the role of sleep duration in diabetes and glucose control … · tween sleep duration and risk of...

Proceedings

oftheNutritionSo

ciety

The Joint Winter Meeting between the Nutrition Society and the Royal Society of Medicine held at The Royal Society of Medicine,London on 8–9 December 2015

Conference on ‘Roles of sleep and circadian rhythms in the origin and nutritionalmanagement of obesity and metabolic disease’Symposium 4: Influence of lifestyle and genetics

The role of sleep duration in diabetes and glucose control

Alia Alnaji1,2, Graham R. Law1 and Eleanor M. Scott1*1Leeds Institute of Cardiovascular and Metabolic Medicine, University of Leeds, Leeds, UK

2Department of Public Health, General Directorate of Health Affairs in Eastern Province, Ministry of Health,Saudi Arabia

Sleep curtailment is common in the Westernised world and coincides with an increase in theprevalence of type 2 diabetesmellitus (T2DM). This review considers the recently published evi-dence forwhether sleep duration is involved in the development ofT2DMinhuman subjects andwhether sleep has a role to play in glucose control in peoplewho have diabetes. Data from large,prospective studies indicate a U-shaped relationship between sleep duration and the develop-ment of T2DM. Smaller, cross-sectional studies also support a relationship between shortsleep duration and the development of both insulin resistance and T2DM. Intervention studiesshow that sleep restriction leads to insulin resistance, with recent sleep extension studies offeringtantalising data showing a potential benefit of sleep extension on glucose control and insulin sen-sitivity. In peoplewith established diabetes the published literature shows anassociationbetweenpoor glucose control and both short and long sleep durations. However, there are currently nostudies that determine the causal direction of this relationship, nor whether sleep interventionsare likely to offer benefit for people with diabetes to help them achieve tighter glucose control.

Diabetes: Glucose: Sleep: Circadian: Clock: Insulin resistance

Life on earth is governed by the 24-h cycle of light anddarkness associated with the rotation of the earth.Normally metabolic and physiological pathways arecoordinated to this 24-h cycle by an endogenous clockenabling our bodies to coordinate appropriate physio-logical processes to the time of day. Research in animalsand human subjects suggests that the advent of a 24/7lifestyle that disrupts our natural sleep cycles and theiralignment to the external light–dark cycle is importantin the regulation of energy balance and glucose metabol-ism(1–3). Sleep curtailment has become a prevalent behav-iour in the Western and developing world where it isestimated that average sleepdurationhasdeclinedbyalmost2 h in the past 50 years(4). In the USA and UK, a third ofthe population report getting <7 h sleep per night(5,6).Coinciding with this there has been an explosion in theprevalence of type 2 diabetes mellitus (T2DM), raising theimportant question ofwhether there is a causal link between

the two. This review will specifically consider the recentlypublished evidence for whether sleep duration is involvedin the development of T2DM in human subjects. It will nei-ther appraise the considerable number of studies lookingpredominantly at the role of sleep in the development ofobesity,nor itwilladdresstheseparate,but related, literaturelinking sleep-related breathing disorders to obesity andT2DM. Having considered the role of sleep duration perse in the development of diabetes, the evidence for whethersleep duration has a role to play in glucose control in peoplewho have diabetes is reviewed.

Association between sleep duration and the risk oftype 2 diabetes

Evidence from prospective studies

Several large cohort studies have investigated the associ-ation between sleep duration and the risk of subsequently

*Corresponding author: Dr E. M. Scott, email [email protected]: HR, hazard ratio; T2DM, type 2 diabetes mellitus.

Proceedings of the Nutrition Society (2016), 75, 512–520 doi:10.1017/S002966511600063X© The Authors 2016 First published online 23 June 2016

https://www.cambridge.org/core/terms. https://doi.org/10.1017/S002966511600063XDownloaded from https://www.cambridge.org/core. IP address: 54.39.106.173, on 14 Feb 2021 at 01:46:15, subject to the Cambridge Core terms of use, available at

http://crossmark.crossref.org/dialog/?doi=10.1017/S002966511600063X&domain=pdf

https://www.cambridge.org/core/terms

https://doi.org/10.1017/S002966511600063X

https://www.cambridge.org/core

Proceedings

oftheNutritionSo

ciety

developing T2DM, studied over varying lengths of follow-up(7–16). Details of their study design and outcomes areshown in Table 1. Several big studies in the USA andGermany have shown a U-shaped association betweensleep duration and increased risk of T2DM(7–9). The stud-ies relied on subjective measures, with sleep duration self-reported at baseline, and T2DM incidence was mainlyby self-report of physician’s diagnosis.Using 7 h sleep dur-ation per night as a reference category, those with shorterand longer sleep duration were significantly more likely todevelop T2DM over the follow-up period of 5–15 years(risk estimates ranging between 1·47 and 1·95 for shortsleep duration, and between 1·40 and 3·12 for long sleepduration). Regression models employed in the analysiswere adjusted for many potential confounders, mainly;age, physical activity, BMI, alcohol consumption, ethni-city, education, marital status, depression and history ofhypertension.Not all studies have shown thisU-shaped re-lationship however. A large Australian study of >192 000adults used information recorded in medical insurancerecords(10) and reported a positive association betweenshort (but not long) sleep duration and subsequent inci-dence of T2DM. However, T2DM incidence was deter-mined from hospital admission records and so those whowere not admitted to hospital during the follow-up periodcould not be identified as T2DM, which might have led tounderestimation of the actual diabetes incidence. In add-ition, the follow-up period was relatively short (mean dur-ation 2·3 years). Another prospective study examined theassociation of sleep duration with development ofimpaired fasting glucose over 6 years follow-up(11),with 6–8 h sleep duration as a reference category, short(but not long) sleepers had higher odds of developingimpaired fasting glucose (OR 3·0, 95 % CI 1·05, 8·59;OR 1·6, 95 % CI 0·45, 5·42 for short and long sleep dura-tions, respectively). A Finnish study in overweight indivi-duals with impaired glucose tolerance found an increasedrisk of T2DMonly in participants with long sleep duration⩾9 h (hazard ratio (HR) 2·29, 95 % CI 1·38, 3·80)(14).Finally, two recent meta-analyses of nine(17) and four-teen(18) prospective cohort studies have also confirmedthe U-shaped relationship (Fig. 1). A couple of other stud-ies have investigated the association between short com-pared with normal sleep duration and the risk of T2DMwithout examining for a U-shaped relationship. The firstshowed that sleeping ⩽7 h per night was associated withhigher odds of developing T2DM after 6 years follow-up(OR 1·96, 95 % CI 1·10, 3·50)(12). Models were adjustedfor age, sex, physical activity, smoking habit, weightgain and abnormal glucose regulation at baseline. Thestudy also found that the odds of becoming obese weresignificantly higher in subjects who slept ⩽7 h per night(OR 1·99, 95 % CI 1·12, 3·55). There was a lack of associ-ation between sleep duration and TD2M at 11 yearsfollow-up that could be related to the attrition in studypopulation over time and to the mediation effect exhibitedby adjusting for weight gain in the model. The secondstudy found a higher odds of T2DM after 2 years follow-up, sleeping ⩽5 h compared with >7 h sleep duration(OR 5·37, 95 % CI 1·38, 20·91)(13). The logistic regressionmodels were however adjusted for fasting plasma glucose,

an integral feature of the outcome measure, T2DM. Thisleads to a statistical phenomenon known as mathematicalcoupling thus rendering the result spurious(19,20).

Extending the understanding of the relationship be-tween sleep duration and risk of T2DM the impact ofa change in sleep duration over time has also been inves-tigated. In the Whitehall II study in the UK, change insleep duration was calculated for participants withoutdiabetes at the beginning and end of four 5-year cyclesand T2DM incidence was observed at the end of the sub-sequent cycle(15). Another, rather convoluted, prospectivestudy (the Nurses’ Health study) examined whether his-toric changes in women’s sleep duration over the preced-ing 14 years was associated with developing T2DM overthe subsequent 12-year follow-up(16). In both studies, lo-gistic regression models showed higher risk of developingT2DM in participants with chronic short sleep duration(⩽5·5–6 h; Whitehall II study OR 1·35, 95 % CI 1·04,1·76; Nurses’ Health study HR 1·10, 95 % CI 1·001,1·21) and in those with an increase of ⩾2 h sleep duration(Whitehall II study OR 1·65, 95 % CI 1·15, 2·37; Nurses’Health study HR 1·15, 95 % CI 1·01, 1·30) comparedwith those who maintained 7–8 h sleep duration. Afteradjusting for BMI both associations were attenuated,suggesting that BMI is a mediator in the association.These studies suggest that the adverse metabolic influ-ence of short sleep duration may not be ameliorated byincreasing sleep duration later in life.

Taken together, these large prospective studies whichinclude both men and women, and a wide range ofages show that a U-shaped relationship exists betweenself-reported sleep duration and the development ofT2DM. Given the increasing societal pressures to sleepless, these data are very persuasive of short sleep durationbeing implicated in the co-existent T2DM epidemic.

Evidence from cross-sectional studies

Whilst they do not carry the same weight as prospectivestudies, there have been several recent cross-sectionalstudies that suggest there may be some key sociodemo-graphic factors that influence the relationship betweensleep duration and T2DM, and these are summarisedin Table 2. Again a U-shaped association between sleepduration (over a 24 h period) and T2DM was observedin 130 943 adults, aged 18–85 years, using data fromthe National Health Interview Survey from 2004 to2011(21). However, short and long sleep durations weremore strongly associated with T2DM in white partici-pants than in black. Adjustment for socioeconomic statusand other health behavioural factors attenuated the asso-ciations in both groups and remained significant only inwhite participants. An additional cross-sectional studyusing the National Health Interview Survey data, fromyears 2004 to 2005, also reported a U-shaped associationbetween sleep duration and T2DM(22). A Chinese studyshowed that longer sleep duration over a 24 h periodwas positively associated with having the metabolic syn-drome and T2DM, but only in women(23). Objectivelymeasured sleep duration (using wrist actigraphy) showeda significant association between shorter sleep duration

The role of sleep duration in diabetes and glucose control 513



https://doi.org/10.1017/S002966511600063X


Proceedings of the Nutrition Society

Table 1. Prospective studies on sleep duration and the risk of developing type 2 diabetes mellitus (T2DM)

Author, year Country Participant Study design Exposure Outcome Result Comment

Gangwisch et al.,2007(8)

USA 8992 adult aged 32–68years from the NHANES I

Prospective cohort Subjective nighttimesleep duration

T2DM incidenceover 8–10 yearsfollow-up period

U-shaped associations

Yaggi et al., 2006(7) USA 1564 men aged 40–70 yearsfrom the MassachusettsMale Aging study

Prospective cohortstudy

Subjective nighttimesleep duration

T2DM incidenceover 15-yearfollow-up period


Kowall et al.,2016(9)

Germany 4814 adults aged 45–75years from the HeinzNixdorf Recall study


Subjective nighttimesleep duration



Holliday et al.,2013(10)

Australia 192 728 adults aged ⩾45selected from medicalinsurance database


Subjective sleepduration

T2DM incidenceover a meanfollow-up periodof 2·3 years

Positive association, onlyshort sleep duration

Diabetes incidentsextracted from hospitaladmission or mortalityelectronic records, shortfollow-up period

Rafalson et al.,2010(11)

USA 363 participants; 91 cases,272 controls, aged 35–79years

nested case-control Subjective sleepduration (weekdaysonly)

Impaired fastingglucose

Positive association, onlyshort sleep duration

Tuomilehto et al.,2009(14)

Finland 522 participants aged 40–64years without diabetesrandomly allocated eitherto a study arm or to acontrol arm

Two Prospectivecohorts based onarms of arandomisedcontrolled trial

Subjective sleepduration


Positive association, onlylong sleep duration

Only in the control armcohort

Gutiérrez-Repisoet al., 2014(12)

Spain 1145 randomly selectedparticipants aged 16–65years from the Pizzarastudy

Prospective cohort Subjective nighttimesleep duration

T2DM incidenceat 6 and 11 yearsfollow-up

Positive association only at6-year follow-up

Change in sleep durationover the 11-yearfollow-up

Kita et al., 2012(13) Japan 3570 adults aged 35–55years

Prospective cohort Subjective sleepduration and sleepquality

T2DM incidenceafter 2-yearfollow-up)

Positive spuriousassociation

Statistical issues

Ferrie et al.,2015(15)

UK 5613 adults aged 35–55years from the Whitehall IIstudy

Prospective cohort,four 5-year cycles

Change in nighttimesleep duration inthe following cycle

T2DM incidenceat the end ofsubsequentcycle

Positive association,increase ⩾2 h

Association could bemediated by weight gain

Cespedes et al.,2016(16)

USA 59 031 middle aged to oldwomen without diabetes


Change in sleepduration over 14years


Positive association,increase ⩾2 h

Association only withincrease in sleep duration⩾2 h/d, Change in sleepduration from a historicbaseline to time ofenrolment

A.Alnaji

etal.

514

https://ww

w.cam

bridge.org/core/terms. https://doi.org/10.1017/S002966511600063X

Dow

nloaded from https://w

ww

.cambridge.org/core. IP address: 54.39.106.173, on 14 Feb 2021 at 01:46:15, subject to the Cam

bridge Core terms of use, available at


https://doi.org/10.1017/S002966511600063X


Proceedings

oftheNutritionSo

ciety

and having impaired fasting glucose and diabetes, butdid not find any ethnic differences in a multi-ethnicstudy(24).

Association between sleep duration and the risk ofinsulin resistance

One of the key features of T2DM is impaired insulinmediated glucose uptake, otherwise known as insulin re-sistance. This precedes the glucose abnormalities andclinical manifestation of T2DM, often by many years.A selection of both observational and intervention stud-ies have recently explored the relationship between sleepduration and measures of insulin resistance and these aresummarised in Table 3.

Evidence from cross-sectional studies

A small study compared the self-reported sleep durationin insulin-resistant individuals (n 35) with that seen ininsulin-sensitive individuals (n 21). Those with insulin re-sistance slept 43 min less per night (P = 0·018). The studyalso found that 60 % of insulin-resistant participantsslept <7 h in comparison with only 24 % only of insulin-sensitive participants (P = 0·013), though no adjustmentfor potential confounders was performed(25).

Whilst observational studies are of interest, it is well-designed interventional studies that really help us understandthe role of sleep duration in the development of insulin resist-ance and glucose tolerance. There have been a cluster ofthese published recently looking at the metabolic effects ofboth sleep restriction and sleep extension.

Evidence from sleep restriction clinical studies

Multiple small laboratory-based crossover studies onhealthy young participants have looked at the effect ofsleep restriction on insulin sensitivity and glucose toler-ance(26–30). Sleep restriction was associated with reducedinsulin sensitivity in all the studies (except one(30)), withreduced glucose tolerance in one of them(27). The studythat found no effect on glucose or insulin aimed to

Fig. 1. U-shaped relationship between sleep duration and risk oftype 2 diabetes mellitus (adapted from Shan et al.(17)).

Table

2.Cross-sec

tiona

lstudieson

slee

pdurationan

dtheris

kof

dev

elop

ingtype2diabetes

mellitus

(T2D

M)

Autho

r,ye

arCou

ntry

Partic

ipan

tStudydes

ign

Exp

osure

Outco

me

Res

ult

Com

men

t

Jack

son

etal.,

2013

(21)

USA

13094

3ad

ults

aged

18–85

years

from

theNHIS

(yea

rs20

04–20

11)

Cross-sec

tiona

lSub

jectiveslee

pdurationin

a24

hperiod

Self-reportedT2

DM

status

U-sha

ped

asso

ciations

Stron

gera

ssoc

iatio

nin

white

pop

ulation

Bux

ton&

Marce

lli,

2010

(22)

USA

5650

7ad

ults

from

theNHIS

(yea

rs20

04–20

05)

Cross-sec

tiona

lSub

jectiveslee

pdurationin

a24

hperiod

Self-reportedch

ronic

disea

sesinclud

ingT2

DM

U-sha

ped

asso

ciations

Multilev

ellogistic

regres

sion

Wuet

al.,

2015

(23)

China

2518

4ad

ults

mea

nag

e63

years

from

theDon

gfen

g-To

ngjiCoh

ort

stud

y

Cross-sec

tiona

lSub

jectiveslee

pduration

Riskof

metab

olic

synd

romeinclud

ingT2

DM

Noas

sociationwith

nigh

ttim

eslee

pduration

Pos

itive

asso

ciation

with

day

timena

pping

duration

Bak

keret

al.,

2015

(24)

USA

2151

partic

ipan

tag

ed45

–84

years

from

theMulti-EthnicStudyof

Atheros

cleros

is

Cross-sec

tiona

lObjectiveslee

pduration

Diabetes

Noas

sociation

Mod

elad

justed

for

OSA

NHIS,Nationa

lHea

lthInterview

Surve

y;OSA,o

bstructiveslee

pap

noea

.




https://doi.org/10.1017/S002966511600063X



Table 3. Studies on sleep duration and development of insulin resistance

Author, year Country Participant Study design Exposure Outcome Result Comment

Liu et al.,2013(25)

USA Fifty-six non-diabeticoverweight–obeseparticipants

Cross sectional Subjective sleepduration

Insulin sensitivity Positive association Only P-values reported

Broussardet al., 2012(26)

USA Seven young healthyparticipants

Crossover clinical study Sleep restriction Insulin sensitivity Positive association

Nedeltchevaet al., 2009(27)

USA Eleven young-middleaged healthyparticipants

Crossover clinical study Sleep restriction Insulin sensitivity andglucose tolerance

Positive association

Wang et al.,online2016(28)

USA Fifteen young healthynon-obeseparticipants

Crossover clinical study Time-in-bed restrictionby 1–3 h for threenights

Insulin sensitivity andglucose tolerance

Positive associationwith insulinsensitivity

No association withglucose tolerance

Donga et al.,2010(1)(29)

TheNetherlands

Nine healthyparticipants, mean age44·6 years

Crossover clinical study Sleep restriction Insulin sensitivity Positive association

St-Onge et al.,2012(30)

USA Twenty-seven healthyyoung non-obeseadults

Crossover clinical study Time in bed restricted to4 h

Insulin sensitivity No association Participants hadcontrolled diet and lostweight during the study

Robertsonet al., 2013(31)

UK Nineteen healthy younglean men

Randomised controlledtrial

Around 1·5 h sleeprestriction per night for3 weeks

Insulin sensitivity Positive associationonly at the end offirst week

Absence of an overalleffect of sleep restrictionon insulin sensitivity

Broussardet al., 2016(32)

USA Nineteen healthy younglean men

Crossover clinical study 2 d of catch-up sleep Recovery of insulinsensitivity

Positive association

Leproult et al.,2015(33)

Belgium Sixteen healthy youngnon-obese adults withchronic sleeprestriction

Crossover clinical study Around 1 h sleepextension per night for6 weeks

Fasting glucose andinsulin levels

No difference in pre-andpost-interventionlevels

Moderate correlationbetween relative changein sleep duration andrelative change infasting glucose andinsulin levels

A.Alnaji

etal.

516

https://ww

w.cam


Dow


ww




https://doi.org/10.1017/S002966511600063X


Proceedings

oftheNutritionSo

ciety

determine the hormonal effects of restricting sleep dur-ation under controlled feeding conditions(30). A con-trolled diet was provided and the participants lostweight in both the habitual and short sleep phases. It ispossible that in the context of negative energy balance,acute short sleep duration does not lead to a state ofincreased insulin resistance. These studies were all per-formed in controlled laboratory-based environmentsand explored acute and often severe sleep restriction.One recent study has examined participants in theirhome environment to determine if milder and morechronic sleep restriction, akin to daily life, has a role toplay(31). Nineteen healthy, young, normal-weight menwith habitual sleep durations of 7·0–7·5 h and no sleepdisturbances were randomised to either study arm (1·5h reduction in habitual bedtime) or control arm (habitualbedtime) for 3 weeks. Sleep restriction led to a decrease ininsulin sensitivity at the end of first week but then recov-ered to baseline levels.

In summary, these intervention studies are showingthat sleep restriction is associated with the developmentof insulin resistance and impairment of glucose tolerance.Whether these effects are short-lived adaptive responsesto an acute stress, or whether they persist longer termand contribute to the risk of T2DM remains unclear.

Evidence from sleep extension clinical studies

Given that short sleep duration and sleep restriction arelinked to the development of insulin resistance, it is time-ly that a couple of studies are starting to address whethersleep extension has beneficial effects on insulin and glu-cose metabolism.

The first, a crossover study(32) showed that whilst insu-lin sensitivity deteriorates after acute sleep restriction itrecovers after 2 d catch-up sleep. Under laboratory-controlled conditions participants had up to 8·5 h sleepper night for four consecutive nights and up to 4·5 hsleep for another four consecutive nights in a randomisedorder. After the nights of restricted sleep, participantshad two catch-up nights of 10–12 h sleep. Participantshad a 23 % decrease in insulin sensitivity after 4 dsleep curtailment compared with normal sleep.However, insulin sensitivity was restored after 2 d catch-up sleep. Although the study showed that catch-up sleepmay reverse the negative impact of short-term sleep de-privation, the long-term impact of a repeated sleep de-privation and catch-up sleep cycles on diabetes risk isnot known.

The second study investigated whether sleep extensionin the home environment has a positive impact on glu-cose metabolism in healthy adults with chronic sleep cur-tailment(33). Sixteen young healthy non-obese adults,mostly females, had 2 weeks habitual time in bed fol-lowed by 6 weeks 1 h/d extension time in bed. Glucoseand insulin were assayed at the end of the two periods.During the intervention phase participants mostly wentto bed an hour earlier and had higher sleep duration dur-ing weekdays but maintained the same sleep durationduring weekends. The study indicated no significantdifference between pre- and post-intervention fasting

glucose and insulin levels, though no statistics wereshown(34). A moderate linear relationship was reportedbetween the relative change in sleep duration and therelative change in fasting glucose (r= +0·65, P = 0·017)and insulin levels (r =−0·57, P = 0·053); however, wecannot quantify these relationships nor state if theywere statistically significant, without a reported estimatemeasure of associations.

In conclusion, these sleep extension studies, offer tan-talising data supporting a potential benefit of sleep exten-sion on glucose control and insulin sensitivity. Muchmore work is clearly needed in this area.

Association between sleep duration and glycaemiccontrol in patients with diabetes

Given the mounting evidence supporting a relationshipbetween sleep duration and the development of insulin re-sistance and T2DM, it is relevant to consider whethersleep duration has an impact on glycaemic control in peo-ple with established diabetes. Most studies to date arecross-sectional with sample size ranging from as low aseighteen participants to as high as 8543 participants,and these are summarised in Table 4. Most of these studiesassessed glycaemic control using HbA1c except one thatused capillary glucose levels(35). Sleep parameters weremainly self-reported except for three studies that measuredsleep objectively using wrist actigraphy(35–37).

Evidence from cross-sectional studies using subjectivelyreported sleep duration

Okhuma et al. showed that shorter and longer sleep dura-tions were associated with a higher HbA1c level com-pared with a sleep duration of 6·5–7·4 h in T2DMpatients (Fig. 2)(38). Sleep duration including naps wasself-reported. This U-shaped association was not attenu-ated after adjusting for BMI, total energy intake and de-pressive symptoms. A similar U-shaped relation wasreported in a large Korean study, which included partici-pants with both T1DM and T2DM(39). The associationbetween short sleep duration and poor glycaemic controlwas strongest for females and participants below the ageof 65 years. However, these associations was attenuatedafter adjusting for BMI and waist circumference andno association was observed after further adjustmentfor treatment status, duration of diabetes, and daily en-ergy intake. Conversely, only longer sleep duration wasassociated with poor glycaemic control in T2DMpatients in a large Chinese(40) and a smaller Taiwanesestudy(41). Perceived sleep debt but not sleep durationwas positively associated with HbA1c in AfricanAmericans with T2DM without diabetes complicationsand not using insulin(42).

Evidence from cross-sectional studies using objectivelymeasured sleep duration

Using wrist actigraphy to objectively measure sleep para-meters for three consecutive days in the home environ-ment, Trento et al. found no difference in sleep duration




https://doi.org/10.1017/S002966511600063X



Table 4. Studies on sleep and glycaemic control in patients with diabetes

Author,year Country Participant Study design Exposure Outcome Result Comment

Ohkumaet al.,2013(38)

Japan 4870 adults, aged ⩾20years with T2DM

Cross-sectional Subjective sleep durationincluding naps

Glycaemic control(HbA1c)

U-shapedassociations

Kim et al.,2013(39)

Korea 2134 adults, aged > 20years with T1DM orT2DM

Cross-sectional Subjective daily sleepduration


Positiveassociations

J-shaped trend with HbA1c; stronger infemales and in the younger age group (<65years). Association disappear after adjustingfor more covariate in the logistic regressionmodel

Zhenget al.,2015(40)

China 8543 adults, aged ⩾40years with T2DM orimpaired glucosetolerance

Cross-sectional Subjective nighttimesleep duration

Glycaemic control(HbA1c, FPG, PPG)

Positiveassociation withlong sleepduration

Only adjusted means and P-values reportedbut no estimate of association

Tsai et al.,2012(41)

Taiwan Forty-six adults, aged43–83 years withT2DM

Cross-sectional Subjective sleep durationand quality (PSQI)

Glycaemic control,HbA1c

Positiveassociation

Participants with diabetic complication ormajor co-morbidities were excluded.association only with sleep efficiency andPSQI score of 8 or more but not sleepduration

Knutsonet al.,2006(42)

USA 161 African Americans,mean age 57 yearswith T2DM

Cross-sectional Subjective sleep durationand sleep quality,modified PSQI andperceived sleep debt


Positiveassociation

Sleep debt association only in participantswithout diabetic complication or not usinginsulin. Sleep quality only in participants withdiabetic complication or using insulinassociation

Trentoet al.,2008(36)

Italy Forty-sevenmiddle-aged adultswith T2DM and 23healthy controls

Cross-sectionalstudy

Objective sleepparameters; durationand quality using wristactigraphy

Glycaemic control(HbA1c) in T2DMgroup

Positiveassociation

Weak negative correlation with sleepefficiency and mild positive correlation withmoving time while asleep. No estimatemeasures of association reported

Borel et al.,2013(37)

France Seventy-nine adults,median age 40 yearswith T1DM

Cross-sectionalstudy

Objective sleepparameters using wristactigraphy


Positiveassociation

Baroneet al.,2015(35)

Brazil Eighteen young adult,aged 20–38 years withT1DM

Cross-sectional Objective sleepmeasures using wristactigraphy

Glycaemic control(average glucosefrom glucometerreading)

No association Methodological issues

FPG, fasting plasma glucose; PPG, postprandial glucose; PSQI, Pittsburgh Sleep Quality Index; T2DM, type 2 diabetes mellitus.

A.Alnaji

etal.

518

https://ww

w.cam


Dow


ww




https://doi.org/10.1017/S002966511600063X


Proceedings

oftheNutritionSo

ciety

between T2DM and control subjects(36). T2DM sleepquality was found to correlate slightly with glycaemic con-trol, while no correlation with sleep duration wasreported. Conversely, Borel et al. shown that T1DMpatients with shorter sleep duration (<6·5 h) had a higherHbA1c than those with longer sleep duration (>6·5 h;mean 8·5 v. mean 7·7 %; P= 0·001)(37). In an adjusted re-gression model shorter sleep duration was associated with0·64 % increase in mean HbA1c level compared withlonger sleep duration but no 95 % CI or P-value werereported. Participants with short sleep duration werealso more likely to have obstructive sleep apnoea and asthis was not considered in the analysis, part of the differ-ence reported could be attributed to it.

Finally Barone et al. assessed the association betweenobjectively measured sleep parameters using wrist acti-graphy and glycaemic control using capillary glucoselevels from glucometer in a group of eighteen youngadults with T1DM(35). They showed a positive correl-ation between the average amount of rest at night andboth average glucose levels (r= 0·5404; P = 0·0697) andglycaemic variability (r= 0·5706; P= 0·0527). No esti-mate measure of the association nor adjustment for anypotential confounders were made. Moreover, the averagenight rest duration was calculated from 10 d actigraphy,which may have included two weekends for some partici-pants and only one weekend for others, and thus it willbe inevitably incomparable between participants.

In summary, in people with diabetes there also appearsto be evidence of an association between both short andlong sleep durations and worse glucose control.However, these studies are cross-sectional and so evi-dence of causality cannot be inferred. A complicatingfactor when interpreting the relationship between glucoseand sleep in people with diabetes is that extremely poorglucose control is well recognised to cause polyuria, poly-dypsia and nocturia meaning they are awake during thenight. Reverse causality cannot be excluded in these stud-ies as they do not distinguish the severity of glucose con-trol and are likely to include participants experiencing

some of these osmotic symptoms. Randomised clinicaltrials with exposure to sleep duration modification (re-striction or extending) and robust methods of assessingtemporal glucose across the 24 h day and night(43) areneeded to yield more definitive answers.

Conclusions

The recently published literature of both observationaland interventional studies strongly supports a role forboth short and long sleep durations in the developmentof insulin resistance and T2DM. There are insufficientsleep intervention studies to determine whether this riskis modifiable long term. In people with established dia-betes the published literature supports an association be-tween poor glucose control and both short and long sleepdurations. However, there are no studies that determinethe causal direction of this relationship in people withdiabetes, nor whether sleep interventions may offerbenefit in achieving glucose control. This is a fertilefield for future research.

Financial support

A. A. receives financial support from the Ministry ofHealth, Saudi Arabia.

Conflicts of interest

None.

Authorship

E. S. gave the talk at the RSM and conceived the article.A. A. and E. S. drafted the original document. Allauthors reviewed and commented on the draft prior todeveloping the final document.

References

1. Prasai MJ, George JT & Scott EM (2008) Molecularclocks, type 2 diabetes and cardiovascular disease. DiabVasc Dis Res 5, 89–95.

2. Prasai MJ, Pernicova I, Grant PJ et al. (2011) An endocri-nologist’s guide to the clock. J Clin Endocrinol Metab 96,913–922.

3. Tan E & Scott EM (2014) Circadian rhythms, insulin ac-tion, and glucose homeostasis. Curr Opin Clin NutrMetab Care 17, 343–348.

4. Knutson KL, Van Cauter E, Rathouz PJ et al. (2010)Trends in the prevalence of short sleepers in the USA:1975–2006. Sleep 33, 37–45.

5. National Sleep Foundation (2005) Adult sleep habits andstyles. https://sleepfoundation.org/sleep-polls-data/sleep-in-america-poll/2005-adult-sleep-habits-and-styles (accessedApril 2016).

6. Barnes M, Byron C & Beninger K (2013) Sleep patternsand health Analysis of the Understanding Society dataset.

Fig. 2. Higher HbA1c observed in shorter and longer sleepduration in Japanese type 2 diabetes mellitus patients comparedwith 6·5–7·4 h sleep duration (*P < 0·05; **P < 0·01), adapted fromOkhuma et al.(38).




https://doi.org/10.1017/S002966511600063X


Proceedings

oftheNutritionSo

ciety

http://www.natcen.ac.uk/media/29127/sleep-patterns-and-health.pdf (accessed April 2016).

7. Yaggi HK, Araujo AB & McKinlay JB (2006) Sleep dur-ation as a risk factor for the development of type 2 dia-betes. Diab Care 29, 657–661.

8. Gangwisch JE, Heymsfield SB, Boden-Albala B et al.(2007) Sleep duration as a risk factor for diabetes incidencein a large US sample. Sleep 30, 1667–1673.

9. Kowall B, Lehnich A-T, Strucksberg K-H et al. (2016)Associations among sleep disturbances, nocturnal sleepduration, daytime napping, and incident prediabetes andtype 2 diabetes: the Heinz Nixdorf Recall study. SleepMed (Epublication ahead of print version).

10. Holliday EG, Magee CA, Kritharides L et al. (2013) Shortsleep duration is associated with risk of future diabetes butnot cardiovascular disease: a prospective study andmeta-analysis. PLoS ONE 8, e82305.

11. Rafalson L, Donahue RP, Stranges S et al. (2010) Shortsleep duration is associated with the development ofimpaired fasting glucose: the Western New York HealthStudy. Ann Epidemiol 20, 883–889.

12. Gutierrez-Repiso C, Soriguer F, Rubio-Martin E et al.(2014) Night-time sleep duration and the incidence of obes-ity and type 2 diabetes. Findings from the prospectivePizarra study. Sleep Med 15, 1398–1404.

13. Kita T, Yoshioka E, Satoh H et al. (2012) Short sleep dur-ation and poor sleep quality increase the risk of diabetes inJapanese workers with no family history of diabetes. DiabCare 35, 313–318.

14. Tuomilehto H, Peltonen M, Partinen M et al. (2009) Sleepduration, lifestyle intervention, and incidence of type 2 dia-betes in impaired glucose tolerance: the Finnish diabetesprevention study. Diab Care 32, 1965–1971.

15. Ferrie JE, Kivimaki M, Akbaraly TN et al. (2015) changein sleep duration and type 2 diabetes: the Whitehall IIstudy. Diab Care 38, 1467–1472.

16. Cespedes EM, Bhupathiraju SN, Li Y et al. (2016)Long-term changes in sleep duration, energy balance andrisk of type 2 diabetes. Diabetologia 59, 101–109.

17. Shan Z, Ma H, Xie M et al. (2015) Sleep duration and riskof type 2 diabetes: a meta-analysis of prospective studies.Diab Care 38, 529–537.

18. Anothaisintawee T, Reutrakul S, Van Cauter E et al.(2015) Sleep disturbances compared to traditional risk fac-tors for diabetes development: systematic review andmeta-analysis. Sleep Med Rev 30, 11–24.

19. Archie JP Jr (1981) Mathematic coupling of data: a com-mon source of error. Ann Surg 193, 296–303.

20. Tu Y-K, Maddick IH, Griffiths GS et al. (2004)Mathematical coupling can undermine the statistical as-sessment of clinical research: illustration from the treatmentof guided tissue regeneration. J Dent 32, 133–142.

21. Jackson CL, Redline S, Kawachi I et al. (2013) Associationbetween sleep duration and diabetes in black and whiteadults. Diab Care 36, 3557–3565.

22. Buxton OM & Marcelli E (2010) Short and long sleep arepositively associated with obesity, diabetes, hypertension,and cardiovascular disease among adults in the UnitedStates. Soc Sci Med 71, 1027–1036.

23. Wu J, Xu G, Shen L et al. (2015) Daily sleep duration andrisk of metabolic syndrome among middle-aged and olderChinese adults: cross-sectional evidence from theDongfeng–Tongji cohort study.BMCPublicHealth 15, 178.

24. Bakker JP, Weng J, Wang R et al. (2015) Associations be-tween obstructive sleep apnea, sleep duration, and abnor-mal fasting glucose. The multi-ethnic study ofatherosclerosis. Am J Respir Crit Care Med 192, 745–753.

25. Liu A, Kushida CA & Reaven GM (2013) Habitual shor-tened sleep and insulin resistance: an independent relation-ship in obese individuals. Metabolism 62, 1553–1556.

26. Broussard JL, Ehrmann DA, Van Cauter E et al. (2012)Impaired insulin signaling in human adipocytes after ex-perimental sleep restriction: a randomized, crossoverstudy. Ann Intern Med 157, 549–557.

27. Nedeltcheva AV, Kessler L, Imperial J et al. (2009)Exposure to recurrent sleep restriction in the setting ofhigh caloric intake and physical inactivity results inincreased insulin resistance and reduced glucose tolerance.J Clin Endocrinol Metab 94, 3242–3250.

28. Wang X, Greer J, Porter RR et al. (2016) Short-term mod-erate sleep restriction decreases insulin sensitivity in younghealthy adults. Sleep Health 2, 63–68.

29. Donga E, van Dijk M, van Dijk JG et al. (2010) A singlenight of partial sleep deprivation induces insulin resistancein multiple metabolic pathways in healthy subjects. J ClinEndocrinol Metab 95, 2963–2968.

30. St-Onge MP, O’Keeffe M, Roberts AL et al. (2012) Shortsleep duration, glucose dysregulation and hormonal regula-tion of appetite in men and women. Sleep 35, 1503–1510.

31. Robertson MD, Russell-Jones D, Umpleby AM et al.(2013) Effects of three weeks of mild sleep restriction imple-mented in the home environment on multiple metabolicand endocrine markers in healthy young men.Metabolism 62, 204–211.

32. Broussard JL, Wroblewski K, Kilkus JM et al. (2016) Twonights of recovery sleep reverses the effects of short-termsleep restriction on diabetes risk. Diab Care 39, e40–e41.

33. Leproult R, Deliens G, Gilson M et al. (2015)Beneficial impact of sleep extension on fasting insulin sen-sitivity in adults with habitual sleep restriction. Sleep 38,707–715.

34. Jones B & Kenward MG (2014) Design and Analysisof Crossover Trials. vol. 138. Boca Raton: Taylor &Francis.

35. BaroneMT,WeyD, Schorr F et al. (2015) Sleep and glycemiccontrol in type 1 diabetes. Arch Endocrinol Metab 59, 71–78.

36. Trento M, Broglio F, Riganti F et al. (2008) Sleep abnor-malities in type 2 diabetes may be associated with glycemiccontrol. Acta Diabetol 45, 225–229.

37. Borel AL, Pepin JL, Nasse L et al. (2013) Short sleep dur-ation measured by wrist actimetry is associated with dete-riorated glycemic control in type 1 diabetes. Diab Care36, 2902–2908.

38. Ohkuma T, Fujii H, Iwase M et al. (2013) Impact of sleepduration on obesity and the glycemic level in patients withtype 2 diabetes: the Fukuoka Diabetes Registry. Diab Care36, 611–617.

39. Kim BK, Kim BS, An SY et al. (2013) Sleep duration andglycemic control in patients with diabetes mellitus: KoreaNational Health and Nutrition Examination Survey2007–2010. J Korean Med Sci 28, 1334–1339.

40. Zheng Y, Wang A, Pan C et al. (2015) Impact of nightsleep duration on glycemic and triglyceride levels inChinese with different glycemic status. J Diab 7, 24–30.

41. Tsai YW, Kann NH, Tung TH et al. (2012) Impact of sub-jective sleep quality on glycemic control in type 2 diabetesmellitus. Fam Pract 29, 30–35.

42. Knutson KL, Ryden AM, Mander BA et al. (2006) Role ofsleep duration and quality in the risk and severity of type 2diabetes mellitus. Arch Intern Med 166, 1768–1774.

43. Law GR, Secher A, Temple R et al. (2015) Analysis of con-tinuous glucose monitoring in pregnant women with dia-betes: distinct temporal patterns of glucose associatedwith infant macrosomia. Diab Care 38, 1319–1325.

A. Alnaji et al.520



https://doi.org/10.1017/S002966511600063X


the role of sleep duration in diabetes and glucose control … · tween sleep duration and risk of...

Documents