Glucose Variations and Activity Are Strongly Coupled in Sleep and Wake in Young Adults With Type 1 Diabetes

Abstract

Background:

Glucose variations are common throughout sleep and wakefulness in people with type 1 diabetes mellitus (T1DM). The objective of this investigation was to characterize the time-varying coupling between glucose and unstructured physical activity over a 60-hr period in young adults with T1DM. The hypothesis was that coupling would differ during sleep versus wakefulness and would exhibit circadian variations.

Method:

Young adults with T1DM treated with an insulin pump participated in the study. Glucose variations were monitored with a continuous glucose monitoring system, and activity was assessed using an activity-monitoring band worn on the nondominant wrist. Simultaneous glucose and physical activity data across a continuous 60-hr period were used for analysis. Wavelet coherence analysis was employed to quantify the coupling between physical activity and glucose. Cosinor analysis was used to assess whether glucose/activity coherence exhibited significant circadian variations.

Results:

Participants comprised 23 adults, aged 18−30 years, with T1DM. Coherence analysis demonstrated substantial coupling between physical activity and glucose variations during both wakefulness and sleep. For rapid (10–30 min) fluctuations, mean coherence was higher during sleep than wakefulness (F = 10.86, p = .003). Rapid glucose variations consistently led to changes in activity (p = .001) during sleep but not during wake. Cosinor analysis revealed significant circadian modulation of glucose/activity coupling, especially for fluctuation periods 2–4 hr.

Conclusions:

Unstructured physical activity and glucose variations demonstrated strong time- and frequency-dependent coupling over a 60-hr period in young adults with T1DM, with sleep/wake differences and circadian modulation evident in this relationship.

Keywords

sleep circadian type 1 diabetes glucose fluctuations

Get full access to this article

View all access options for this article.

References

Bally

Laimer

Stettler

(2015). Exercise-associated glucose metabolism in individuals with type 1 diabetes mellitus. Current Opinion in Clinical Nutrition and Metabolic Care, 18, 428–433. doi:10.1097/MCO.0000000000000185

Cappuccio

F. P.

Cooper

D’Elia

Strazzullo

Miller

M. A.

(2011). Sleep duration predicts cardiovascular outcomes: A systematic review and meta-analysis of prospective studies. European Heart Journal, 32, 1484–1492. doi:10.1093/eurheartj/ehr007

Coomans

C. P.

van den Berg

S. A. A.

Lucassen

E. A.

Houben

Pronk

A. C. M.

van der Spek

R. D.

… Meijer

J. H.

(2013). The suprachiasmatic nucleus controls circadian energy metabolism and hepatic insulin sensitivity. Diabetes, 62, 1102–1108. doi:10.2337/db12-0507

Davey

R. J.

Howe

Paramalingam

Ferreira

L. D.

Davis

E. A.

Fournier

P. A.

Jones

T. W.

(2013). The effect of midday moderate-intensity exercise on postexercise hypoglycemia risk in individuals with type 1 diabetes. Journal of Clinical Endocrinology and Metabolism, 98, 2908–2914. doi:10.1210/jc.2013-1169

Davidson

J. R.

Moldofsky

Lue

F. A.

(1991). Growth hormone and cortisol secretion in relation to sleep and wakefulness. Journal of Psychiatry & Neuroscience, 16, 96–102.

de Ferranti

S. D.

de Boer

I. H.

de Fonseca

Fox

C. S.

Golden

S. H.

Lavie

C. J.

… Eckel

R. H.

(2014). Type 1 diabetes mellitus and cardiovascular disease: A scientific statement from the American Heart Association and American Diabetes Association. Diabetes Care, 37, 2843–2863. doi:10.2337/dc14-1720

Grinsted

Moore

Jevrejeva

(2004). Application of the cross wavelet transform and wavelet coherence to geophysical time series. Nonlinear Processes in Geophysics, 11, 561–566.

Gross

T. M.

Mastrototaro

J. J.

(2000). Efficacy and reliability of the continuous glucose monitoring system. Diabetes Technology & Therapeutics, 2, 19–26. doi:10.1089/15209150050214087

Hanlon

E. C.

Van Cauter

(2011). Quantification of sleep behavior and of its impact on the cross-talk between the brain and peripheral metabolism. Proceedings of the National Academy of Sciences of the United States of America, 108, 15609–15616. doi:10.1073/pnas.1101338108

10.

Hinshaw

Dalla Man

Nandy

D. K.

Saad

Bharucha

A. E.

Levine

J. A.

… Basu

(2013). Diurnal pattern of insulin action in type 1 diabetes: Implications for a closed-loop system. Diabetes, 62, 2223–2229. doi:10.2337/db12-1759

11.

Houmard

J. A.

Tanner

C. J.

Slentz

C. A.

Duscha

B. D.

McCartney

J. S.

Kraus

W. E.

(2004). Effect of the volume and intensity of exercise training on insulin sensitivity. Journal of Applied Physiology, 96, 101–106. doi:10.1152/japplphysiol.00707.2003

12.

Islam

(2011). Wavelets, its application and technique in signal and image processing. Global Journal of Computer Science & Technology, 11. Retrieved from http://globaljournals.org/GJCST_Volume11/7-Wavelets-its-Application-and-Technique-in-signal-and-image-processing.pdf

13.

Johns

M. W.

(1991). A new method for measuring daytime sleepiness: The Epworth sleepiness scale. Sleep, 14, 540–545.

14.

Matyka

K. A.

Crawford

Wiggs

Dunger

D. B.

Stores

(2000). Alterations in sleep physiology in young children with insulin-dependent diabetes mellitus: Relationship to nocturnal hypoglycemia. Journal of Pediatrics, 137, 233–238. doi:10.1067/mpd.2000.107186

15.

McMahon

S. K.

Ferreira

L. D.

Ratnam

Davey

R. J.

Youngs

L. M.

Davis

E. A.

… Jones

T. W.

(2007). Glucose requirements to maintain euglycemia after moderate-intensity afternoon exercise in adolescents with type 1 diabetes are increased in a biphasic manner. Journal of Clinical Endocrinology and Metabolism, 92, 963–968. doi:10.1210/jc.2006-2263

16.

Neu

Behret

Braun

Herrlich

Liebrich

Loesch-Binder

… Schweizer

(2015). Higher glucose concentrations following protein- and fat-rich meals—The Tuebingen Grill study: A pilot study in adolescents with type 1 diabetes. Pediatric Diabetes, 16, 587–591. doi:10.1111/pedi.12224

17.

Pillar

Schuscheim

Weiss

Malhotra

McCowen

K. C.

Shlitner

… Shehadeh

(2003). Interactions between hypoglycemia and sleep architecture in children with type 1 diabetes mellitus. Journal of Pediatrics, 142, 163–168. doi:10.1067/mpd.2003.66

18.

Quirk

Blake

Tennyson

Randell

T. L.

Glazebrook

(2014). Physical activity interventions in children and young people with type 1 diabetes mellitus: A systematic review with meta-analysis. Diabetic Medicine, 31, 1163–1173. doi:10.1111/dme.12531

19.

Radan

Rajer

Ursic Bratina

Neubauer

Krzisnik

Battelino

(2004). Motor activity during asymptomatic nocturnal hypoglycemia in adolescents with Type 1 diabetes mellitus. Acta Diabetologica, 41, 33–37. doi:10.1007/s00592-004-0141-3

20.

Rizza

R. A.

Mandarino

L. J.

Gerich

J. E.

(1982). Effects of growth hormone on insulin action in man: Mechanisms of insulin resistance, impaired suppression of glucose production, and impaired stimulation of glucose utilization. Diabetes, 31, 663–669. doi:10.2337/diab.31.8.663

21.

Shin

Swan

Chow

C. M.

(2015). The validity of Actiwatch2 and SenseWear armband compared against polysomnography at different ambient temperature conditions. Sleep Science, 8, 9–15. doi:10.1016/j.slsci.2015.02.003

22.

Silveira

A. P. S.

Bentes

C. M.

Costa

P. B.

Simão

Silva

F. C.

Silva

R. P.

Novaes

J. S.

(2014). Acute effects of different intensities of resistance training on glycemic fluctuations in patients with type 1 diabetes mellitus. Research in Sports Medicine, 22, 75–87. doi:10.1080/15438627.2013.852096

23.

Sonnenberg

G. E.

Kemmer

F. W.

Berger

(1990). Exercise in type 1 (insulin-dependent) diabetic patients treated with continuous subcutaneous insulin infusion. Prevention of exercise induced hypoglycaemia. Diabetologia, 33, 696–703.

24.

Spira

A. P.

Beaudreau

S. A.

Stone

K. L.

Kezirian

E. J.

Lui

L.-Y.

Redline

… Stewart

(2011). Reliability and validity of the Pittsburgh Sleep Quality Index and the Epworth Sleepiness Scale in older men. Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 67A, 433–439. doi:10.1093/gerona/glr172

25.

Stamatakis

K. A.

Punjabi

N. M.

(2009). Effects of sleep fragmentation on glucose metabolism in normal subjects. Chest, 137, 95–101. doi:10.1378/chest.09-0791

26.

Summa

K. C.

Turek

F. W.

(2014). Chronobiology and obesity: Interactions between circadian rhythms and energy regulation. Advances in Nutrition, 5, 312S–319S. doi:10.3945/an.113.005132

27.

Tatò

Beyer

Schrezenmeir

(1991). Circadian variation of basal and postprandial insulin sensitivity in healthy individuals and patients with type-1 diabetes. Diabetes Research, 17, 13–24.

28.

Torrence

Compo

G. P.

(1998). A practical guide to wavelet analysis. Bulletin of the American Meteorological Society, 79, 61.

29.

Trümper

B. G.

Reschke

Molling

(1995). Circadian variation of insulin requirement in insulin dependent diabetes mellitus: The relationship between circadian change in insulin demand and diurnal patterns of growth hormone, cortisol and glucagon during euglycemia. Hormone and Metabolic Research, 27, 141–147. doi:10.1055/s-2007-979926

30.

Van Cauter

(1997). Roles of circadian rhythmicity and sleep in human glucose regulation. Endocrine Reviews, 18, 716–738. doi:10.1210/er.18.5.716

31.

Van Cauter

Blackman

J. D.

Roland

Spire

J. P.

Refetoff

Polonsky

K. S.

(1991). Modulation of glucose regulation and insulin secretion by circadian rhythmicity and sleep. Journal of Clinical Investigation, 88, 934–942. doi:10.1172/JCI115396