Muscle respiratory capacity and fiber type

as determinants of the lactate threshold

J. L. IVY, R. T. WITHERS, P. J. VAN HANDEL, D. H. ELGER, AND D. L. COSTILL

Human Performance Laboratory, Ball State University, Muncie, Indiana 47306

IvY,J.L, R.T. WITHERS, P.J. VAN HANDEL, D. H. ELGER, METHODS

AND II. L. COSTILL. Muscle respiratory capacity and fiber type
as determinants of the lactate threshold. J. Appl. Physiol.:
Respirat. Environ. Exercise Physiol. 48(3): 523-527,1980.-This
study examined the relationship between the respiratory
pacity of an individual’s skeletal muscle and the work rate at
which blood lactate accumulation begins (lactate threshold).
Comparisons were also made among fiber type, ~OZ max,and the
lactate threshold. Muscle biopsies were taken from the vastus
lateralis muscle for determination of respiratory capacity and
fiber type (myosin ATPase). The lactate threshold was assessed
in terms of both the absolute work rate (i.702) and relative work
rate (%Voz max). The capacity of muscle homogenates to oxidize
pyruvate was significantly (P < 0.01) related to the absolute (r
= 0.94) and relative (r = 0.83) lactate thresholds. Significant
positive correlations (P < 0.01) were also found between the
percent of slow-twitch fibers and absolute (r = 0.74) and relative
(r = 0.70) lactate thresholds. The results suggest that the
muscle’s respiratory capacity is of primary importance in deter-
mining the work rate at which blood lactate accumulation
begins. They also suggest that the proportion of slow-twitch
fibers may play an important role in determining the relative
lactate threshold.
skeletal muscle homogenate; absolute and relative lactate
threshold
IT IS WELL KNOWN that the work load at which blood
lactate starts to accumulate (lactate threshold) is higher
for endurance-trained subjects than for untrained sub-
jects. This appears to be true not only at the same
absolute work load and oxygen uptake, but even at the
same relative oxygen uptake (6,17,23,24). Muscle lactate
levels have also been found to be lower at the same
absolute and relative work loads in the same subjects
retested after a program of endurance exercise (23). Re-
cently, Henriksson (10) reported lower respiratory quo-
tient values and a lower release of lactate during sub-
maximal exercise following endurance training. This was
attributed to an increased muscle respiratory capacity
estimated by muscle succinate dehydrogenase activity.
Furthermore, it has been demonstrated that slow-twitch
fibers have a higher respiratory capacity than fast-twitch
fibers (7, 8).
The purpose of this study was, therefore, to examine
the relationship of the respiratory capacity of the skeletal
muscle and the proportion of slow-twitch fibers to the
lactate threshold.
0161-7567/8O/oooO-oooO$O1.25 Copyright 0 B8O the American Physiological
Subjects. Thirteen male volunteers served as subjects
in this study. Their age, height, and weight were (mean
ca- t SD) 23.8 t 5.0 yr, 180.3 t 7.6 cm, and 77.0 t 8.6 kg,
respectively. Informed consent was obtained in accord-
ance with established human subjects protocol,
Biochemical analysis. Two needle biopsies were ob-
tained from the vastus lateralis muscle of the right leg 2
days prior to the lactate threshold test. The first speci-
men was weighed and a 1% (wt/vol) homogenate pre-
pared in 175 mM KCl, 2 mM ethylene diaminetetraacetic
acid (EDTA), pH 7.4 and used immediately for measure-
ment of respiratory capacity (Qo2) with pyruvate as
substrate. Oxygen uptake was measured with a Clark
electrode with excess ADP, inorganic phosphate (Pi), and
substrate. The assay was run in duplicate at 3O”C, pH
7.4. The reaction mixture consisted of the following in a
final volume of 1.0 ml: Na pyruvate 10 mM; Na malate 1
mM; ADP 2 mM; EDTA 1.4 mM; KP04 buffer 20 mM,
pH 7.4; MgClz 5 mM; sucrose 100 mM; KC1 37.5 mM; and
cytochrome c 0.075 mM. The second biopsy specimen
was mounted in OCT and frozen in isopentane cooled to
the temperature of liquid nitrogen. Tissue slices (10 pm
thick) were cut in a cryostat set at -2OOC and incubated
for myosin ATPase and cu-glycerophosphate dehydrogen-
ase activity according to Padykula and Herman (19) and
Wattenberg and Leong (29), respectively. The stained
sections were projected and the percentage of fast-twitch
(FT) and slow-twitch (ST) fibers were determined ac-
cording to the method of Dubowitz and Brooke (5).
Blood samples were obtained immediately before and
after each minute of work (see below) from a Longwell
Teflon catheter (18 gauge, 2.5 in.), which had been in-
serted into an antecubital vein. Blood lactate was deter-
mined by the enzymatic method described by Gutman
and Wahlefeld (9).
Physiological analysis. The lactate threshold test was
performed on a Collins electrically braked cycle ergom-
eter using the procedure of Wasserman et al. (28). The
initial work rate consisted of 2 min of pedaling (60 rpm)
at zero work load. Thereafter the work load was increased
by 25 W each minute until the occurrence of volitional
fatigue. Respiratory parameters (VE, ~OZ, VCOZ, and R)
were monitored each minute by an open-circuit semiau-
tomated sampling system (30). The highest oxygen con-
sumption recorded during the lactate threshold test was
considered the Tj02 max.Blood lactate values were plotted
Society 523

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Copyright © 1980 American Physiological Society. All rights reserved.
524 IVY ET AL.

against the percent of J?o~ max. The lactate threshold was TABLE 1. Descriptive statistics for vo 2IIECLd,
relatiue
held to occur just before the unset of blood lactate and absolute lactate thresholds, muscle respiratory
accumulation (Fig. 1). It was established independently capacity, and percent of slow-twitch fibers
by three researchers and reported in both absolute (voz,
ml kg-’ gmin-I) and relative (!V?O, max) terms. Expired
l
LT
VO 2 max,
pulmonary ventilation (VE) was also plotted against the VO 2 maxt
ml-kg-‘.
%ST ST Fibers, Bo,, pl 02 a
l/min Fibers %area h-leg- ’
p&cent of Vo 2 max as a secondary measure of the lactate min-’
threshold. No significant difference was noted between
the lactate threshold estimated directly or by the VE. 3.54 50.6
Statistical procedures. Bivariate correlation coeffi- H.6 28.1
cients were computed on the data and the 0.05 probabil- 3.0-5.0 38.0-64.7
ity level was used to determine their statistical signifi- Values are means & SD and *range, ~oZ max, maximal oxygen con-
cance. sumption; LT, lactate threshold; Qo~, muscle respiratory capacity; %ST,
percent of slow-twitch fibers; %area, percent relative area of slow-twitch
fibers.
RESULTS

The data for each of the physiological and biochemical TABLE 2. Intercorrelations among physiological
parameters studied in the 13 subjects are presented in and biochemical variables
Table 1. Intercorrelations for these data are given in
1 2 3 4 5
Table 2.
Muscle respiratory capacity. The rate of pyruvate 1. TO2 n&kg-’
maxyWmin-’
oxidation was measured on muscle homogenates to eval- 2. LT, %VO~ max 0.60"
uate muscle respiratory capacity (Qoz). The muscle res- 3. LT, ml 02, kg-l f min-’ 0.9lt 0.87t
4. %ST, fibers 0.62" 0.70t 0.74t
piratory capacity was found to be significantly related to
l 5. ST fibers, %area 0.67-f 0,62* 0.73t 0.97t
vo 2 max ( n = 0.83). When the Qo2 was compared with the 6. hr-’ g-’
Bog, pl l l 0.83t 0.83t U.94t 0.73t 0.70t
absolute lactate threshold, an even higher positive cor- VO 2 max, maximal oxygen consumption; LT, lactate threshold; ST,
relation of r = 0.94 was noted (Fig. 2). Muscle respiratory slow twitch; %area, percent relative area of slow-twitch fibers; &,
capacity was also found to be significantly related to the muscle respiratory capacity. * Significant beyond the 0.05
relative lactate threshold (r = 0.83), the percent of ST level. t Significant beyond the 0.01 level,
fibers (r = 0.73), and the percent relative area of ST
fibers (r = 0.70). ST fibers have a greater respiratory capacity than the
Percent of ST fibers. The two main fiber types found FT fibers. In light of this fact, the percent of ST fibers
in the human vastus lateralis muscle were identified by and their relationship to the work rate at which blood
staining for myosin ATPase. It has been qualitatively lactate starts to accumulate was examined. The percent
demonstrated by histochemical means (8) and quantita- of ST fibers was found to be significantly related to the
tively demonstrated by single-fiber analysis (7) that the lactate threshold, both in absolute (r = 0.74) and relative
(r = 0.70) terms (Fig. 3). When the relative fiber area
was considered, significant positive correlations were also
found between the percent relative area of ST fibers and
the absolute (r = 0.73) and relative (r = 0.62) lactate
thresholds. In addition, positive correlations were noted
between the percent of ST fibers and VOW maxand percent
relative area of ST fibers and VOW max.
Maximal oxygen consumption. Although Vo2 maxdif-
fered widely among the subjects, their oxygen uptake at
submaximal work rates of the same intensity were the
same. Inasmuch as an increase in maximal oxygen uptake
has been shown to be associated with a slowing of gly-
cogenolysis and lower muscle and blood, lactate levels
(24), the high correlation found between Vo2 mstxand the
absolute lactate threshold (r = 0.91) was expected. How-
ever, somewhat surprisingly, when the lactate threshold
was reported as a percent of VOW max, the correlation
although reduced was still significant (Table 2, Fig. 4).

DISCUSSION

Maximal oxygen consumption. In the present study

0 20 40 60 80 100 % W2max. significant correlations were found among v02 Max as
0 9.3 18.5 27.8 37.0 46.3 VO2ml/kg x mid measured by open-circuit spirometry and the absolute
1. Method
FIG. of determining relative and absolute lactate thresh- and relative lactate thresholds. This is in agreement with
old for 1 subject. VE, expired pulmonary ventilation/min; HLa, blood previous findings that physically trained individuals have
lactate. lower blood lactate concentrations than untrained at the

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Copyright © 1980 American Physiological Society. All rights reserved.
 DETERMINANTS OF LACTATE THRESHOLD 525

60

l
l y = x(.61) t 23.4

40
T

.-E
* 30
m
<
ii
N 20
0
*>
L
d IO
I
L 1 1 1 1 1 I 1
1 1 1
35 40 45 50 55 60 65
20 30 40 V02 max. ml/kg x min.-l
602 yl/hr x g-l x lo*
FIG. 4. Relationship between maximal oxygen consumption and rel-
FIG. 2. Relationship between respiratory capacity (Qo~) of vastus ative (LT-%VO,) and absolute lactate thresholds (LT-VO,), respec-
lateralis muscle and ab,solute lactate threshold (LT-HOP) and maximal tively. Regression equation was determined by linear regression anal-
oxygen consumption (VO,), respectively, Regression equation was de- ysis.
termined by linear regression analysis.

same absolute and relative work rates during submaximal

exercise (6,17,23,24). It has also been shown that muscle
lactate levels are lower both at the same absolute and at
the same relative work levels in well-trained as compared
to untrained men (24).
Maximal oxygen consumption was also found to be
significantly related to the muscle respiratory capacity,
as indicated by the rate of pyruvate oxidation by muscle
homogenates. Several studies have indicated the exist-
ence of a high correlation between the activity of selected
oxidative enzymes and maximal oxygen consumption (1,
4, 25). In addition, a high positive relationship (r = 0.82)
has been demonstrated between J?o~ max and the volume
density of mitochondria in biopsies from the vastus la-
teralis muscle in both trained and untrained men and
women (13).
Muscle respiratory capacity. The finding that oxygen
uptake was identical for all the subjects at the same
submaximal work rate provides evidence that oxygen
delivery was not limiting. Along the same lines, Saltin et
al. (25) have reported that lactate release from an endur-
ance-trained leg was significantly less than from its con-
y = x(.31)$ I 1.72 tralateral control during the same absolute submaximal
l
exercise even though blood flow and oxygen consumption
were the same for both legs. Other investigators (2-6)
” ,/ have noted that blood flow per kilogram of working
20 30 40 50 60 70 80 muscle was lower in the trained state at the same abso-
% ST FIBERS lute submaximal work load, even though oxygen con-
FIG. 3. Relationship between percent of slow-twitch (ST) fibers and sumption remained unchanged due to an increased ar-
relative (LT-%J?o?) and absolute lactate thresholds (LT-VO,), respec- terial-mixed venous 02 difference. In this context, the
tively. Regression equation was determined by linear regression anal- high correlation found between the muscle’s respiratory
ysis. canacitv and the absolute and relative lactate thresholds

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Copyright © 1980 American Physiological Society. All rights reserved.
526 IVY ET AL.

suggests that the mitochondrial content of muscle is Percent of ST fibers. Both active (15) and inactive (20)
important in determining the work rate at which blood skeletal muscle can remove lactate during exercise. It has
lactate starts to accumulate. been suggested that 50% of that removed by the exercis-
Several cellular mechanisms may be responsible for ing muscle is immediately catabolized to CO2 and thereby
the significant correlation between the muscle’s respira- used as fuel. The blood lactate concentration during
tory capacity and the lactate threshold. Saltin and Karls- exercise therefore represents the balance between its
son (24) have shown that at the same absolute submax- production and oxidation.- ST fibers have a high mito-
imal work level the fall in creatine phosphate and ATP chondrial density (13) and mitochondrial enzyme activity
concentrations and the rate of glycogen depletion and (7, B), which favor oxidative energy production. The
lactate production in the quadriceps muscle are lower in metabolic profile of FT fibers, on the other hand, favors
the same individual in the trained than in the untrained glycolytic energy production (7, 27). Also, as a result of
state. Thus, the steady-state level of the hypothesized a high lactate dehydrogenase-H isozyme subunit concen-
intramitoch.ondrial ADP and Pi attained at a given sub- tration, ST fibers have a greater lactate oxidative capac-
maximal level of work is probably related to the muscle’s ity than FT fibers (26). The finding that the percent of
respiratory capacity: the higher the respiratory capacity ST fibers was related to both the absolute and relative
the lower the steady-state-level of ADP and Pi obtained. lactate thresholds would suggest that the ratio of ST to
The intracellular levels of Pi, AMP, ADP, and ATP to a FT fibers may exert a genetic influence over the lactate
large extent control the rate of glycolysis and glycogen- threshold and possibly control the range in which the
olysis; because of lower steady-state cytoplasmic levels relative lactate threshold can shift. This could partly
of Pi, AMP, and ADP and high levels of ATP, glycolysis explain the high submaximal capacities df elite marathon
and glycogenolysis should therefore occur at a slower runners who possessboth a high relative lactate thresh-
rate at a given submaximal work level (12). old (17) and a high percent of ST fibers (3).
The rate of lipid oxidation is also associated with the Though the high correlation between the muscle’s
muscle’s respiratory capacity. Physi tally tra ined individ- respiratory capacity and lactate threshold and between
uals derive a much greater percent of their energy from the percent of ST fibers and lactate threshold do not, of
fatty acid oxidation than do untrained during exercise of course, prove a cause-and-effect relationship, it seems
the same intensity (II, 14). Increasing lipid oxidation likely, in the context of the physiological mechanisms
during exercise has been shown to slow the rate of reviewed above, that such a relationship may exist.
glycoiysis (21) and inhibit lactate formation (3, 22). Fur-
thermore, we have recently demonstrated that the lactate
threshold could be shifted to a higher GO, maXby raising Present addresses: J. L. Ivy, Dept. of Preventive Medicine, Wash-
ington University School of Medicine, St, Louis, MO 63110; and R. T.
the blood free fatty acid concentration (16). In addition, Withers, Physical Education Laboratory, School of Education, Flinders
the trained muscle may increase its capacity for resisting University of South Australia, Bedford Park, South Australia 5042.
lactate production by shunting a greater proportion of
pyruvate to alanine than to lactate (18). Received 3 August 1979; accepted in final form 15 November 1979.

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Copyright © 1980 American Physiological Society. All rights reserved.