Influence of Aerobic Exercise on Fuel Utilization by ... - ACS Publications

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3 Influence of Aerobic Exercise on Fuel Utilization by Skeletal Muscle Michael N. Goodman Department of Medicine and Physiology, Boston University School of Medicine, Boston, M A 02118

During the past decade, we have witnessed a renaissance of interest in muscular exercise and the potential benefits it may have on the health of the individual. Evidence is available that exercise can prevent or at least delay cardiovascular disease, lower risk factors for atherosclerosis, help in weight reduction and may help prevent complications of certain diseases such as diabetes (1,2). The impact physical exertion has had on our society is quite evident by the numbers or aerobic-related advertisements in non-scientific publications as well as the numbers of individuals running, walking or cycling. Years ago these activities were usually confined to the athlete, and at that time athletes may have been more concerned with what was the best foodstuff for maximum performance or endurance rather than on how physical exertion may prevent complications or delay debilitating diseases. Nevertheless, the impact of nutrition on physical performance capacity has been a subject of considerable interest for numerous years. Even today, individuals who exercise for health benefits may manipulate their diet so as to gain better performance capacity. The present r e v i e w w i l l focus on a p a r t i c u l a r a s p e c t o f t h i s s u b j e c t , s p e c i f i c a l l y how the use of v a r i o u s m e t a b o l i c fuels are regulated during muscular e x e r c i s e . F o r t h e m o s t p a r t s t u d i e s i n man w i l l be c i t e d , b u t some s e c t i o n s w i l l i n c l u d e r e f e r e n c e t o a n i m a l s t u d i e s f o r a p a r t i c u l a r emphasis. The q u e s t i o n o f what f u e l s are used by the w o r k i n g muscles d u r i n g p h y s i c a l performance and the r e l a t i v e i m p o r t a n c e o f each i s n o t new and has b e e n d e b a t e d f o r a l o n g t i m e . E a r l y s t u d i e s as f a r b a c k as 1896 s u g g e s t e d t h a t c a r b o h y d r a t e s w e r e t h e o n l y f u e l t h a t c o u l d be o x i d i z e d by the w o r k i n g muscles Ci,4). I t was only l a t e r that s t u d i e s e s t a b l i s h e d that both carbohydrates ( i . e . , p l a s m a g l u c o s e and m u s c l e g l y c o g e n ) and l i p i d s ( i . e . , p l a s m a f r e e f a t t y a c i d s and m u s c l e t r i g l y c e r i d e s ) c o u l d be u t i l i z e d by t h e w o r k i n g m u s c l e s . The use o i p r o t e i n a s a f u e l a l s o r e c e i v e d a t t e n t i o n i n e a r l y s t u d i e s , but more r e c e n t s t u d i e s s u g g e s t t h a t i t s u s a g e by m u s c l e i s s m a l l i n r e l a t i o n t o c a r b o h y d r a t e s and l i p i d s (4). 0097-6156/86/0294-0027$06.00/0 © 1986 American Chemical Society

Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.


28

NUTRT IO IN AND AEROBC I EXERCS IE Some i n s i g h t s i n t o now c a r b o h y d r a t e and l i p i d u t i l i z a t i o n may be r e g u l a t e d d u r i n g e x e r c i s e may be g a i n e d by c o m p a r i n g e x e r c i s e t o t h e m e t a b o l i s m o f s t a r v a t i o n . As c a n be s e e n i n F i g u r e 1, e x e r c i s e and s t a r v a t i o n have s e v e r a l f e a t u r e s i n common. D u r i n g s t a r v a t i o n , b l o o d g l u c o s e f a l l s e a r l y i n the f a s t and then r e m a i n s r e m a r k a b l y s t a b l e . C o n c o m i t t a n t l y , c i r c u l a t i n g l i p i d f u e l s (i.e., f r e e f a t t y a c i a s and ketone b o d i e s ) r i s e . The f a l l i n i n s u l i n d u r i n g the f a s t p r o b a b l y o r c h e s t r a t e s the i n c r e a s e i n l i p o i y s i s by s t i m u l a t i n g t h e b r e a k d o w n o f t r i g l y c e r i d e s stored i n adipose t i s s u e . Although v a r i a b l e g l u c a g o n may r i s e e a r l y i n t h e f a s t and t h e n f a i l as the f a s t i s lengthened. A somewhat s i m i l a r m e t a b o l i c p r o f i l e o c c u r s d u r i n g e x e r c i s e , e s p e c i a l l y i f i t i s of the t y p e t h a t i s o f l i g h t t o moderate i n t e n s i t y w i t h a d u r a t i o n o f one hour o r l o n g e r . T e l e o l o g i c a l l y , the g o a l of these m e t a b o l i c changes i s to m a i n t a i n a c o n s t a n t f u e l s u p p l y t o the b r a i n w h i l e p r o v i d i n g the p e r i p h e r a l t i s s u e s such as muscle w i t h an a l t e r n a t e f u e l i n the form of l i p i d ( e i t h e r f r e e f a t t y a c i d s or ketone bodies) to r e p l a c e g l u c o s e (5,6). As shown i n F i g u r e 2, as fasting p r o g r e s s e s , l i p i d becomes the most i m p o r t a n t source of f u e l f o r m u s c l e , w h i l e the use o f c a r b o h y d r a t e d i m i n i s h e s . This i s r e f l e c t e d i n a f a l l of the r e s p i r a t o r y q u o t i e n t a c r o s s muscle. D u r i n g e x e r c i s e , c a r b o h y d r a t e i s o f p r i m e i m p o r t a n c e as a f u e l d u r i n g the e a r l y minutes. As e x e r c i s e p r o g r e s s e s , l i p i d becomes a more i m p o r t a n t f u e l . H o w e v e r , c a r b o h y d r a t e o x i d a t i o n i s n o t n e g l i g i b l e and seems i m p o r t a n t i n p r e v e n t i n g e x h a u s t i o n . In e l i t e u l t r a d i s t a n c e runners who can r e m a i n a c t i v e f o r 24 h o u r s , l i p i d becomes t h e s o l e f u e l as g l y c o g e n s t o r e s i n t h e m u s c l e become exhausted (7). The r e s p i r a t o r y q u o t i e n t at t h i s t i m e i s a b o u t 0.7. These e l i t e r u n n e r s a l s o e x p e r i e n c e a marked r e d u c t i o n i n power output i n d i c a t i n g t h a t somehow muscle glycogen may be i m p o r t a n t i n m a i n t a i n i n g maximum e f f i c i e n c y d u r i n g exercise. Thus, i t i s e v i d e n t t h a t the m o b i l i z a t i o n and p r o v i s i o n o f l i p i d to muscle d u r i n g e x e r c i s e , l i k e during starvation, r e s t r i c t s the usage of c a r b o h y d r a t e . I f t h i s d i d not o c c u r d u r i n g e x e r c i s e , g l y c o g e n s t o r e s w i t h i n muscle (as w e l l as i n the l i v e r ) w o u l d be d e p l e t e d more r a p i d l y t h a n n o r m a l and may s i g n i f i c a n t l y l i m i t the d u r a t i o n o f e x e r c i s e . Hypoglycemia c o u l d a l s o r e s u l t and l i m i t performance. F u e l r e s e r v e s of the body The i m p o r t a n c e o f r e g u l a t i n g c a r b o h y d r a t e s t o r e s w i t h i n muscle (and l i v e r ) d u r i n g a e r o b i c work can be r e a d i l y a p p r e c i a t e d when one c o n s i d e r s t h a t t h e d i s t a n c e o f a m a r a t h o n (20.2 m i l e s ) i s c o m p l e t e d by top r u n n e r s i n about 130 minutes w i t h a t o t a l energy expenditure of a b o u t 2,600 k i i o c a l o r i e s , roughly 20 k i l o c a l o r i e s / m i n u t e (8,9). One of the problems i n c o m p l e t i n g the d i s t a n c e i n s u c h t i m e i s the p r o v i s i o n o f s u f f i c i e n t f u e l t o s a t i s f y the r a t e o f energy e x p e n d i t u r e . As shown i n Table I , the l a r g e s t f u e l r e s e r v e i n t h e body i s t r i g l y c e r i d e l o c a t e d p r i m a r i l y i n a d i p o s e t i s s u e w i t h a s m a l l e r amount i n s k e l e t a l muscle. Compared t o the t r i g l y c e r i d e s t o r e s , a much s m a l l e r amount o f f u e l i s a v a i l a b l e as g l y c o g e n s t o r e d w i t h i n l i v e r and


3.

Fuel

GOODMAN

Utilization

Glucose (mM)

29

5.0 2.5 J


Lipid fuels (mM)

I

I

L

6

3 Insulin

8

(μυ/ml)

Glucagon i(pg/ml) 100 n r % / " n 5

0

0

24

Days of starvation

0

2

4

Hours of exercise

F i g u r e 1 - E f f e c t o f s t a r v a t i o n and e x e r c i s e o f m o d e r a t e i n t e n s i t y on t h e c o n c e n t r a t i o n s o f b l o o d g l u c o s e , l i p i d s ( f r e e f a t t y a c i d s and ketone b o d i e s ) , i n s u l i n and glucagon. Data from C a h i l l (5) and F e l i g and Wahren (11).

100

Ζ» ο Ο φ

»

carbohydrate

Si ο *

a oc

0

3

24

Days of starvation

0

2

4

24

Hours of exercise

F i g u r e 2 - U t i l i z a t i o n o f c a r b o h y d r a t e and l i p i d by s k e l e t a l muscle d u r i n g s t a r v a t i o n and e x e r c i s e . R e s p i r a t o r y q u o t i e n t (RQ) i s the r a t i o of p r o d u c e a / 0 2 consumed. D a t a f r o m Owen and R e i c h a r d ( 6 ) , F e l i g and Wahren (11) and Wahren (12).



30

NUTRITION AND AEROBIC EXERCISE

muscle. A l t h o u g n p r o t e i n nas been o m i t t e d , the c a l o r i c v a l u e of p r o t e i n i n t h e body may a c c o u n t f o r 15% o f t h e body f u e l r e s e r v e s ; however, i t s u s e f u l l n e s s as a f u e l i s l i m i t e d because i t s c o n s u m p t i o n would n e c e s s i t a t e the d i s s o l u t i o n of s k e l e t a l muscle. I t can be seen i n l a b l e I, t h a t i f a normal 70kg man were to undergo t o t a l s t a r v a t i o n and r e m a i n i n the b a s a l s t a t e he c o u l d , i n t h e o r y , s u r v i v e f o r about 60 days w i t n h i s f u e l r e q u i r e m e n t s b e i n g met by t r i g l y c e r i d e breakdown. On the o t h e r hand, a t t h i s b a s a l r a t e of m e t a b o l i s m , c a r b o h y d r a t e s t o r e s would be d i m i n i s h e d w i t h i n a day. I f t h i s i n d i v i d u a l w e r e t o r u n a m a r a t h o n (20 k c a l / m i n ) , t r i g l y c e r i d e s t o r e s c o u l d p r o v i d e energy f o r about 5 d a y s , w h e r e a s , c a r b o h y d r a t e s t o r e s f o r o n l y 90 m i n u t e s . The l a t t e r i s p r o b a b l y an o v e r e s t i m a t i o n , i f one c o n s i d e r s t h a t not a l l m u s c l e s w o u l d be u s e d d u r i n g t h e r u n and t h a t the c o n v e r s i o n o f c a r b o h y d r a t e o x i d a t i o n to ATP g e n e r a t i o n i s not a t 100% e f f i c i e n c y . W i t h t h i s c o n s i d e r a t i o n c a r b o h y d r a t e s t o r e s may p r o v i d e e n e r g y f o r p e r h a p s 60 m i n u t e s , f a r s h o r t o f t h e t i m e needed f o r c o m p l e t i o n o f a marathon. Factors Regulating Fuel U t i l i z a t i o n during Aerobic

Performance

From t h e a b o v e d i s c u s s i o n , i t i s e v i d e n t t h a t t h e p r o v i s i o n of f u e l f o r the m u s c l e i s a major l i m i t i n g f a c t o r d u r i n g e x e r c i s e and s e l e c t i o n o f f u e l s f o r o x i d a t i o n by t h e m u s c l e i s o f c o n s i d e r a b l e i m p o r t a n c e i n d e l a y i n g tne o n s e t of f a t i g u e , e s p e c i a l l y i n t h e t y p e o f e x e r t i o n t h a t may go b e y o n d 10 o r 20 minutes. A number of f a c t o r s can r e g u l a t e f u e l u t i l i z a t i o n d u r i n g e x e r c i s e i n c l u d i n g 1) muscle f i b e r type, 2) d u r a t i o n and i n t e n s i t y of e x e r c i s e , 3; p h y s i c a l t r a i n i n g and 4) d i e t . Musc l e F i b e r T y p e s . S k e l e t a l m u s c l e i s u s u a l l y c l a s s i f i e d a c c o r d i n g t o i t s f i b e r type. T h i s c l a s s i f i c a t i o n i s based upon s t a i n i n g p r o p e r t i e s of some muscle enzymes as w e l l as measurement of b i o c h e m i c a l markers (10). I n man, muscle f i b e r s are c l a s s i f i e d as b e i n g o f e i t h e r t y p e I o r t y p e I I (A o r B) ( T a b l e II). Type I f i b e r s are s l o w - t w i t c n h i g h l y o x i d a t i v e f i b e r s w i t h a h i g h c a p i l l a r y d e n s i t y . These c h a r a c t e r i s t i c s u s u a l l y c o n f e r a h i g h c a p a b i l i t y f o r l i p i d o x i d a t i o n . Type I I f i o e r s on the o t h e r hand a r e f a s t - t w i t c h f i b e r s . Type I1A f i b e r s a r e somewhat s i m i l a r t o t h o s e o f t y p e I i n t h a t t h e y a l s o nave a m o d e r a t e l y h i g h o x i d a t i v e c a p a c i t y ; i n a d d i t i o n , they have a m o d e r a t e l y h i g h g l y c o l y t i c c a p a c i t y . Type 11B f i b e r s a l s o have a n i g h g l y c o l y t i c but low o x i d a t i v e c a p a c i t y . One can u s u a l l y p r e d i c t from these v a r i o u s c h a r a c t e r i s t i c s w h e t h e r o r n o t a p a r t i c u l a r m u s c l e w o u l d be more i n v o l v e d i n e n d u r a n c e v e r s u s s p r i n t a c t i v i t y as w e l l as t h e f u e l o r f u e l m i x t u r e used. F o r e x a m p l e , as d i s c u s s e d i n t h e preceding c h a p t e r by T e r j u n g type I and I I A f i b e r s are more i n v o l v e d w i t h e n d u r a n c e p e r f o r m a n c e r e l y i n g on a f u e l m i x t u r e o f b o t h l i p i d s and c a r b o h y d r a t e . On t h e o t h e r n a n d , t y p e l i b f i b e r s a r e more involved w i t h short s p r i n t - t y p e of a c t i v i t y w i t h a f u e l d e p e n d e n c e a l m o s t e x c l u s i v e l y on c a r b o h y d r a t e . The fiber c o m p o s i t i o n o f m u s c l e f r o m a few a n i m a l s and man i s shown i n T a b l e I I I . A n i m a l s r a i s e d f o r q u i c k " s t o p and go" a c t i v i t y



Data from Newsholme ( 3 7 ) .

Blood g l u c o s e

71

4

0.60

0.03

1,500

8U

350

20

Muscle g l y c o g e n

18

0.15

375

90

L i v e r glycogen

7143

Minutes o f a marathon

86

60

Days o f starvation

E s t i m a t e d p e r i o d f o r which f u e l s t o r ^ would p r o v i d e energy

0.72

1,800

Muscle t r i g l y c e r i d e

200

(kcal)

15ϋ,0ϋϋ

(g)

Approximate t o t a l fuel reserve

16,000

Adipose t i s s u e t r i g l y c e r ide

Tissue of source

Table I. Fuel Reserves and Rates of U t i l i z a t i o n under Different Conditions i n Humans


32

NUTRT IO IN AND AEROBC I EXERCS IE

Table II

Characteristics of Different Fiber Types Muscle f i b e r type


Characteristics

1. 2. 3. 4. 5. 6.

M y o f i b r i l l a r ATPase M i t o c h o n d r i a l eyzymes G l y c o l y t i c enzymes Lipids Glycogen Capillary density

liB

IIA

I slow-•twitch high low high same high

lasc-twitch intermediate intermediate intermediate same intermediate

fast-twitch low high low same low

Data from S a l t i n e t a l . ( 1 0 ) .

Table I I I . Fiber Composition of Muscle from Horses, Dogs and Man Percentage f i b e r c o m p o s i t i o n Type I

Type I I

Horse Quarterhorse

7

93

Dog Greyhound

3

97

53 24 79

47 76 21

Man untrained Sprinters E l i t e runners

Data from Newshoime and Leech ( 7 ) .


3.

GOODMAN

Fuel

utilization


( q u a r t e r h o r s e ) o r v e r y s h o r e d i s t a n c e speed r u n n i n g (greyhound) have a h i g h p r o p o r t i o n o f t y p e I I m u s c l e f i b e r s . I n man, i n d i v i d u a l s c o n s i d e r e d n o n - a t h l e t e s o r u n t r a i n e d have an equal number o f t y p e I and I I f i b e r s , w h e r e a s , s p r i n t e r s h a v e a preponderance o f type 11 f i b e r s and e l i t e d i s t a n c e runners more type I f i b e r s . I t i s i n t r i g u i n g t h a t some i n d i v i d u a l s h a v e a h i g h p r o p o r t i o n (70-80%) o f e i t h e r type I or I I f i b e r s . It r e m a i n s t o be d e t e r m i n e d whether o r not t h i s i s due t o a g e n e t i c predisposition.

D u r a t i o n and i n t e n s i t y o f E x e r c i s e . A k e y f a c t o r r e g u l a t i n g c a r b o h y d r a t e as w e l l as l i p i d u t i l i z a t i o n d u r i n g aerobic performance i s both the i n t e n s i t y of the e x e r c i s e as w e l l as i t s d u r a t i o n . As shown i n F i g u r e 3, t h e i n c r e a s e i n g l u c o s e u p t a k e by the w o r k i n g l e g muscles i s an e a r l y event, and the uptake i s p r o p o r t i o n a l t o t h e work l o a d (11-13). A f t e r s e v e r a l h o u r s o f e x e r c i s e , l e g g l u c o s e uptake b e g i n s t o f a l l p o s s i b l y as a r e s u l t of a f a l l i n blood g l u c o s e i n d i c a t i n g t h a t l i v e r g l y c o g e n s t o r e s are nearing exhaustion. i t i s noteworthy that the increase i n m u s c l e g l u c o s e u p t a k e o c c u r s as i n s u l i n l e v e l s i n p l a s m a f a l l ( F i g u r e 1) i n d i c a t i n g t h i s response i s not mediated by i n c r e a s e d s e c r e t i o n o f i n s u l i n (12). Whether i n s u l i n i s p e r m i s s i v e f o r t h i s r e s p o n s e r e m a i n s t o be d e t e r m i n e d ( 1 4 ) . £arly i n t h e e x e r c i s e , l e g g l u c o s e uptake i s matched by s p l a n c h n i c ( i . e . l i v e r ) g l u c o s e o u t p u t but as l i v e r g l y c o g e n becomes d e p l e t e d s p l a n c h n i c g l u c o s e o u t p u t f a l l s (11,12). Glycogen breakdown w i t h i n w o r k i n g muscles a l s o o c c u r s d u r i n g the e a r l y s t a g e s o f e x e r c i s e and i t s breakdown i s p r o p o r t i o n a l t o t h e w o r k l o a d (15) ( F i g u r e 4 ) . A t h i g h w o r k l o a d s (80% o f VO2 max), g l y c o g e n d e p l e t i o n o c c u r s r a p i d l y and l i m i t s d u r a t i o n o f the e x e r c i s e . I t s d e p l e t i o n i s more g r a d u a l w i t h l i g h t to moderate e x e r c i s e and may not be a l i m i t i n g f a c t o r u n t i l l a t e i n the e x e r c i s e . L i k e g l y c o g e n , muscle t r i g l y c e r i d e breakdown can a l s o occur d u r i n g e x e r c i s e (15) however, t h i s has not been as w e l l s t u d i e d as muscle g l y c o g e n breakdown t o i n d i c a t e w h e t n e r o r n o t i t s d e g r a d a t i o n i s a l s o i n f l u e n c e d by i n t e n s i t y and d u r a t i o n o f e x e r c i s e . On t h e o t h e r h a n d , i t h a s b e e n shown t h a t u p t a k e o f f r e e f a t t y a c i d s f r o m p l a s m a by w o r k i n g m u s c l e i n c r e a s e s s t e a d i l y d u r i n g e x e r c i s e (11,12). From m e a s u r e m e n t s o f t h e u p t a k e o f g l u c o s e and f r e e f a t t y a c i d s and g l y c o g e n b r e a k d o w n by t h e w o r k i n g m u s c l e s , one c a n estimate t h e c o n t r i b u t i o n made oy e a c h f u e l t o t h e t o t a l o x i d a t i v e m e t a b o l i s m . As shown i n T a b l e I V , d u r i n g t h e f i r s t s e v e r a l hours of l i g h t t o moderate e x e r c i s e the m a j o r i t y o f the f u e l f o r t h e m u s c l e i s d e r i v e d f r o m p l a s m a g l u c o s e and m u s c l e glycogen. Between 3-4 hours, plasma f r e e f a t t y a c i d s become the more i m p o r t a n t f u e l , as p l a s m a g l u c o s e l e v e l s f a l l and m u s c l e g l y c o g e n becomes d e p l e t e d . A l t h o u g h m u s c l e and p l a s m a t r i g l y c e r i d e s are also u t i l i z e d during exercise, their c o n t r i b u t i o n to t o t a l o x i d a t i v e metabolism during prolonged e x e r c i s e i s n o t p r e c i s e l y known s i n c e t h e i r p a t t e r n o f u s a g e t h r o u g h o u t e x e r c i s e has not been w e l l d e t e r m i n e d . One may s p e c u l a t e , however, t h a t l i k e f a t t y a c i d s t h e i r c o n t r i b u t i o n t o the f u e l m e t a b o l i s m of muscle may r i s e as e x e r c i s e i s prolonged.


33


34


F i g u r e 4 - Glycogen d e p l e t i o n from the quadraceps f e m o r i s e x e r c i s e . Data from Essen ( 1 5 ) .


during

Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986. Muscle

36 22 14 8

glycogen

27 41 36 30

Plasma

glucose Plasma

37 37 j>0 62

fatty

Percentage c o n t r i b u t i o n t o oxygen uptake acids

D a t a f r o m F e l i g and Wahren (11) and N e w s h o l m e and L e e c h ( 7 ) . G l u c o s e , f r e e f a t t y a c i d s and oxygen uptake and g l y c o g e n breakdown by the w o r k i n g muscles were d e t e r m i n e d . C a l c u l a t i o n s d e r i v e d f r o m t h e s e d a t a assume t h a t a l l s u b s t r a t e s are c o m p l e t e l y o x i d i z e d by the w o r k i n g muscles. The c a l c u l a t i o n s a l s o assume t h a t the complete m e t a b o l i s m o f one mole o f g l u c o s e (or g l y c o g e n ) r e q u i r e s 6 moles o f oxygen w h i l e one mole of f a t t y a c i d r e q u i r e s 25 moles o f oxygen.

40 90 IdO 240

P e r i o d of exercise (minutes)

Table IV. Contribution of Glucose, Glycogen and Fatty Acids to Oxygen Consumption of Leg Muscles of Man during Mild Prolonged Exercise



36

NUTRT IO IN AND AEROBC I EXERCS IE Physical Training. Programs o f l i g h t to moderate endurance e x e r c i s e (i.e. t r a i n i n g ) have been found t o i n c r e a s e t h e r e s p i r a t o r y c a p a c i t y o f s k e l e t a l m u s c l e (16,17). T h i s response i s a s s o c i a t e d w i t h both an i n c r e a s e i n the number o f m i t o c h o n d r i a as w e l l as a m o u n t s o f o x i d a t i v e e n z y m e s . As shown i n T a b l e V, the a d a p t i v e response t o t r a i n i n g i n v o l v e s i n c r e a s e s i n o x i d a t i v e enzyme a c t i v i t i e s i n a l l muscle f i b e r types. T h i s i n d i c a t e s t h a t the m a j o r f a c t o r t h a t d e t e r m i n e s t h e r e s p i r a t o r y c a p a c i t y o f a m u s c l e f i b e r a p p e a r s t o be i t s c o n t r a c t i l e a c t i v i t y ; t h e more f r e q u e n t l y a muscle f i b e r c o n t r a c t s t h e g r e a t e r i t s m i t o c h o n d r i a l c o n t e n t and o x i d a t i v e c a p a c i t y . I n c o n t r a s t t o changes i n m i t o c h o n d r i a l o x i d a t i v e enzymes, many o f t h e e n z y m e s o f g l y c o l y s i s e i t h e r do n o t c h a n g e o r may e v e n d e c r e a s e f o l l o w i n g t r a i n i n g (17,18). This a d a p t a t i o n i s s p e c i f i c to endurance e x e r c i s e s i n c e s t r e n g t h e x e r c i s e ( i . e . w e i g h t l i f t i n g ) which can r e s u l t i n m u s c l e h y p e r t r o p h y , does n o t i n d u c e an i n c r e a s e i n muscle m i t o c h o n d r i a (8). Due t o the a d a p t i v e i n c r e a s e i n the r e s p i r a t o r y c a p a c i t y o f muscle p h y s i c a l l y t r a i n e d i n d i v i d u a l s d e r i v e a g r e a t e r p r o p o r t i o n o f t h e i r energy from o x i d a t i o n o f f a t and l e s s from c a r b o h y d r a t e d u r i n g submaximal e x e r c i s e (17,19). Ample e v i d e n c e suggests t h a t d e p l e t i o n o f body c a r b o h y d r a t e s t o r e s can p l a y an i m p o r t a n t r o l e i n the development of p h y s i c a l exhaustion during prolonged e x e r c i s e (16,17,£0). One m e c h a n i s m by w h i c h t r a i n i n g may i n c r e a s e endurance appears t o i n v o l v e a g l y c o g e n - s p a r i n g e f f e c t . D i r e c t m e a s u r e m e n t s o f m u s c l e g l y c o g e n i n man and a n i m a l s f o l l o w i n g s u b m a x i m a l e x e r c i s e have shown t h a t i t s c o n t e n t d e c r e a s e s more s l o w l y f o l l o w i n g t r a i n i n g (17,20). I t i s a l s o o f i n t e r e s t that p h y s i c a l t r a i n i n g can lead to l e s s hepatic glycogen d e p l e t i o n f o l l o w i n g s u b m a x i m a l e x e r c i s e ( 2 0 ) . The b e n e f i c i a l e f f e c t o f t h i s a d a p t a t i o n i s t o p r o t e c t the t r a i n e d i n d i v i d u a l o r a n i m a i a g a i n s t h e p a t i c g l y c o g e n d e p l e t i o n and the development o f hypoglycemia during prolonged e x e r c i s e . D i e t . There i s a w i d e l y h e l d n o t i o n t h a t a h i g h muscle g l y c o g e n c o n t e n t p r i o r t o a d i s t a n c e r u n c a n e n h a n c e p e r f o r m a n c e and delay exhaustion. Indeed t h i s has l e d t o the p o p u l a r b e l i e f t h a t " g l y c o g e n l o a d i n g " d i e t s s e v e r a l days p r i o r t o a d i s t a n c e r u n may p r o l o n g e n d u r a n c e and p e r f o r m a n c e ( s e e r e f 7 ) . Too e l e v a t e m u s c l e g l y c o g e n , i t s l e v e l i s f i r s t d e p l e t e d by r u n n i n g a t a moderate t o h i g h i n t e n s i t y f o r a p r o l o n g e d time. F o r t h e next 24 days p r i o r t o a d i s t a n c e r u n , a d i e t h i g h i n c a r b o h y d r a t e ( p a s t a and breads) i s consumed. D u r i n g t h i s t i m e d a i l y t r a i n i n g bouts can continue. This regimen s u c c e s s f u l l y leads t o muscle g l y o c g e n c o n t e n t s h i g h e r t h a n n o r m a l a phenomenon t e r m e d "supercompensation". As can be seen i n T a b l e VI (Group 1), human subjects undergoing a "glycogen loading" regimen p r i o r to a d i s t a n c e r u n o f moderate i n t e n s i t y had a h i g h g l y c o g e n c o n t e n t and c o u l d r u n s i g n i f i c a n t l y l o n g e r t h a n s u b j e c t s c o n s u m i n g a mixed o r a low c a r b o h y d r a t e d i e t . On t h e o t h e r hand, s e v e r a l s t u d i e s have s u g g e s t e d t h a t d i e t s low i n c a r b o h y d r a t e s t h a t r e d u c e m u s c l e g l y c o g e n may n o t be a t a l l d e l e t e r i o u s o r r e d u c e d u r a t i o n o f e x e r c i s e . I n one study by Phinney e t a l . (21), obese i n d i v i d u a l s were p l a c e d on a w e i g h t r e d u c i n g d i e t c o n s i s t i n g o f a h i g h q u a l i t y p r o t e i n ( " p r o t e i n s p a r i n g m o d i f i e d f a s t " ) . As shown


3.

Fuel

GOODMAN

Table V.

utilization

37

Effects of Training on Mitochondrial Enzyme A c t i v i t y of Rat Skeletal Muscle


F i b e r types Enzyme

Group

C i t r a t e synthase

Sedentary Trained

Carnitine palmityltransferase

Sedentary Trained

3-hydroxybutyrate dehydrogenase

Sedentary Trained

Cytochrome o x i d a s e

Sedentary Trained

IIB

IIA

I

10.3 18.5

36 70

23 41

0.11 0.20

0.72 1.20

0.63 1.20

not d e t e c t a b l e 0.14 0.03 ϋ.8υ

0.34 ΰ.88

167 339

830 2041

621 1347

Enzyme activités i n umole/g.rain, except cytochrome o x i d a s e which i s i n u l C^/g x min. Data from B a l d w i n e t a l . ( 1 6 ) .

Table VI. E f f e c t of Diet on Muscle Glycogen Content and Duration of Exercise Subjects

Diet

Muscle g l y c o g e n content before exercise (umol/g)

Duration of exercise (minutes)

Humans

Normal mixed d i e t Low c a r b o h y d r a t e d i e t f o r 3 days High c a r b o h y d r a t e d i e t f o r 3 days (glycogen loading)

97 36 103

116 57 166

Humans

Normal mixed d i e t Low c a r b o h y d r a t e d i e t f o r 6 weeks

85 58

168 249

54 40

30 47

Rats

Normal chow d i e t Low c a r b o h y d r a t e d i e t f o r 5 weeks

Data i n group 1 from Bergstrom e t a l . ( 3 8 ) , Group 2 from Phinney e t a l . ( 2 1 ) , and Group 3 from M i l l e r e t a l . ( 2 2 ) .



38

NUTRT IO IN AND AEROBC I EXERCS IE i n T a b l e VI (Group 2 ) , a f t e r ό weeks on t h i s d i e t muscle g l y c o g e n was r e d u c e d b u t t h e a b i l i t y o f t h e s e i n d i v i d u a l s t o r e m a i n a c t i v e at a low i n t e n s i t y e x e r c i s e i n c r e a s e d by 50%. In another s t u d y (22), r a t s fed a low c a r b o h y d r a t e ( h i g h f a t ) d i e t f o r 5 weeks were a b l e t o t o l e r a t e an i n t e n s e t r e a d m i l l run l o n g e r t h a n r a t s on a n o r m a l d i e t ( T a b l e V I , Group 3 ) . T h u s , d i e t s t h a t may a c t u a l l y l o w e r muscle g l y c o g e n c o n t e n t are not a l w a y s a s s o c i a t e d w i t h reduced performance. I t i s conceivable that i n g r o u p s 2 and 3 t h e p r i m a r y f u e l f o r t h e w o r k i n g m u s c l e s w e r e p r o v i d e d by f r e e f a t t y a c i d s and t r i g l y c e r i d e s r e s u l t i n g i n s p a r i n g o f g l y c o g e n , i f s u c h was t h e c a s e , i t may h e l p e x p l a i n why e x e r c i s e d u r a t i o n was prolonged. I t would a l s o re-emphasize t h a t p r o t e c t i o n of g l y c o g e n s t o r e s are i m p r o t a n t i n d e l a y i n g the onset of e x h a u s t i o n d u r i n g e x e r c i s e . More a c u t e d i e t a r y m a n i p u l a t i o n s h a v e a l s o b e e n shown t o m o d i f y e x e r c i s e performance. When f r e e f a t t y a c i d l e v e l s were a r t i f i c i a l l y r a i s e d i n r a t s by g i v i n g c o r n o i l p l u s h e p a r i n , they w e r e a b l e t o r u n a b o u t 50% l o n g e r t h a n c o n t r o l r a t s b e f o r e b e c o m i n g e x h a u s t e d (9,23,24). T h i s was a s s o c i a t e d w i t h a g l y c o g e n - s p a r i n g e f f e c t d u r i n g the run i n t h a t both b l o o d g l u c o s e and m u s c l e g l y c o g e n d e c l i n e d more s l o w l y . In t h i s a s s o c i a t i o n the g l y c o g e n - s p a r i n g e f f e c t was p o s t u l a t e d t o be due t o an e n h a n c e d o x i d a t i o n o r f a t t y a c i d s . On t h e o t h e r h a n d , g l u c o s e i n g e s t i o n during prolonged l i g h t - i n t e n s i t y e x e r c i s e r e s u l t e d i n augmented uptake and o x i d a t i o n of g l u c o s e by w o r k i n g muscles i n a s s o c i a t i o n w i t h d i m i n i s h e d l i p o l y s i s (25,26). It i s also t h o u g h t t h a t e x o g e n o u s g l u c o s e may r e d u c e e n d o g e n o u s g l y c o g e n breakdown ( 2 6 ) . B i o c h e m i c a l R e g u l a t i o n of F u e l U t i l i z a t i o n d u r i n g E x e r c i s e The p r e v i o u s s e c t i o n s have i n d i c a t e d t h a t both c a r b o h y d r a t e s and l i p i d s can be u t i l i z e d by muscle d u r i n g a e r o b i c performance. Due to the s m a l l r e s e r v e of c a r b o h y d r a t e i n the body ( T a b l e I ) , i t s use as a f u e l i s l i m i t e d . To o b t a i n maximal performance d u r i n g e n d u r a n c e r u n n i n g ( i . e . , m a r a t h o n ) , b o t h c a r b o h y d r a t e and l i p i d f u e l s must be u s e d s i m u l t a n e o u s l y ( 7 ) . As much f a t t y a c i d as p o s s i b l e m u s t be o x i d i z e d t o a l l o w t h e l i m i t e d c a r b o h y d r a t e r e s e r v e s t o l a s t f o r the d u r a t i o n of e x e r c i s e . Hypoglycemia m u s t be p r e v e n t e d and g l u c o s e must be s u p p l i e d t o t h e b r a i n a t a l l t i m e s . T h i s c a r b o h y d r a t e s p a r i n g a t the expense of f a t t y a c i d o x i d a t i o n has been proposed t o be f a c i l i t a t e d by a s p e c i f i c i n t r a c e l l u l a r c o n t r o l mechanism. I t i s w e l l documented t h a t g l u c o s e u p t a k e , g l y c o l y s i s , g l y c o g e n b r e a k d o w n and p y r u v a t e o x i d a t i o n are i n h i b i t e d i n the h e a r t by o x i d a t i o n o£ l a t t y a c i d s (27). R a n d l e and c o w o r k e r s (27) p r o p o s e d t h a t t h i s i n h i b i t i o n of c a r b o h y d r a t e u t i l i z a t i o n by f a t t y a c i d s was a g e n e r a l phenomenon. T h i s i n h i b i t i o n i s m e d i a t e d by t h e r i s e i n m u s c l e a c e t y l - C o A , c i t r a t e and g l u c o s e - 6 - p h o s p h a t e d u r i n g f a t t y a c i d o x i d a t i o n ( F i g u r e 5). An i n c r e a s e i n the a c e t y l - C o A r a t i o w i l l i n h i b i t pyruvaue dehydrogenase and reduce c a r b o h y d r a t e o x i d a t i o n ; c i t r a t e produced w i t h i n the m i t o c h o n d r i a w i l l be t r a n s p o r t e d i n t o t h e c y t o p l a s m and w i l l i n h i b i t p h o s p h o f r u e t o k i n a s e t h e r e b y r e s t r i c t i n g g l y c o l y s i s ; and t h e r e s u l t a n t r i s e i n g l u c o s e - 6 p h o s p h a t e c a n i n h i b i t h e x o k i n a s e r e s t r i c t i n g g l u c o s e uptake by



GOODMAN

Fuel

Utilization

F i g u r e 5 - I n t e r a c t i o n of c a r b o h y d r a t e snd l i p i d metabolism d u r i n g e x e r c i s e . G6P, glucose--6-phosphate;F6P, fructose-6phosphate; FDP, f r u c t o s e - 1 , 6 - d i p h o s p h a t e ; P y r , P y r u v a t e ; FFA, f r e e f a t t y a c i d TG, t r i g l y c e r i d e - , HK, h e x o k i n a s e ; PL, p h o s p h o r y l a s e ; PFK, p h o s p h o f r u c t o k i n a s e and PDH, p y r u v a t e dehydrogenase.



40

NUTRT IO IN AND AEROBC I EXERCS IE muscle. There i s a l s o e v i d e n c e t h a t a r i s e i n g l u c o s e - 6 p h o s p h a t e may i n h i b i t g l y c o g e n b r e a k d o w n ( 7 ) . A l t h o u g h t h i s mechanism i s o p e r a t i v e i n c a r d i a c muscle, s t u d i e s u s i n g s k e l e t a l muscle ( i n c u b a t e d in_ v i t r o o r p e r f u s e d j j i s i t u ) have not a l w a y s demonstrated an i n h i b i t o r y e f f e c t o f f a t t y a c i d s ( o r o t h e r l i p i d f u e l s ) on g l u c o s e m e t a b o l i s m (28-30). When demonstrated, i t has been c o n f i n e d t o t h o s e m u s c l e s t h a t have a h i g h c a p a c i t y t o o x i d i z e l i p i d f u e l s such as type I and I I A f i b e r s (29,30). As n o t e d p r e v i o u s l y , l i k e s k e l e t a l m u s c l e , g l y c o g e n d e p l e t i o n i n l i v e r d u r i n g e n d u r a n c e e x e r c i s e i s much l e s s i n t r a i n e d a n i m a l s and i n a n i m a l s who have h a d f r e e f a t t y a c i d s a r t i f i c i a l l y e l e v a t e d . No e v i d e n c e e x i s t s t h a t t h e m e c h a n i s m proposed by Randle t o account f o r the i n h i b i t i o n o f c a r b o h y d r a t e m e t a b o l i s m i n muscle by o x i d a t i o n o f f a t t y a c i d s i s o p e r a t i v e i n the l i v e r . Thus o t h e r f a c t o r s must be r e s p o n s i b l e f o r the s l o w e r r a t e o f l i v e r g l y c o g e n d e p l e t i o n i n t h e s e s i t u a t i o n s . Such f a c t o r s may i n c l u d e a s m a l l e r i n c r e a s e i n c a t e c h o l a m i n e l e v e l s , a smaller reduction i n i n s u l i n levels, and a s m a l l e r r e d u c t i o n i n b l o o d f l o w t o the l i v e r d u r i n g e x e r c i s e (19,20). Carbohydrate M e t a b o l i s m F o l l o w i n g

Exercise

Following e x e r c i s e , g l u c o s e u p t a k e by t h e p r e v i o u s l y w o r k i n g muscles does not f a l l t o p r e - e x e r c i s e l e v e l s but remains e l e v a t e d (31). T e l e o l o g i c a l l y , t h i s would ensure t h a t muscle g l y c o g e n s t o r e s d e p l e t e d d u r i n g e x e r c i s e a r e r a p i d l y r e p l e n i s h e d upon c e s s a t i o n o f e x e r c i s e . Recent s t u d i e s i n the r a t have shown t h a t f o l l o w i n g e x e r c i s e , g l u c o s e t r a n s p o r t and g l y c o g e n s y n t h e s i s i n s k e l e t a l m u s c l e a r e e n h a n c e d due a t l e a s t , i n p a r t , t o an i n c r e a s e i n i n s u l i n s e n s i t i v i t y (32-36). I t was a l s o shown t h a t the i n c r e a s e i n i n s u l i n s e n s i t i v i t y o c c u r s p r e d o m i n a n t l y i n muscle f i b e r s t h a t a r e d e g l y c o g e n a t e d d u r i n g e x e r c i s e , i n o t h e r words, i n the a c t i v e muscles (33). The p r e c i s e mechanism f o r the i n c r e a s e i n i n s u l i n s e n s i t i v i t y f o l l o w i n g e x e r c i s e i s not known nor i s i t a s s o c i a t e d w i t h an i n c r e a s e i n i n s u l i n b i n d i n g t o i t s r e c e p t o r on the muscle c e l l (34-36). Summary During the e a r l y minutes o f e x e r c i s e , carbohydrate (plasma g l u c o s e and m u s c l e g l y c o g e n ) i s t h e p r e d o m i n a n t f u e l f o r t h e w o r k i n g muscles. When the e x e r c i s e i s p r o l o n g e d and i n t e n s i v e , c a r b o h y d r a t e remains a predominant f u e l w i t h l i p i d s (plasma f r e e f a t t y a c i d s and muscle t r i g l y c e r i d e s ) b e i n g o f l e s s e r importance. When t h e e x e r c i s e i s o f m o d e r a t e i n t e n s i t y , l i p i d s e v e n t u a l l y become the p r i m a r y f u e l as c a r b o h y d r a t e s t o r e s a r e reduced. A f t e r t r a i n i n g , which increases the o x i d a t i v e c a p a c i t y of t h e m u s c l e s , l i p i d f u e l s become t h e m a j o r e n e r g y s o u r c e o f t h e w o r k i n g muscles d u r i n g p r o l o n g e d e x e r t i o n s p a r i n g c a r b o h y d r a t e utilization. Both low and h i g h c a r b o n y d r a t e d i e t s can i n c r e a s e e x e r c i s e d u r a t i o n ; however, low c a r b o h y d r a t e d i e t s may d i m i n i s h the power output or max d u r i n g e x e r t i o n . Althouth d i e t s high i n c a r b o h y d r a t e o r f a t ( l o w c a r b o h y d r a t e ) may e n h a n c e e x e r c i s e performance, i t i s recommended t h a t a mixed d i e t be consumed by


3.

GOODMAN

Fuel

Utilization

41

those undertaking exercise f o r h e a l t h b e n e f i t s or weight reduction. During recovery from e x e r c i s e , glucose u p t a k e by t h e p r e v i o u s l y working muscles remains elevated. T h i s i s due, i n p a r t , t o an i n c r e a s e i n the s e n s i t i v i t y o f m u s c l e t o i n s u l i n , f a c i l i t a t i n g glycogen repletion.


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5.

7. 8.

10.

11. 12. 13. 14. 15. lo.

Ruderman, N.B. α Haudenschild, C. (1984) Diabetes as an atherogenic factor. Progress in Cardiovascular Diseases 26:373-412. Richter, E.A., Ruderman, N.B. and Schneider, S.H. (1984) Diabetes and Exercise. Am. J. Med. 70:201-209. Gollnick, P.D. (1977) Free fatty acid turnover and the quantability of substrates as a limiting factor in prolonged exercise. Ann. N.Y. Acad. Sci. 301:64-71. Goodman, M.N. and Ruderman, N.B. (1982) Influence of muscle use on amino acid metabolism. In, Exercise and Sport Science Reviews, ed. by R.L. Terjung, The Franklin Institute, Philadelphia, PA, 1-26. Cahill, G.F. (1970) Starvation in man. New Eng. J. Med. 282:668-675, 6. Owen, O.E. and Reichard, G.A. (1971) Human forearm metabolism during progressive starvation. J. Clin, Invest. 50:1536-1545. Newsholme, E.A., and Leech, A.R. (1983) Metabolism in Exercise. In, Biochemistry for the Medical Sciences John Wiley and sons, New York, Chapter 9. Newsholme, E.A. (1977) The regulation of intracellular and extracellular fuel supply during sustained exercise. Ann. N.Y. Acad. Sci. 301:81-91, 9. Holloszy, J.O., Rennie, M.J., Hickson, R.C., Conlee, R.K. and Hagberg, J.M. (1977) Consequences of the biochemical adaptations to endurance exercise. Ann. N.Y. Acad. Sci. 301:440-450. Saltin, B., Henriksson, J., Nygaard, E. and Andersen, P. (1977) Fiber types and metabolic potentials of skeletal muscles in sedentary man and endurance runners. Ann. N.Y. Acad. Sci. 301:3-29. Felig, P. and Wahren, J. (1975) Fuel homeostasis in exercise. N. Engl. J. Med. 293:1078-1084. Wahren, J.: Glucose turnover during exercise in man (1977) Ann. N.Y. Acad. Sci. 301:45-53. Wahren, J., Felig, P. and Hagenfeldt, L. (1978) Physical exercise and fuel homeostasis in diabetes mellitus. Diabetologia, 14:213-222. Berger, M., riagg, S. and Kuderman, N.B. (1975) Glucose metabolism in perfused skeletal muscle. Biochem. J. 146:231238. Essen, B. (1977) Intramuscular substrate utilization during prolonged exercise. Ann. N.Y. Acad. Sci. 301:30-44. Baldwin, K.M., Klinkerfuss, G.H., Terjung, R.L., Mole, P.A. and Holloszy, J.O. (1972) Respiratory capacity of white, red, and intermediate muscle: adaptive response to exercise. Am. J. Physiol. 222:373-378.



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17. Holloszy, J.O. and Coyle, E.F. (1984) Adaptations of skeletal muscle to endurance exercise and their metabolic consequences. J. Appl. Physiol. 56:831-838. 18. Baldwin, K.M., Winder, W.W., Terjung, R.L., and Holloszy, J.O. (1973) Glycolytic enzymes in different types of skeletal muscle: adaptation to exercise. Am. J. Physiol. 225:962-906. 19. Koivisto, V., R. Hendler, R., Nadel, E. & Felig, P. (1982) Influence of physical training on the fuel-hormone response to prolonged low intensity exercise. Metabolism 31;192—197. 20. Baldwin, K.M. Fitts, R.H., Booth, F.W., Winder, W.W. & holloszy, J.O. (1975) Depletion of muscle and liver glycogen during exercise. Pflugers Arch.354;203-212 1975. 21. Phinney, S.D., Harton, E.S., Sims, E.A., Hanson, J.S., Danforth, E. & La Grange, B.M. (1984) Capacity for moderate exercise in obese subjects after adaptation to a hpyocaloric, ketogenic diet. J. Clin. Investigation 66;1152-1161. 22. Miller, W.C., Bryce, R.K. & Conlee, R.K. (1984) Adaptations to a night-fat diet that increases exercise endurance in male rats. J. Appl. Pnysiol. 58; 78-83. 23. Hickson, R.C., Rennie, M.J., Conlee, R.K., Winder, W.W. & Holloszy, J.O. (1977) Effects of increased plasma fatty acids on glycogen utilization and endurance. J. Appl. Physiol. 43, 829-633. 24. Rennie, M.J., Winder, W.W. & Holloszy, J.O. (1976) A sparing effect of increased plasma fatty acids on muscle and liver glycogen content in exercising rat. Biochem. J. 156: 647-655. 25. Ahlborg, G. & Felig, P. (1976) Influence of glucose ingestion on fuel-hormone response during prolonged exercise. J. App;. Physiol. 41: 683-688. 26. Krezentowski, G., Freddy, P., Luyckx, A.S., Lacroix, M. Mosora, F. & Letebvre, P.J. (1984) Effects of physical training on utilization of a glucose load given orally during exercise. Am, J. Physiol. 246, E412-E417. 27. Randle, P.J., Garland, P.B., Hales, C.N., Newsholme, E.A., Denton, R.M. & Pogson, C.I. (1966) Interactions of metabolism and physiological role of insulin.Rec. Prog. Horm. Res. 22, 1-44. 28. Goodman, M.N., Berger, M. & Ruderman, N.B. (1974) Glucose metabolism in rat skeletal muscle at rest. Diabetes 23; 881-888. 29. Maizels, E.Z., Ruderman, N.B., Goodman, M.N. & Lau, D. (1977) Effects of acetoacetate on glucose metabolism in soleus and extensor digitorum longus muscles of the rat. Biochem, J. 162; 557-568. 30. Rennie, M.J. & Holloszy, J.O. (1977) Inhibition of glucose uptake and glycogenolysis by availability of oleate in well-oxygenated perfused skeletal muscle. Biochem. J. 168; 161-170. 31. Wahren, J., Felig, P., Hendler, R. & Ahlborg, G. (1973) Glucose and amino acid metabolism during recovery after exercise. J. Appl. Physiol. 34; 838-845.


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Ivy, J. & Holloszy, J.O. (1981) Persistent increase in glucose uptake by rat skeletal muscle following exercise. Am. J. Physiol. 241, C200-C203. Richter, E.A., Garetto, L.P., Goodman, M.N. & Ruderman, N.B. (1982) Muscle glucose metabolism following exercise in the rat. J. Clin. Investigation. 69, 765-793. Garetto, L.P., Richter, E.A., Goodman, M.N. & Ruderman, N.B. (1983) Enhanced insullin sensitivity of skeletal muscle following exercise. In: Biochemistry of Exercise, ed. by H. Knuttgen, J. Vogel and J. Poortman. Champaign, IL., p. 681687. Horton, E.G. (1983) Increased insulin sensitivity without altered insulin binding in rat soleus muscle. Excerpta Med. Int. Cong. Ser. 577, 182. Ian, M. & Bonen, Α. (1983) Exercise enhances glycogenesis in muscle without affecting their insulin binding and 2deoxyglucose uptake. Excerpta Med. int. Ser. 5577, 182. Newsholme, E.A. (1983) Control of metabolism and integration of fuel supply for the marathon runner. In: Biochemistry of Exercise, ed. by H. Knuttgen, J. Vogel and J. Poortman. Champaign, IL., p.144-150. Bergstrom, J., Hermansen, L. & Hultman, E. (1967) Diet, muscle glycogen and physical performance. Acta. Physiol. Scand. 71, 140-150.

RECEIVED May 14, 1985


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Influence of Aerobic Exercise on Fuel Utilization by ... - ACS Publications

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