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Influence of pulmonary rehabilitation on the sleep patterns

of patients with chronic obstructive pulmonary disease*

RENATA CLAUDIA ZANCHET*, CARLOS ALBERTO DE ASSIS VIEGAS**(TE SBPT)

TEREZINHA DO SOCORRO MACÊDO LIMA**(TE SBPT)

Background: Pulmonary Rehabilitation (PR) improves the quality of life of chronic obstructive pulmonary

disease (COPD) patients. However, the influence of PR on the sleep pattern of these patients is unknown.

Objective: To evaluate the influence of PR on the sleep patterns of patients with COPD.

Method: A t ot al of 27 pat ien t s (22 men / 5 women ) were su bmit t ed t o polysomn ographic, gasomet ric

an d an t hropomet ric st u dies before an d aft er six weeks of PR an d were evalu at ed u sin g t he Epwort h

Sleepin ess Scale. The resu lt s were an alyzed u sin g paired St u den t ’s t- t est , ANOVA an d Newman - Keu ls

mu lt iple comparison t est .

Results: Mean age was 63.3 ± 5.3 years, mean FEV1 was 54.8 ± 25.4% of predict ed, mean FEV1/ FVC

was 49.9 ± 12.0% of predict ed, mean rest in g PaO2 was 69.7 ± 7.3 mmHg, an d mean rest in g SaO2 was

93.7 ± 2.1%. Polysomn ography revealed sleep pat t ern s t o be fragmen t ed, wit h frequ en t wakin g an d redu ced slow- wave sleep, as well as oxygen desat u rat ion . The most sign ifican t drops in oxygen saturation occurred during rapid eye movement sleep. No significant differences were observed between

pre- an d post - PR valu es for t he ot her variables st u died (p > 0.05).

Conclusion: In the group of patients studied, PR did not alter sleep patterns.

Key words: Sleep. Pulmonary Disease. Chronic Obstructive. Lung Diseases, rehabilitation.

*St u dy carried ou t at t he Un iversidade Cat ólica de Brasilia (UCB) an d at t he **Hospit al Un iversit ário de Brasília (HUB), Brasilia, DF

Correspon den ce t o: Ren at a Clau dia Zan chet . Un iversidade Cat ólica de Brasília. Cu rso de Fisiot erapia. QS 07, lot e 01, Águ as Claras. CEP: 71966-7 0 0 Tag u at in g a - DF. Brazil

Ph o n e: 5 5 - 61 - 3 5 6 9 2 0 5 – Fa x: 5 5 - 61 - 3 5 6 1 8 0 0 - E- m a il: ren a t a c@ u cb.b r

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Abbreviations used in this paper: AI – Awaken in g in dex AHI – Apn ea- hypopn ea in dex BMI – Body mass in dex

COPD – Chron ic obst ru ct ive pu lm on ary disease FEV1 – Forced expirat ory volu me in on e secon d FVC – Forced vit al capacit y

NREM – Non - rapid eye movemen t OSAS – Obst ru ct ive sleep apn ea syn drome PaCO2 – Art erial carbon dioxide t en sion Pa O2 – Art erial oxygen t en sion PR – Pu lm o n ary reh ab ilit at io n REM – Rapid eye movemen t SaO2 – Art erial oxygen sat u rat ion Sp O2 – Art erial oxygen sat u rat ion TST – Tot al sleep t ime

INTRODUCTION

Depen din g on t he t ype of exercise, du rat ion , t ime of day performed an d frequ en cy, physical a c t ivit y m a y in f lu e n c e s le e p in h e a lt h y in dividu als(1,2). In a met a- an alysis st u dy(1), it was

report ed t hat acu t e an d chron ic physical exercise resu lt ed in in creases in delt a sleep (st ages 3 an d 4) and total sleep time (TST) and decreases in sleep lat en cy an d rapid eye movemen t (REM) sleep.

Kin g et al. (3) evalu at ed t he effect of 16 weeks

of moderat ely- in t en se exercise on 67 in dividu als aged 50 t o 76 who were seden t ary an d report ed moderate sleep complaints: either awakening during t he n ight or havin g difficu lt y in goin g t o sleep. The authors demonstrated that, after the program, the quality of sleep improved for these individuals. In addition, it has been shown that, although there is a correlation between arterial oxygen saturation (SpO2) du rin g sleep an d physical exercise(7 ,8 ), a

decrease in oxygen sat u rat ion is n ot predict ive of n o ct u rn al o xyg en d esat u rat io n , sin ce a slig h t decrease in SpO2 du rin g physical act ivit y does n ot ru le o u t a m o re d ram at ic d ecrease in o xyg en sat u rat ion du rin g t he n ight(7,9).

On the other hand, studies have shown that, in t h e ca se o f p a t ien t s d ia g n o sed wit h ch ro n ic obst ru ct ive pu lmon ary disease (COPD), n oct u rn al hypoxemia an d hypercapn ia are closely relat ed t o periods of REM sleep(4,5). The lowest nocturnal SpO

2

levels have been found in patients presenting more severe diu rn al hypoxemia an d lon ger REM sleep periods(6).

In addition to gas exchange alterations, patients diagnosed with COPD present other changes in the q u a lit y o f sleep(10 ,11 ). Sin ce sleep t en d s t o b e

fragmen t ed by frequ en t awaken in gs, t here is a decrease in delt a an d REM sleep(12), as well as a

decrease in TST an d a great er n u mber of sleep-st age chan ges(14,15). However, sleep dist u rban ce is

freq u en t ly ig n o red b y m o st p h ysician s in t h e evaluation of patients diagnosed with COPD, even in study protocols designed to evaluate the quality of life of t hese pat ien t s(12).

Although there have been many studies of COPD pat ien t sleep pat t ern s, t he relat ion ship bet ween p u lm o n a ry reh a b ilit a t io n (PR) a n d t h e sleep patterns of these patients has not yet been studied. Therefore, t he object ive of t he presen t st u dy was t o det ermin e t he in flu en ce of PR on t he sleep patterns of patients with COPD.

METHOD

In a n on - ran domized, open clin ical t rial, 35 pat ien t s wit h COPD were evalu at ed. Of t hose, 8 patients were excluded: 3 for presenting obstructive sleep apnea syndrome (OSAS), 2 for refusing to be submitted to a repeat polysomnography following PR, 1 for developing an orthopedic problem during training sessions, 1 for presenting severe arrhythmia d u rin g t h e p ro g ra m , a n d 1 f o r p re se n t in g u n con t rolled art erial hypert en sion . Therefore, t he st u dy sample con sist ed of 27 pat ien t s: 22 males an d 5 females. The st u dy period was from Au gu st 2001 t o April 2003. Diagn osis of COPD was made in accordance to the criteria defined by The Global In it iat ive for Chron ic Obst ru ct ive Lu n g Disease(16).

An apnea- hypopnea index (AHI) greater than 5 per hou r of sleep was t he crit eria u sed for classifyin g patients as suffering from OSAS(17).

This st u dy in clu ded pat ien t s wit h clin ically st able COPD who were former smokers (smoke-free for at least 3 months). Patients were excluded if t h e y p re se n t e d OSAS, c a rd io va sc u la r o r orthopedic diseases that would prevent them from p erfo rm in g t h e exercises p ro p o sed in t h e PR prot ocol, or ot her comorbidit ies t hat wou ld pu t t hem at risk du rin g exercise.

The Ethics Research Committee of the Hospital Un iversit ário de Brasilia approved t he st u dy. All patien ts gave written in formed con sen t.

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Pulmonary function: absolute values of forced vit al capacit y (FVC), forced expirat ory volu me in o n e seco n d (FEV1), a n d FEV1/ FVC ra t io were measu red (Vmax

22 series spiromet er; Sen sor Medics, Yorba Linda, CA, USA). Relative predictive valu es based on gen der, age an d height were calcu lat ed con siderin g t he valu es described by Knudson et al.(18) Spirometry tests were performed

in accordan ce wit h t he gu idelin es est ablished by t he American Thoracic Societ y(19).

Art e rial blo o d g as an aly s is : Va lu es were det ermin ed for art erial oxygen t en sion (PaO2), arterial carbon dioxide tension (PaCO2) and arterial oxygen saturation (SaO2) using a Ciba Corning 278 Gas Syst em (Ciba Corn in g, Diagn ost ics Corp., Medfield, MA, USA).

Anthropometry: Body mass in dex (BMI) was

calculated using the formula: weight/ height2 (kg/

m2). Neck circumference (cm) was measured above

t he cricoid cart ilage.

All- night polysomnography: Parameters were

m o n it o re d u s in g e le c t ro e n c e p h a lo g ra p h y, e l e c t r o c a r d i o g r a p h y, e l e c t r o m y o g r a p h y, electroculography and nasal/oral airflow thermistry, as well as by recording body position, snoring, ribcage/abdominal movement and arterial oxygen saturation (SpO2). These measurements were taken using an Alice 3® digital polysomnographic system

(Healt hdyn e Techn ologies, Mariet t a, GA, USA). Traditional polysomnographic variables were also evaluated in accordance with the Rechtschaffen & Kales method(20). We also included the awakening

index (AI), which is the number of awakenings divided by sleep period time and multiplied by 60,

thus representing the number of awakenings per hour of sleep.

Epworth Sleepiness Scale: Prior to and following

t h e PR p ro g ra m , a ll p a t ie n t s co m p le t e d t h e sleepin ess scale qu est ion n aire creat ed by John s(21).

Physical practice: The PR program con sist ed

of t hree (morn in g) session s a week for 6 weeks. Each PR program exercise session was con du ct ed in a cco rd a n ce wit h t h e g u id elin es d evised b y Rodrigues et al.(22) The effect of PR on patients was

eva lu a t ed u sin g t h e 6 - m in u t e wa lk t est a n d in crem en t al exercise t est s in vo lvin g t h e u p p er extremities.

Statistics: Valu es of t he st u died variables are

presen t ed as mean s ± st an dard deviat ion (SD). Paired Student’s t- test was used for the comparison of variables prior to and following the PR program. Differen ces bet ween SpO2 levels du rin g n oct u rn al vigilan ce, n on - REM (NREM) sleep, an d REM sleep were an alyzed u sin g ANOVA an d Newman - Keu ls mu lt iple comparison t est . Valu es of p < 0.05 were considered statistically significant.

RESULTS

The mean age of t he pat ien t s st u died was 63.3 ± 5.3, ran gin g from 54 t o 72.

Values for spirometric, blood gas analysis and anthropometric variables prior to and following the PR program are shown in Table 1. There were no statistically significant differences among these variables (p > 0.05). Polysomn ography revealed fragmen t ed sleep pat t ern s, redu ced delt a sleep an d less hemoglobin desat u rat ion . Prior t o PR, SpO2 du rin g REM sleep

TABLE 1

Spiromet ric, gas exchan ge, an t hropomet ric an d Epwort h sleepin ess scale valu es of pat ien t s wit h COPD before an d aft er t he PR program

Before PR After PR

FVC (%) 85.0 ± 26.6 87.4 ± 22.5

FEV1 (%) 54.8 ± 25.4 55.0 ± 22.5

FEV1/ FVC (%) 49.9 ± 12.0 49.5 ± 12.4

PaO2 (mmHg) 69.7 ± 7.3 71 ± 8.7

PaCO2 (mmHg) 35.0 ± 4.8 34.7 ± 4.6

Dayt ime SpO2 (%) 93.7 ± 2.1 93.7 ± 2.2

BMI (kg/ m2) 24.6 ± 4.2 24.6 ± 4.1

Neck circu mferen ce (cm) 37.5 ± 3.7 37.9 ± 3.7

Epwort h sleepin ess scale 9 ± 4 9 ± 4

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Fig ure 1 – Comparison of SpO2 valu es du rin g n oct u rn al vigilan ce an d du rin g sleep

was sign ifican t ly lower (88 ± 4.2%) t han du rin g n oct u rn al vigilan ce (90 ± 2.9%) or NREM sleep (89.4 ± 3.3%) (p < 0.05). In t u rn , SpO2 du rin g NREM sleep was sign ifican t ly lower t han du rin g n oct u rn al vigilan ce (p < 0.05) (Fig. 1).

There was no statistically significant difference between polysomnographic variables and daytime drowsiness measured prior to and following PR (p > 0.05) (Table 2).

As for PR, there was a significant increase in the distance covered in the 6- minute walk test as well as in the maximum load achieved in the incremental exercise test of the upper extremities (p < 0.05).

DISCUSSION

Th e d esig n o f t h e p resen t st u d y m a d e it p o ssib le t o ch aract erize t h e sleep p at t ern s o f pat ien t s wit h COPD. When we compared t he sleep pat t ern s of t he pat ien t s in t he presen t st u dy wit h t hose of healt hy adu lt s(2 3 ), we realized t hat sleep

pat t ern s of pat ien t s wit h COPD were fragmen t ed, charact erized by in creased vigilan ce t hrou ghou t t h e e n t ir e s le e p p e r io d a n d b y f r e q u e n t a wa ken in g s. We a lso n o t iced t h a t sleep wa s in efficien t , an d t h at it was d ifficu lt fo r p at ien t s

t o fall asleep (in creased sleep o n set lat en cy an d REM sleep) an d t o move in t o deeper sleep st ages (in creased p ercen t ag es o f st ag e 1 NREM sleep an d decreased percen t ages of delt a sleep). These d at a are in acco rd an ce wit h resu lt s rep o rt ed b y o t h er a u t h o rs(1 2 - 1 5 ).

In a review art icle, George(24) called at t en t ion

t o in somn ia in pat ien t s wit h COPD, corroborat in g the high incidence of awakenings and the difficulty in fallin g asleep observed in t he presen t st u dy.

TABLE 2

Polysomn ographic valu es for pat ien t s wit h COPD before an d aft er t he PR program.

Prior t o PR Aft er PR

AHI (events/hour) 2.3 ± 3.9 2.8 ± 5.2

Sn orin g period (min u t es) 10.9 ± 9.1 9.8 ± 7.3

Regist rat ion period (min u t es) 486.4 ± 46.0 483.2 ± 32.4

TSP (minutes) 441.9 ± 67.1 442.7 ± 39.1

TST (minutes) 321.3 ± 75.8 323.1 ± 69.1

TST/ TSP (%) 72.8 ± 13.9 72.7 ± 12.7

Vigilan ce du rin g TSP (%) 27.2 ± 13.9 27.3 ± 12.7

Sleep lat en cy (min u t es) 28.8 ± 28.5 27.3 ± 23.1

REM sleep lat en cy (min u t es) 113.9 ± 73.0 105.6 ± 56.3

St age chan ges 126.8 ± 35.2 117.1 ± 33.6

Movement episodes 40.1 ± 14.6 37.2 ± 14.3

AI (events/hour) 30.3 ± 10.0 30.9 ± 8.2

St age 1 (%) 20.7 ± 7.6 19.7 ± 8.8

St age 2 (%) 49.0 ± 8.3 48.7 ± 9.5

Delt a sleep (%) 8.8 ± 4.9 9.5 ± 7.4

REM sleep (%) 19.9 ± 6.4 20.6 ± 7.0

SpO2 t ime < 90% (%) 40.1 ± 37.8 45.1 ± 37.2

SpO2 (%) – mean du rin g vigilan ce 90.0 ± 2.9 90.6 ± 2.0

SpO2 (%) – mean du rin g NREM sleep 89.4 ± 3.3 89.7 ± 2.2

SpO2 (%) – mean du rin g REM sleep 88.0 ± 4.2 87.5 ± 3.6

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Some pat ien t s diagn osed wit h COPD presen t c o n c o m it a n t OSAS. De sig n a t e d a n o ve rla p syndrome, COPD concomitant with OSAS may result in a worsening of nocturnal hypoxemia(10,11). In our

st u d y, 8 .6 % o f t h e p o p u la t io n st u d ie d wa s diagnosed with this syndrome. This figure is similar to that reported by Chaouat et al.(25), who reported

t hat 11% of t he 265 COPD pat ien t s st u died also presen t ed OSAS. It is difficu lt t o evalu at e t he real associat ion bet ween COPD an d OSAS, prin cipally d u e t o t wo m ain fact o rs. First , t h ere m ay b e problems in t he t riage of pat ien t s. For example, Guilleminault et al.(26) evaluated patients with COPD

who, in most cases, had been referred t o t he sleep clin ic du e t o excessive dayt ime sleepin ess. These au t hors report ed t hat 84% of t he pat ien t s were diagn osed wit h overlap syn drome. The secon d fact or is t he lack of con sen su s amon g au t hors regardin g t he n u mber of apn ea an d hypopn ea episodes t hat charact erize OSAS(24,27- 30).

In review articles, Douglas(11) and McNicholas(31)

defin ed some fact ors t hat may be respon sible for hypoxemia during sleep in patients diagnosed with COP D. Th e s e f a c t o r s in c lu d e a lve o la r hypoven t ilat ion , decreased fu n ct ion al residu al capacity, and changes in the ventilation/perfusion rat io. Du e t o t he effect of t he oxyhemoglobin dissociation curve, patients with hypoxemia present h ig h e r d e s a t u r a t io n le ve ls in r e la t io n t o h yp o ven t ila t io n t h a n d o p a t ien t s p resen t in g normoxemia(31).

The present study confirmed data in the literature showing that there is a decrease in SpO2 during sleep, and that the highest desaturation level is reached during REM sleep in patients with COPD(14,27).

Considering the objectives of the present study, we noticed that, although the 6- week PR program had a posit ive effect on exercise performan ce, it had n o impact on t he polysomn ographic dat a o b t a in e d fro m t h e 2 7 p a t ie n t s wit h COPD. Therefore, our results revealed that COPD patients m ight respon d t o exercise differen t ly t han do normal individuals, whose quality of sleep improves aft er performin g physical act ivit ies(1,3).

Ku b it z et a l.(1 ), in a m et a - a n a lyt ic review,

report ed t hat bot h acu t e exercise (exercisin g vs. n ot exercisin g) an d chron ic exercise (pract it ion ers vs. n on - pract it ion ers, at hlet es vs. n on - at hlet es) promot e in creased delt a sleep an d in creased TST, as well as redu cin g lat en cy of sleep on set an d of

REM sleep. However, the effect of chronic exercise on sleep is more ext en sive t han t hat of acu t e e xe rcise . In a d d it io n , lo n g - d u ra t io n a e ro b ic exercises (u n less pract iced t oo close t o bedt ime) have a greater impact on sleep quality. The studies u se d in t h is m e t a - a n a lysis re fe r t o e xe rcise p r a c t ic e d b e t w e e n 2 p m t o 7 p m , o f approximat ely on e hou r in du rat ion .

According to Horne & Staff(32), there may be an

in crease in slow- wave sleep when ever t here is an in crease in body t em perat u re du rin g exercise. However, t his hypot hesis is debat able, sin ce body t e m p e r a t u r e d e c r e a s e s t o it s b a s a l va lu e approximat ely 2 hou rs aft er exercise. You n gst edt et al.(2) con clu ded that body temperatu re does n ot

moderat e delt a sleep aft er exercise.

On e o f t h e f a c t o r s t h a t m i g h t h a v e co n t rib u t ed t o t h e fa ct t h a t we o b served n o effect o f t h e PR o n t h e sleep p a t t ern s o f o u r p a t ien t s wa s t h e sh o rt d u ra t io n o f t h e p ro g ra m (o n ly 6 weeks) a n d o f t h e in d ivid u a l sessio n s (3 0 m i n u t e s e a c h ). In s t u d i e s i n v o l v i n g in d ivid u a ls n o t d ia g n o se d w it h p u lm o n a ry d isea ses, exercise sessio n s a re t yp ica lly lo n g er. H o w e ve r, w e b e l i e v e t h a t t h e p r i n c i p a l d e t e rm in a n t o f h ig h e r q u a lit y p o st - e xe rcise sleep in t h ese p a t ien t s is t h e t im e o f t h e d a y a t wh ich t h e exercises a re p erfo rm ed . Driver & Ta ylo r(3 4 ) co rro b o ra t ed t h is h yp o t h esis, st a t in g

t h a t wh en h ea lt h y in d ivid u a ls exercise in t h e morn in g, in depen den t ly of in t en sit y or du rat ion , t h e re is p ro b a b ly n o e f f e ct o n t h e ir sle e p p a t t ern s, d ifferen t ly t h a n wh en t h ey p ra ct ice exercises la t e in t h e a ft ern o o n . In a d d it io n , a ll o f t h e st u d ies a n a lyzed in t h e Ku b it z et a l.(1 )

m et a - a n a lysis rep o rt ed o n exercises p erfo rm ed in t h e a ft ern o o n o r in t h e even in g .

In addition, we must bear in mind that, all these fa ct o rs t h a t m a y in flu en ce sleep p a t t ern s notwithstanding, patients with chronic lung disease may also presen t chron ic hypoxemia. As previou sly mentioned, hypoxemia may lead to sleep fragmentation. Since PR does not affect this condition, sleep patterns would be expected to remain unchanged.

In light of t his, we believe t hat addit ion al st u dies in volvin g more prolon ged periods of PR, con du cted at variou s times of day for the pu rpose of comparison , shou ld be carried ou t .

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2 2 . Ro d rig u e s SL, Vie g a s CAA, Lim a T. Efe t ivid a d e d a rea b ilit a çã o p u lm o n a r co m o t ra t a m en t o co a d ju va n t e d a d o en ça p u lm o n a r o b st ru t iva crô n ica . J Pn eu m o l 2 0 0 2 ;2 8 : 6 5 - 7 0 .

2 3 . Gu io t M. P o lisso n o g ra f ia . In : Re im ã o R. So n o – e st u d o a b ra n g e n t e . 2 º e d . Sã o P a u lo : At h e n e u , 2 e d . , 1 9 9 6 ; 9 2 - 8 .

2 4 . Ge o rg e , C.F.P. Pe rsp e ct ive o n t h e m a n a g e m e n t o f in somn ia in pat ien t s wit h chron ic respirat ory disorders. Sleep 2000;23 :S31- 5.

2 5 . Ch a o u a t A, We t z e n b lu m E, Krie g e r J , Ifo u n d z a T, Oswald M, Kessler R. Associat ion of chron ic obst ru ct ive p u lm o n a ry d isea se a n d sleep a p n ea syn d ro m e. Am J Respir Crit Care Med 1995;151: 82- 6.

2 6 . Gu ille m in a u t C, Cu m m in ske y J , Mo t t a J . Ch ro n ic o b st ru ct ive a irflo w d isea se a n d sleep st u d ies. Am J Respir Crit Care Med 1980;122:397- 406.

27. Don n er CF, Braghiroli A, Sacco C, Caron e M. Non - apn oeic n o ct u rn a l O2 d e sa t u ra t io n s in COPD p a t ie n t s wit h d a yt im e b o r d e r lin e h yp o x a e m ia . Eu r Re s p ir J 1 9 9 0 ;11 :5 3 8 S- 4 8 S.

2 8 . No rm a n J F, Vo n Esse n SG, Fu ch s RH, McEllio t M. Exercise t ra in in g effect o n o b st ru ct ive sleep a p n ea syn d ro m e. Sleep Res On lin e 2 0 0 0 ;3 :1 2 1 - 9 .

2 9 . Ch a o u a t A, We t z e n b lu m E, Ke s s le r R, Sc h o t t R, Charpen t ier C, Levi- Valensi P, et al. Ou t come of COPD pat ien t s wit h mild dayt ime hypoxaemia wit h or wit hou t s le e p - r e la t e d o x yg e n d e s a t u r a t io n . Eu r Re s p ir J 2 0 01 ; 1 7 : 8 4 8 - 5 5 .

3 0 . Ma yo s M, P la z a LH, Fa rré A, Mo t a Y, Sn a ch is J . Efet o d e la o xig en o t era p ia n o ct u rn a en el p a cien t e c o n s í n d r o m e d e a p n e a - h i p o n e a d e l s u e ñ o y l i m i t a c i ó n c r ó n i c a a l f l u j o a é r e o . Ar c h Bro n c o n e u m o l 2 0 01 ; 3 7 : 6 5 - 8 .

31 . Mc Nic h o la s WT. Im p a c t o f sle e p in COP D. Ch e st 2 0 0 0 ;11 7 :4 8 S- 5 3 S.

32. Horn e JA, St aff LHE. Exercise an d sleep: body- heat in g effect s. Sleep 1 9 8 3 ;6 :3 6 - 6 .

3 3 . Go re, C.J .; Wit h ers, R.T. Effect o f exercise in t en sit y a n d d u ra t io n o n p o st e xe rcise m e t a b o lism . J Ap p l Ph ysio l 1 9 9 0 ;6 8 : 2 3 6 2 - 8 .

Imagem

Fig ure  1  – Comparison  of SpO2 valu es du rin g n oct u rn al vigilan ce an d du rin g sleep

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