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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.
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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
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
3.
Fuel
GOODMAN
Utilization
Glucose (mM)
29
5.0 2.5 J
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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).
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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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
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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
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32
NUTRT IO IN AND AEROBC I EXERCS IE
Table II
Characteristics of Different Fiber Types Muscle f i b e r type
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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 ) .
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
3.
GOODMAN
Fuel
utilization
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( 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.
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34
NUTRITION AND AEROBIC EXERCISE
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 ) .
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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
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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
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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
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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 ) .
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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
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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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.
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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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
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
3.
GOODMAN
Fuel
Utilization
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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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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.
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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NUTRITION AND AEROBIC EXERCISE
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.
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
3. GOODMAN 32. 33.
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Fuel Utilization
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
Layman; Nutrition and Aerobic Exercise ACS Symposium Series; American Chemical Society: Washington, DC, 1986.
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