PARTI. METABOLISM

IN

PROLONGED EXERCISE

FIBER TYPES AND METABOLIC POTENTIALS OF SKELETAL MUSCLES IN SEDENTARY MAN AND ENDURANCE RUNNERS * Bengt Saltin, Jan Henriksson, Else Nygaard, and Per Andersen August Krogh Institute Copenhagen University DK-2100 Copenhagen 9 Denmark

Eva Jansson Department of Clinical Physiology Karolinska Hospital Stockholm, Sweden

During the last decade the needle biopsy technique has been widely applied for obtaining samples from the skeletal muscle of healthy people. In the early exercise studies the metabolic response of whole muscle was the focus of attention.'. More recently, histochemical techniques have been applied to identify different fiber types in human skeletal muscle and to relate their contractile characteristics to their function and metabolism in exercise. The metabolic potential of muscle tissue has also been evaluated by determining different substrate and enzyme activities. In this paper these latter reports will be reviewed. Special attention will be given to the adaptations that take place as a result of physical inactivity and activity. Classification of Skeletal Muscle Fibers in Man

The smallest unit that can be activated in a muscle contraction is the motor unit. The muscle fibers within that unit appear to have identical characterisa few exceptions have been d e ~ c r i b e d .The ~ most frequently t i c ~ , ~although . used method to distinguish among different muscle fiber types is based on single or multiple stains of freeze-sectioned muscle samples. The number of stains available for classifying muscle fibers is overwhelming. This explains the existence of the great number of different systems employed to classify and name 1 a summary is presented of some of the commuscle fiber types. In TABLE monly used stains and the nomenclature applied. The classical terminology of red and white muscle fibers was based on the color of the fibers, which in turn was related to the myoglobin content.' The activities of the mitochondria1 enzymes are related to the myoglobin content, while the content of sarcoplasmatic, glycolytic enzymes usually are inversely related to the oxidative enzymes and myoglobin content.s, Stains for glycolytic or oxidative enzymes as well as for myoglobin give rise to a variety of staining intensities. Fibers can be divided into different classes. but the boundaries between these classes are The papers cited in this article that were written by the authors (August Krogh Institute) have been sponsored by grants from the Danish Natural Science Research Council and the Research Council of the Danish Sports Federation.

3

FOG

so

9

~~

FG

(A) Fast twitch ( F T b ) (type IIB)

High Glycolytic (HG 1 Lowcontent

(LO)

White Low Oxidative

stains applied is Reference 6. iThis stain for classification gives a fourth fiber type (IIC) staining dark at preincubations of pH 10.3 and 4.3. This fiber is rarely seen in normal adult human muscles.

* A general reference for the

Fast twitch (FT") (type IIA)

Slow twitch (ST) (type I)

(B)

10, 14, 15

(C)

5. Myofibrillar ATPase -i: (preincubations pH 10.3, 4.64.8) Combination of 2, 3, and 5

Glycolytic (GI Intermediate content

17, 19,22

11,21

3. Glycolytical enzymes

(0)

Intermediate Oxidative

Nomenclature

NOMENCLATURE TO DESIGNATE FIBERTYPES *

Red High Oxidative (HO) Low glycolytic (LG) High content

AND

4. Lipids

7,9 11,21

TABLE1 MORE FREQUENTLY USED STAINS

1. Myoglobin 2. Mitochondria1 enzymes

OF THE

Reference

OF %ME

Base for Classification

A SUMMARY

t)

8

gg

0,

3e

o,

&

5

*

Z CD

E

2

P

Saltin et a[.: Fiber Types

5

unclear. This is true for skeletal muscle of most species, including man. In 1962 Engel suggested the use of a stain for myofibrillar ATPase after alkaline preincubation.lo This method separates muscle fibers into two well-defined groups. He proposed the names type I and I1 fibers for those fibers staining light and dark, respectively. The type I fibers were supposed to have slow contraction times, and the type I1 fibers, fast. By adding a stain for a mitochondrial enzyme, a subdivision of the type I1 fibers is sometimes possible: One type of fiber can be found with a high oxidative potential, and another, low.11 Thus, in many species two rather distinctly different subgroups of type I1 muscle fibers are present. Using these same two stains on the skeletal muscle of man, Edgerton rt and Prince er d.l:'also found different types of fibers, which they accepted as being clearly separated into three groups. We do not 1 ) as we do not see clear-cut boundaries find this procedure satisfactory (FIGURE between the two groups of type 11 fibers. In man, a subdivision of the type 11 fibers can be made by the use of the different sensitivities for acid pH that the type 11 fibers have. Some of them lose activity (and thereby their dark color) at a pH of 4.6-4.8, whereas other type I1 fibers maintain color until a pH of 4.5 (FIGURE I ) . Brooke and Kaiser l5 named the latter subgroup IIB, and the former, type At this point it is worth emphasizing that it appears as if the subdivision of type 11 fibers as done by Edgerton rt 01.12 and Prince et ~ 1 . on l ~ the one hand, and by Brooke and Kaiser on the other,11.15 do not give rise to identical subgroups of the type I 1 fibers. With a mitochondria1 stain, a larger number of type IIB (fast twitch glycolytic) fibers are identified as compared to the use of the stain for myofibrillar ATPase after an alkaline (pH 10.3) and an acid preincubation (pH 4.6-4.8). Before a more firm conclusion can be reached on this particular point a comparative study is necessary of the two different methods to classify the skeletal niuscle fibers of man. Muscle Fiber Normwcltitirrc~

In the preceding discussion, different names have been used to designate the different fiber types (TABLE I ) . We have neutral names like type 1 and IIA and I1B fibers or A, B, and C fibers, as others prefer to call However, the disadvantage with neutral names is that the names do not indicate any of the characteristics of the different fiber types. Peter et (11. favor a nomenclature that includes both contractile and metabolic characteristics of the different fibers.!' This nomenclature is based upon the close correlation between enzyme activity levels and the contractile characteristics, as well as the specific metabolism of the fibers. Good experimental evidence is available revealing a close coupling between In man, the charactcristics of a fiber and its function in many species.'. ', such a complete validation is still lacking. However, contractile characteristics of the fibers l', I " . 2" together with quantitative data of the metabolic profile " I give a good base for the assumption that a coupling between the characteristics of a fiber and its function also exists in man.22 With this background we find that it is valid to use descriptive terms when naming the fibers. However, we will not go further than to designate the two main types as slow (ST) and fast twitch (FT) fibers, and add an "a" (FT,,) and a "b" (FT,,) for the subgroups of the fast twitch fibers. The reason for this is as follows: It is true that in

6

Annals New York Academy of Sciences

FIGURE 1. Cross-sections of human skeletal muscle (vastus lateralis) are stained for myofibrillar ATPase after preincubations in ( 1 ) pH 4.3, (2) 4.6, (3) NADHdiaphorase, and (4) a-glycerophosphate dehydrogenase. Of note is the fact that classification of the different fiber types is solely based on the stains for myofibrillar ATPase.

7

Saltin el al.: Fiber Types

sedentary subjects a difference can be observed in metabolic potentials, both with histochemical and quantitative biochemical techniques, when one compares 1, 2, FIGURE 2 ) . However, the absolute level the different fiber types (TABLES for the activities of oxidative and glycolytic enzymes is, in all fiber types in human skeletal muscle, large enough to accommodate a rather substantial aerobic and anaerobic metabolism. Moreover, with endurance training, for example, the enhancement of the oxidative potential of FT,,and FT,, fibers is very impressive, resulting in a potential for oxidation in these fibers markedly surpassing the aerobic capacity of ST fibers of untrained subjects.21.2a Thus we feel that it is wrong to include abbreviations for the metabolic potentials in the names as these, in some cases, can be very misleading. The subscripts “a” and “b” indicate that there are certain differences in the population of FT fibers most likely related to differences in the myosin molecules.lZ When this

ON

_ ~

TABLE 2 A SUMMARY or: MEAN VALUES FOR DIFFERENT VARIABLES MEASURED HUMANSKELETAL MUSCLETO CHARACTERIZE THE DIFFERENT FIBERTYPES*

_

_

_

~

~~

Muscle Fiber Types Characteristics

ST

FT.

FTI,

References

Contructile churocteristics

Ca” act. myosin ATPase (mmoles/min ‘mg myosin) Mg’+ act. actomyosin ATPase (mmoles/min.g protein) “Time to peak tension” (msec)

0.16

0.48

21

0.30 80

0.84 30

27 18,19

13.1

16.6

27

Enzymes

Creatine phosphokinase (mmoles/min.g protein) Phosphof ructokinase (rnmoleslkg .min, wet weight Succinate deh ydrogenase (mmoles/kg.min, wet weight)

9.4

14.0

20.0

21

11.5

9.0

6.5

21

____._

* Values for substrate concentrations can be found in Reference 22. point has been more completely clarified and possibly found to be correlated to different contractile characteristics, it will be time to exchange the neutral subscripts to more descriptive terms. In connection with these problems it may be worthwhile to consider the question as to whether the previously described fiber types in human skeletal muscles are similar to those found in the muscle fiber types of other species. To a certain extent it may be true for the ST fiber of man, which should be equivalent with the SO fiber of other species, as well as for the human FTb being similar to the FG fibers (TABLE1 ) . The FT, fiber and the FOG fiber may be the fiber that is most different both in character and function, when comparing man with other species such as the cat, rat, guinea pig.* Besides the difference in staining intensity for oxidative enzymes, it appears that in such species as rats and guinea pigs the FOG fibers are more easily

8

Annals New York Academy of Sciences

recruited in muscle contractions than the FOG fibers in human muscles.8 Moreover, Thorstensson and Karlsson have provided some indirect evidence that the fatigability of human FT fibers is different from that of the fasttwitching fibers in cat gastrocnemius muscle.25 A study comparing the staining profiles and physiological properties of fiber types in the same muscles of different species, ranging from lower vertebrates to primates and man, with the known physical activity levels would constitute an extremely valuable contribution at this time. Until such a study becomes available, caution is recommended regarding the application of conclusions to more than the species studied.

ST

MUSCLE FIBRE TYPE 9

CONTRACTILE PROPERTIES

MYOSIN ATP-ASE I"ETAB0LIC POTENTIALS GLYCOLYSIS OXIDATION

SUBSlRATES GLYCOGEN

lR IGLYCERIDE CAPIUARY SUPPLY FIBRE AREA

FIGURE 2. A schematic summary of some characteristics observed for the three major types of fiber found in skeletal muscle of sedentary subjects. The results are 2 have also been primarily based on histochemical findings, but the results in TABLE

used. Quantitative Measures of Contractile and Metabolic Characteristics of Diflerent Muscle Fiber Types

Histochemical techniques can at best give a semiquantitative estimation of the metabolic profile of a certain fiber type and its twitch characteristics. Reliable quantitative data exist on muscle from cats, guinea pigs, and rats,x and are now becoming available for muscle from man (TABLE 2). The muscles of man are mixed in regard to fiber composition and the fiber types exist in a mosaic pattern. To determine quantitatively the metabolic profile one has to use a method where fibers argdissected out, typed, and

Saltin et al.: Fiber Types

9

analyzed for content of a substrate or an enzyme.21 By adding the information - contraction times on twitch characteristics obtained in vivo 19 or in vitro l Rzn for FT and ST fibers are also available. In many aspects these quantitative data confirm what has been postulated from the histochemical work on muscle from man. Nevertheless, it is important to point out that the activity of succinate dehydrogenase is considerably higher in ST fibers than in FT, and FT,, fibers in muscles of sedentary men (TABLE 2). The reverse pattern is true for phosphofructokinase. It is also of note that the glycolytic potential is considerable in the ST fiber and that the oxidative potential is substantial in the FT, fiber. There has been some argument about a lower glycogen content in the ST fibers compared to the FT fibers,h*2'; but direct measurements of the glycogen content of the different fiber types clearly demonstrate that at rest after a mixed diet no significant differences between fiber types can be detected in man. In contrast, the other major intramuscular substrate, the triglyceride pool, is much larger in the ST fibers than in the FT fibers. Whether this is different in the subgroups of FT fibers is not known, although staining with Sudan black or oil red for lipids does indicate that this is the case.", 22 . The Ca++-activated myosin ATPase is approximately 2.5 times higher in FT than ST fibers, which matches well with the data on contraction 2n Whether FT, fibers have a higher myosin ATPase activity or a faster time to peak tension than FT,, fibers cannot be settled either by our work 2 1 or other 2i In rat soleus muscle Kugelberg found a close relationship between histochemical staining intensity for myofibrillar ATPase and contraction times.5 Based on these results Prince et al.l:j have suggested that the FG (FT,) fibers have slower contraction times than the FOG (FT,,) fibers in man. This may be true, but with the existing large variation between species, we need more direct evidence before any firm conclusions can be drawn on this particular point. Moreover, Burke's data on cat muscle point to the possibility of quite different contraction times, although histochemical staining properties are the same or very similar.", z 5 Muscle Fiber Composition in Human Skeletal Muscle

The most commonly studied muscle in man is the lateral portion of the 16thigh (vastus lateralis). In a recent study of 70 men and 45 women-all years-old-representing an unselected group of individuals at this age, a mean value of 52% of total fibers as being ST fibers was found for both sexeszR (FIGURE 3 ) . Within the FT fibers, the FT, fibers were approximately twice as common as the FT,, fibers, the mean values being 33% and 14% of total fibers, respectively. Similar mean values for the percentage of ST, FT,, and FT,,fibers were observed in a study of 54 adult women.2!' Thus, ample evidence is available suggesting that no difference exists between males and females in this respect. For both sexes a wide variation in fiber composition between individuals is present, which is most pronounced for the males. Whether this is due to a sex difference cannot be fully answered today. However, all available reports on muscle fiber composition in man indicate that greater extremes in 2R-33 fiber composition are found in Another difference between the sexes is found in the size of the fibers. I n general, cross-sectional areas of fibers are larger in male than in female muscle (TABLE3). In men the mean cross-sectional area of the FT fibers of the thigh (FT,, being larger than FT, fibers) is larger than the mean area of ST fiber,

Annals New York Academy of Sciences

10

20 0

L

e

.-d

0

lo 5

10

> 20

30

LO

50

60

Sl, vastus

70

80

90

100

*/a

lateralis

FIGURE 3. The distribution of relative occurrence of ST fibers in vastus lateralis in men and women.=

IN THE

TABLE 3 CROSS-SECTIONAL AREAS(pm') OF SKELETALMUSCLEFIBERS VASTUS LATERALISMUSCLEFROM NOT SPECIALLY TRAINED SUBJECTS*

Fiber Type

ST FT. FTb n References

Female

Male 16yrs

20-3Oyrs

4880 (1200) 5500 (1390) 4900 (1590) 70 28

53 10 (1210) 61 10 (1200) 5600 (1450) 10 36,53,81

16 yrs

2&30 yrs

4310 ( 1270)

4310 ( 1300)

3920 (910) 45 28

* Mean values ( 2 standard deviations). The increase in muscle fiber size after the age of 16 in males is most likely related to the fact that they are still growing. Females do not grow much after the age of 16. The reduction in muscle fiber may be related to less physical activity later in life.

Saltin et af.: Fiber Types

11

whereas in sedentary women the ST fiber is larger than the FT,,. In both sexes the FT,, fiber is the smallest fiber. One possible explanation for the difference between fiber areas in the two sexes may be related to differences in the physical activity pattern. All fiber types can respond to increased activity with some enlargement of the size of the fiber.:

Fiber types and metabolic potentials of skeletal muscles in sedentary man and endurance runners.

PARTI. METABOLISM IN PROLONGED EXERCISE FIBER TYPES AND METABOLIC POTENTIALS OF SKELETAL MUSCLES IN SEDENTARY MAN AND ENDURANCE RUNNERS * Bengt Sal...
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