impaired in 33%; attention in 35%; motor skills in 42%; and executive function in 51% of individuals. At the final evaluation (N = 74), subjective sleep quality improved by 24% (p<0.001), self-reported sleep duration increased by 11% by questionnaires (p<0.001) and by 4% by diaries (p = 0.04), and daytime sleepiness tended to improve (p = 0.10). Global cognitive function and attention improved by 7% and 10%, respectively (both p = 0.001), and memory and executive functions tended to improve (p = 0.07 and p = 0.06). Serum cortisol increased by 17% (p = 0.02). In a multivariate mixed model, subjective sleep quality and sleep efficiency, urinary free cortisol and dopamine and plasma total ghrelin accounted for 1/5 of the variability in global cognitive function.

Limitations: Drop-out rate.

Conclusions: Chronically sleep-deprived obese individuals exhibit substantial neurocognitive deficits that are partially reversible upon improvement of sleep in a non-pharmacological way. These findings have clinical implications for large segments of the US population.

Trail registration: www.ClinicalTrials.gov NCT00261898. NIDDK protocol 06-DK-0036.

Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Figure 1. Neurocognitive function at baseline.
Figure 1. Neurocognitive function at baseline.
Left Figure: Results of deficit scores and individual neurocognitive tests. Right Figure: Results of the IGT per subsequent block of the test. The left vertical axis depicts the percentage of individuals in the following categories of neuropsychological function levels: impaired (t-score 0–39), below average (t-score 40–44), average (t-score 45–54), and above average (t-score 55–100). The right y-axis shows the mean±SD of the t-scores for each separate test. Mean and SD for deficit scores are not shown, because these variables exhibited a skewed distribution. Memory was tested by Rey-DR, the CVLT-II SD and the CVLT-II LD. Attention was tested by the CVLT-II Sum and by the TMT-A. Motor skills were assessed by the GPeg Dom and the GPeg Non-Dom. Executive functions were tested by the WCST, the TMT-B and the IGT. For all t-score computations, age was taken into account. In addition, ayears of education were taken into consideration for the t-scores for the WCST and IGT, and bgender was taken into account for the CVLT scores. cEducation, race, and gender were all taken into account for t-scores of the TMT, GPeg, and FAS. Abbreviations: GDS  =  Global Deficit Score, DDS  =  Domain Deficit Score, Rey-DR  =  Rey Complex Figure Test Delayed Recall, CVLT-II SD  =  California Verbal Learning Test II Short Delay, CVLT-II LD  =  California Verbal Learning Test II Long Delay, CVLT-II Sum  =  California Verbal Learning Test II Sum Score, TMT-A =  Trail Making Test Part A, TMT-B =  Trail Making Test Part B, GPeg Dom  =  Grooved Peg Board Test Dominant Hand, GPeg Non-Dom  =  Grooved Peg Board Test Non-Dominant Hand, WCST  =  Wisconsin Card Sort Test, IGT  =  Iowa Gambling Task.

References

    1. Flegal KM, Carroll MD, Kit BK, Ogden CL (2012) Prevalence of obesity and trends in the distribution of body mass index among US adults, 1999–2010. JAMA 307: 491–7.
    1. Centers for Disease Control and Prevention (CDC) (2012) Short sleep duration among workers -United States, 2010. MMWR Morb Mortal Wkly Rep 61: 281–5.
    1. Cizza G, Requena M, Galli G, de Jonge L (2011) Chronic sleep deprivation and seasonality: implications for the obesity epidemic. J Endocrinol Invest 34: 793–800.
    1. Lucassen EA, Rother KI, Cizza G (2012) Interacting epidemics? Sleep curtailment, insulin resistance, and obesity. Ann N Y Acad Sci 1264: 110–34.
    1. Boeka AG, Lokken KL (2008) Neuropsychological performance of a clinical sample of extremely obese individuals. Arch Clin Neuropsychol 23: 467–74.
    1. Mobbs O, Crépin C, Thiéry C, Golay A, Van der Linden M (2010) Obesity and the four facets of impulsivity. Patient Educ Couns 79: 372–7.
    1. Volkow ND, Wang GJ, Tomasi D, Baler RD (2013) Obesity and addiction: neurobiological overlaps. Obes Rev 14: 2–18.
    1. Davis C, Patte K, Curtis C, Reid C (2010) Immediate pleasures and future consequences. A neuropsychological study of binge eating and obesity. Appetite 54: 208–13.
    1. Waldstein SR, Katzel LI (2006) Interactive relations of central versus total obesity and blood pressure to cognitive function. Int J Obes (Lond) 30: 201–7.
    1. Brogan A, Hevey D, Pignatti R (2010) Anorexia, bulimia, and obesity: shared decision making deficits on the Iowa Gambling Task (IGT). J Int Neuropsychol Soc 16: 711–5.
    1. Kanoski SE (2012) Cognitive and neuronal systems underlying obesity. Physiol Behav 106: 337–44.
    1. Waters F, Bucks RS (2011) Neuropsychological Effects of Sleep Loss: Implication for Neuropsychologists. J Int Neuropsychol Soc 17: 571–86.
    1. Tomasi D, Wang RL, Telang F, Fowler JS, Wang RL, et al. (2009) Impairment of attentional networks after 1 night of sleep deprivation. Cereb Cortex 19: 233–40.
    1. Gradisar M, Terrill G, Johnston A, Douglas P (2008) Adolescent sleep and working memory performance. Sleep Biol Rhythm 6: 146–148.
    1. Philibert I (2005) Sleep loss and performance in residents and nonphysicians: a meta-analytic examination. Sleep 28: 1392–402.
    1. Mahajan N, Hong N, Wigal TL, Gehricke JG (2010) Hyperactive-impulsive symptoms associated with self-reported sleep quality in nonmedicated adults with ADHD. J Atten Disord 14: 132–7.
    1. Potkin KT, Bunney WE Jr (2012) Sleep improves memory: the effect of sleep on long term memory in early adolescence. PLoS One 7: e42191.
    1. St-Onge MP, McReynolds A, Trivedi ZB, Roberts AL, Sy M, et al. (2012) Sleep restriction leads to increased activation of brain regions sensitive to food stimuli. Am J Clin Nutr 95: 818–24.
    1. de Jonge L, Zhao X, Mattingly MS, Zuber SM, Piaggi P, et al. (2012) Poor sleep quality and sleep apnea are associated with higher resting energy expenditure in obese individuals with short sleep duration. J Clin Endocrinol Metab 97: 2881–9.
    1. Osterrieth PA (1944) File test de copie d′une figure complex: Contribution a l′etude de la perception et de la memoire [The test of copying a complex figure: A contribution to the study of perception and memory] Archives de Psychologie. 30: 286–356.
    1. Delis DC, Kramer JH, Kaplan E, Ober BA (2000) California Verbal Learning Test: Second Edition. San Antonio, TX: Psychological Corporation
    1. Berg EA (1948) A simple objective technique for measuring flexibility in thinking J Gen Psychol. 39: 15–22.
    1. Reitan RM (1958) Validity of the Trail Making test as an indicator of organic brain damage. Percept Mot Skills 8: 271–276.
    1. Benton LA, de Hamsher K, Sivan AB (1994) Controlled oral word association test. Multilingual aphasia examination (3rd ed). Iowa City, IA: AJA.
    1. Bechara A, Damásio AR, Damásio H, Anderson SW (1994) Insensitivity to future consequences following damage to human prefrontal cortex. Cognition 50: 7–15.
    1. Dikmen SS, Heaton RK, Grant I, Temkin NR (1999) Test-retest reliability and practice effects of expanded Halstead-Reitan Neuropsychological Test Battery. J Int Neuropsychol Soc 5: 346–56.
    1. Alberti KG, Eckel RH, Grundy SM, Zimmet PZ, Cleeman JI, et al. (2009) Harmonizing the metabolic syndrome: a joint interim statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120: 1640–5.
    1. Ayappa I, Norman RG, Seelall V, Rapoport DM (2008) Validation of a self-applied unattended monitor for sleep disordered breathing. J Clin Sleep Med 4: 26–37.
    1. Johns MW (1991) A new method for measuring daytime sleepiness: The Epworth Sleepiness Scale. Sleep 14: 540–5.
    1. Buysse DJ, Reynolds CF 3rd, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 28: 193–213.
    1. Heaton RK, Miller W, Taylor MJ, Grant I (2004) Revised comprehensive norms for an expanded halstead-reitan battery. Demographically adjusted neuropsychological norms for African American and Caucasian adults. Lutz, USAPsychological Assessment Resources inc.
    1. Carey CL, Woods SP, Gonzalez R, Conover E, Marcotte TD, et al. (2004) Predictive validity of global deficit scores in detecting neuropsychological impairment in HIV infection. J Clin Exp Neuropsychol 26: 307–19.
    1. Lauderdale DS, Knutson KL, Yan LL, Liu K, Rathouz PJ (2008) Self-reported and measured sleep duration: how similar are they? Epidemiology 19: 838–45.
    1. Johnson NL, Kirchner HL, Rosen CL, Storfer-Isser A, Cartar LN, et al. (2007) Sleep estimation using wrist actigraphy in adolescents with and without sleep disordered breathing: a comparison of three data modes. Sleep 30: 899–905.
    1. Duchesne M, Mattos P, Appolinario J, Freitas S, Coutinho G, et al. (2010) Assessment of executive functions in obese individuals with binge eating disorder. Rev Bras Psychiatr 32: 381–8.
    1. Danner UN, Ouwehand C, van Haastert NL, Hornsveld H, de Ridder DT (2012) Decision-making impairments in women with binge eating disorder in comparison with obese and normal weight women. Eur Eat Disord Rev 20: e56–62.
    1. Kim HJ, Kim JH, Park KD, Choi KG, Lee HW A (2011) survey of sleep deprivation patterns and their effects on cognitive functions of residents and interns in Korea. Sleep Med 12: 390–6.
    1. Saunamäki T, Himanen SL, Polo O, Jehkonen M (2009) Executive dysfunction in patients with obstructive sleep apnea syndrome. Eur Neurol 62: 237–42.
    1. Göder R, Scharffetter F, Aldenhoff JB, Fritzer G (2007) Visual declarative memory is associated with non-rapid eye movement sleep and sleep cycles in patients with chronic non-restorative sleep. Sleep Med 8: 503–8.
    1. Pearson VE, Allen RP, Dean T, Gamaldo CE, Lesage SR, et al. (2006) Cognitive deficits associated with restless legs syndrome (RLS). Sleep Med 7: 25–30.
    1. Cools R, D′Esposito M (2011) Inverted-U-shaped dopamine actions on human working memory and cognitive control. Biol Psychiatry 69: e113–25.
    1. Sara SJ (2009) The locus coeruleus and noradrenergic modulation of cognition. Nat Rev Neurosci 10: 211–23.
    1. Gahete MD, Córdoba-Chacón J, Kineman RD, Luque RM, Castaño JP (2011) Role of ghrelin system in neuroprotection and cognitive functions: implications in Alzheimer's disease. Peptides 32: 2225–8.

Source: PubMed

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