1
Kohji Hirakoba
INTRODUCTION
It is well known that lactic acid (La) production during heavy exercise
( i.e., above lactate threshold ) is increased by promotion of anaerobic
glycolyisis. The hydrogen ion (H+) dissociated from La in exercising muscle
and in blood leads to a decrement of pH (i.e., lactic acidosis) which could
affect on the body functions via both positive and negative ways (Sahlin, 1983).
Briefly, the positive effects of the pH decrement are: (1) increased O2 delivery
(Bohr effect) and (2) increased muscle blood flow due to local vasodilation,
whereas the negative effects are: (1) inhibition of glycolysis and lypolysis
(Fredholm and Hjemdahl, 1978), (2) increased water content of muscle
(Sahlin et al., 1978), (3) decreased lactate efflux from muscle (Hirche et al.,
1975), (4) increased requirement of Ca2+ (Donaldson et al., 1978), (5)
decreased myosin ATP-ase activity (Shalder, 1967), (6) increased protein
binding of Ca2+ in sarcoplasmic reticulum (Nakamura and Schwarts, 1972) and
(7) increased of K+ in the extracellular space (Saltin et al., 1981).
The above-mentioned negative mechanisms have been considered mainly
to inhibit exercise performance capacity via an acceleration of local muscle
fatigue since body functions are very sensitive to changes in pH. It is
Department of Human Sciences, Faculty of Computer Scienceand Systems Engineering, Kyushu Institute of Technology
Buffering Capacity in Human SkeletalMuscle: A Brief Review
Kohji Hirakoba2
hypothesized that breakdown of the whole muscle glycogen store (400 mmol
glucosyl units・kg1 dry muscle) to lactate would release 800 mmol of protons
and the concomitant accumulation in H+ ion decrease muscle pH to less than 3
without the protective mechanisms (Sahlin, 1994). It has been, however,
reported in human skeletal muscle that actually measured pH values
immediately after high-intensity exercise were from 6.5 to 6.9 (Table 1). From
the finding that the magnitude of pH decrement was lesser than being
expected from La accumulation in exercising muscle, it is supposed that
skeletal muscle possesses an ability to neutralize H+ loaded. This is defined as
buffering capacity, which is a potent protective mechanism to prevent pH
decrement from excessive acidosis. Thus high buffering capacity in skeletal
Table 1. Muscle pH after high-intensity exercise to fatigue in human
Exercise Condition Muscle SampleMuscle lactate Muscle pH
Referencerest fatigue rest fatigue
maximal treadmill sprinting for 30 s vastus lateralis -- -- 7.17 6.57 Allsop et al. 1990
one-leggedmaximal pedaling for 60 s vastus lateralis -- -- pr 6.92po 6.94
6.596.72
Bell & Wegner 1988
treadmill running at 125%VO2maxgastrocnemiusvastus lateralis --
54.3a
47.0a7.037.04
6.886.86 Costill et al. 1983
dynamic exhaustive cycling at~112%VO2max vastus lateralis 6.8 87.3 7.03 6.72 Green at al. 1993
isometric exercise at 60%MVCdynamic exhaustive cycling
quadriceps femoris6.26.7
64.784.6
7.197.20
6.846.73
Mannion et al. 1993
isometric contraction at 60%MVC quadriceps femorissed 3.5tra 3.4
83.959.2
7.127.10
6.616.80
Sahlin & Henriksson1984
isometric contraction at 68%MVCdynamic exhaustive cycling
quadriceps femoris 4.194.0
114.07.08
6.566.60
Sahlin 1978
incrementalexhaustive cycling vastus lateralis --pr 93.0a
po 111.3a 7.09pr 6.65po 6.69
Sharp et al. 1986
52 times of electrical stimulation lasting1.6 s at 20 Hz followed by 1.6 s of rest
quadriceps femoris 3.2 108.9 7.12 6.55 Spriet et al. 1986
Values are expressed as means.Muscle lactate, mmol・kg1 dry musclel; MVC, maximum voluntary contraction force; VO2max, maximal oxygen uptake;pr, pre-training; po, post-training; sed, sedentrary; tra, traineda Calculated from the conversion factors: 1 mmol・kg1 dry muscle=0.23 mmol・kg1 wet muscle=0.3 mmol・kg1 muscle
water, assuming that water content in muscle is 77 % (Hultman and Sahlin, 1980)
Buffering Capacity in Human Skeletal Muscle: A Brief Review 3
muscle is considered to delay muscle fatigue at the same level of La
accumulation in muscle by attenuating the pH decrement-induced negative
effects, which may be associated with the improvement of performance in short
-term, heavy exercise.
This short review will focus on the components that contribute to
buffering actions in human skeletal muscle and on the effects of physical
training on skeletal muscle buffering capacity.
A large part of H+ dissociated from La during exercise will be buffered in
both intra- and extracellular buffer actions. The pH regulation (acid-base
balance) in the cell during exercise has been indicated to depend on three
buffering processes (Siesjö and Messeter, 1971).
1) Physco-chemical buffering
a. Muscle protein (protein-bound histidine residutes, histidine related
dipeptides)
dipeptide carnosine (N-b-alanyl-metyl-L-histidine)
dipeptide anserine (N-b-alanyl-3-metyl-L-histidine)
b. Inorganic phosphate (HPO42+H+→ H2PO4
)
c. Bicarbonate (HCO3+H+→ CO2+H2O)
2) Metabolic buffering
a. Phosphocreatine (PCr+ADP+H+→ Cr+ATP)
b. Glutamate (Glutamate+NH3→ Gulutamine)
3) Transmembrane fluxes of H+ or HCO3 ions
CONSTITUENTS FOR SKELETAL MUSCLE BUFFERING
CAPACITY
Buffering Capacity in Human Skeletal Muscle: A Brief Review
Table 1. Muscle pH after high-intensity exercise to fatigue in human
Exercise Condition Muscle SampleMuscle lactate Muscle pH
Referencerest fatigue rest fatigue
maximal treadmill sprinting for 30 s vastus lateralis -- -- 7.17 6.57 Allsop et al. 1990
one-leggedmaximal pedaling for 60 s vastus lateralis -- -- pr 6.92po 6.94
6.596.72
Bell & Wegner 1988
treadmill running at 125%VO2maxgastrocnemiusvastus lateralis --
54.3a
47.0a7.037.04
6.886.86 Costill et al. 1983
dynamic exhaustive cycling at~112%VO2max vastus lateralis 6.8 87.3 7.03 6.72 Green at al. 1993
isometric exercise at 60%MVCdynamic exhaustive cycling
quadriceps femoris6.26.7
64.784.6
7.197.20
6.846.73
Mannion et al. 1993
isometric contraction at 60%MVC quadriceps femorissed 3.5tra 3.4
83.959.2
7.127.10
6.616.80
Sahlin & Henriksson1984
isometric contraction at 68%MVCdynamic exhaustive cycling
quadriceps femoris 4.194.0
114.07.08
6.566.60
Sahlin 1978
incrementalexhaustive cycling vastus lateralis --pr 93.0a
po 111.3a 7.09pr 6.65po 6.69
Sharp et al. 1986
52 times of electrical stimulation lasting1.6 s at 20 Hz followed by 1.6 s of rest
quadriceps femoris 3.2 108.9 7.12 6.55 Spriet et al. 1986
Values are expressed as means.Muscle lactate, mmol・kg1 dry musclel; MVC, maximum voluntary contraction force; VO2max, maximal oxygen uptake;pr, pre-training; po, post-training; sed, sedentrary; tra, traineda Calculated from the conversion factors: 1 mmol・kg1 dry muscle=0.23 mmol・kg1 wet muscle=0.3 mmol・kg1 muscle
water, assuming that water content in muscle is 77 % (Hultman and Sahlin, 1980)
Kohji Hirakoba4
It is difficult to quantify the transmembrane of H+/HCO3 fluxes in vivo
because of rapid ionic equilibration and of small fluxes of H+ or HCO3 ions
under short-term exercise (Hultman and Sahlin, 1980). Consequently, the
primary buffer systems in skeletal muscle appear to consist of physico-
chemical and metabolic buffering actions. According to Hultman and Sahlin
(1980), about 61 % of H+ ion uptake in muscle during exercise is due to
physico-chemical buffering and the remaining 39 % of the total H+ ion uptake
in muscle is provided by metabolic buffering processes.
Buffer value (β) is usually expressed as the mmols of acid (H+) or base
(OH) needed to change one pH unit per liter solution (mmol・l1・pH1).
This expression is based on the original study of Van Slyke (1922), and the
unit for β is termed“slyke”.
1 Physicochemical buffering
In generally, protein has been recognized as a major buffer in skeletal
muscle. Bate-Smith (1938) reported that in mammalian muscle in rigor
protein contribution was 25-40 % of skeletal muscle buffering capacity (βm).
Sahlin (1978) showed that βm in human skeletal muscle (quadriceps femoris)
was 68 slykes and protein buffer value was 15 slykes, which corresponds to
about 40 % of physico-chemical buffering and to 22 % of βm. In human muscle
buffer value of protein has been estimated to be around 15-45 slykes or
~ 40 % of total buffering capacity (Kemp et al., 1993). Concerning histidine
containing dipeptides (mainly carnosine), Harris et al. (1990) measured βm in
Thoroughbred horse and Greyhound dog and man, and found that most of the
variation in βm among the three species could be accounted for by carnosine
5Buffering Capacity in Human Skeletal Muscle: A Brief Review
levels in their skeletal muscles. If we try to calculate the rate of contribution
of carnosine to βm from the data of Harris et al. (1990), it will give the rates of
contribution ranging from 6.7 (man) to 30.6 % (Thoroughbred) of βm. This
calculation reveals a lower rate of carnosine contribution to βm in human
skeletal muscle.
Free inorganic phosphate (Pi) has been indicated to be the second most
important buffer constituent in physico-chemical buffering actions.
Monohydrogen phosphate (HPO42) readily accepts an extra H+ to become
dihydrogen phosphate (H2PO4). When muscle pH decreases from 7.0 (rest)
to 6.4 (fatigue), assuming that H+ ion uptake per mmol of Pi is 0.33 mmol,
the buffer value of Pi can be calculated from Pi concentration in skeletal
muscle at rest and the changes of muscle pH (β=0.33 ×[Pi]/∆pH; Hultman
and Sahlin, 1980). The Pi concentration previously reported (Sahlin, 1978;
Sahlin et al., 1997) is 9.4-13.2 mmol・l1 muscle water (31.3-44.0 mmol・kg1
dry muscle) so that the contribution of Pi (5.2-7.3 slykes) is only approxi-
mately 8-11 % of βm (68 slykes). Gordon et al. (1991) have described that
the importance of phosphate buffer system is much greater in intracellular
environment although its buffer system plays a small role in exracellular space.
Namely, this implies that the pH (6.9-7.1 at rest; 6.4-6.6 during exercise) in
intracellular fluid is close to the effective pH (pH=6.1-7.7) of phosphate buffer
system.
Maximum buffering capacity in bicarbonate (CO2-HCO3) buffer system
is obtained when CO2 can diffuse freely in and out of the body fluids. Dynamic
exercise is regarded as an open system where exchanges substances with
blood and static exercise as a closed system where CO2 is trapped (CO2-HCO3
Kohji Hirakoba6
buffer system is negligible). Since local circulation within the muscle utilizing
during isometrc contractions (static exercise) is occluded due to muscle
tension exerted, the efflux of CO2 from the muscle to blood is very small
compared with dynamic exercise, which would lead to the inhibition of the
CO2-HCO3 buffering action (HCO3
+H+ → CO2+H2O ) in the muscle.
According to Sahlin’s study (1978), βm (73 slykes) in dynamic bicycle
exercise was higher than that in static exercise (57 slykes). The difference of
βm between these two types of exercise is approximately equivalent to the
buffering capacity of CO2-HCO3 system, indicating that the CO2-HCO3
buffer
system in skeletal muscle could contribute to 18-20 % of βm.
2 Metabolic buffering
There are two buffer constituents of metabolic buffering processes, i.e.,
phosphocreatine and glutamate. The buffering action of glutamate is negligible,
since glutamate buffering action is very small in human muscle (Sahlin, 1978).
Breakdown of phosphocreatine (PCr) gives an immediate energy source to
resynthesize ATP from ADP and Pi during short-term, heavy exercise and
is also associated with proton consumption (PCr+ADP+H+→ creatine+ATP).
The stoichiometrical uptake (α) of H+ per mmol PCr depleted during exercise
increases with the decrease of muscle pH within the physiological pH range,
as described in an equation: α=1/[1+10(pH-pKa)]. Since hydrolysis of 1 mmol
PCr can theoretically remove H+ ion between 0.38 and 0.83 mmol over the
range pH 7.0-6.0, the buffer value of PCr during exercise can be calculated
using a following equation: β=α × ∆[PCr]/∆pH (Adams et al., 1990). Maximal
proton uptake of PCr at fatigue (α=0.70 at muscle pH=6.4; PCr content=78
7Buffering Capacity in Human Skeletal Muscle: A Brief Review
mmol・kg1 dry muscle, Sahlin et al., 1997) is expected to be about 55 mmol
・kg1 dry muscle (β=27 slykes), resulting in the contribution of 40 % to
βm. It has been reported that the content of PCr is higher in type II fibers
with high glycolytic capacity than in type I fibers with low glycolytic and high
oxidative capacity ( Hultman and Sahlin, 1980; Nevill et al., 1996 ) .
Consequently it is possible that metabolic buffering may vary between subject
to subject, depending on muscle fiber type composition and/or PCr content
(Weston et al., 1996).
1 Methods for estimating skeletal muscle buffering capacity m
The methods for estimating βm are: (1) Titrimetric determination of
muscle homogenate (in vitro method, βmvitro) and (2) Calculating the ratio
(∆La/∆pH) of the changes in muscle La and pH due to a exercise stress test
(in vivo method, βmvivo). In HCl titrimetric determination, freeze-dried muscle
is homogenized at a dilution of 20-30 mg dry muscle per ml (50-33 µl per
mg dry muscle) of homogenizing solution containing 145 mM KCl, 10 mM
NaCl, 5 mM IAA ( iodoacetic acid is used to inhibit glycolysis during
homogenization), and pH=7.0. Thereafter the titration is performed with a
serial addition of 2 µl aliquots of HCl (10 mmol・l1) over the range pH 7.2
-6.2 at a temperature of 37 ℃. βmvitro is calculated from the fitted titration
curve, which means the number of mmoles of H+ required to change the pH of
1 kg of dry muscle from 7.1 to 6.5 (Figure 1). This pH range represents
the changes in muscle pH from rest to fatigue in high-intensity exercise as
ESTIMATIION OF SKELETAL MUSCLE BUFFERING
CAPACITY
Kohji Hirakoba8
listed in Table 1. In contrast, βmvivo is estimated from the changes in muscle
La and pH before (rest) and immediately after exercise to fatigue and is
calculated from a following equation: βmvivo=(Lawork-Larest)/(pHrest-pHwork).
Thus it seems likely that minimal determination errors of La and pH would
lead to greater error in buffer value by calculation from the two points of La
and pH before and after exercise (Mannion et al., 1993). In addition, in vivo
method needs to take muscle sample twice for one trial.
Figure 1. Typical HCl titration curve for human muscle homogenate (Hirakoba, Tonkonogi& Sahlin, unpublished work). The titration was performed with the serial additionof 2 µl aliquots of HCl (10 mM). The number of mmoles of H+ corresponded tothe pH 7.1 and 6.5 were calculated from the interpolation of the titration curve.
9Buffering Capacity in Human Skeletal Muscle: A Brief Review
2 Comparison of mvitro and mvivo
According to the theory on acid-base balance in muscle, βmvitro gives only
physico-chemical buffering capacity. In addition, it has been reported that
buffering capacity in wet muscle was 15-20 % higher than that in dry muscle
and this difference of βmvitro between the two muscle samples resulted from
the loss of HCO3 under freeze-drying process of muscle (MaCutecheon et
al., 1987, Marlin and Harris, 1991). The value of physico-chemical buffering
capacity in dry muscle without bicarbonate buffering would be lower compared
with the theoretical value. βmvivo reflects total muscle buffering capacity (both
physico-chemical and metabolic buffering actions). Therefore, βmvivo is thought
to be higher than βmvitro since βmvitro measured by the titration technique of
muscle homogenate does not include metabolic buffering processes.
EFFECTS OF HIGHINTENSITY EXERCISE TRAINING ON m
βm could be considered as an important factor to improvement of
performances in short-term events. Recently, Green et al. (1996) found a
significant, positive correlation (r=0.81) between βm and anaerobic ATP yield
in well-trained male cyclists, suggesting that the higher βm enhances ATP
resynthesis rate at high-intensity exercise. Sahlin and Henriksson (1984)
reported that trained men who carried out anaerobic high-intensity training
had a higher βm than untrained men did. Parkhouse et al. (1985) also
observed that deproteinized muscle buffering capacity in sprinters and rowers
showed higher values compared to marathoners and untrained subjects. From
the cross-sectional comparisons, the βm is anticipated to be increased by high
-intensity exercise training. This possibility has been supported by the
Figure 1. Typical HCl titration curve for human muscle homogenate (Hirakoba, Tonkonogi& Sahlin, unpublished work). The titration was performed with the serial additionof 2 µl aliquots of HCl (10 mM). The number of mmoles of H+ corresponded tothe pH 7.1 and 6.5 were calculated from the interpolation of the titration curve.
Kohji Hirakoba10
longitudinal studies of Bell and Wenger (1988), Sharp at al. (1986) and
Weston et al. (1997) in human (Table 2) and of Troup et al. (1986) and
Weston et al. (1996) in animal. Mizuno et al. (1990) showed a significant,
positive correlation (r=0.83) between relative increases in βm and in short
-term running performance as a result of two weeks of training at high altitude
(2,700 m above sea level), suggesting that physical training under hypoxic
condition would be useful to the increased βm.
On the contrary, Mannion et al. (1995) have recently indicated that βm is
not a major limiting factor to the performance of high-intensity exercise, which
is consistent with the results that high-intensity training had little effect on βm
in spite of the enhanced performances of high-intensity anaerobic exercise
(Mannion et al., 1994, Nevill et al. 1989). However, Nevill et al. (1989)
estimated the changes of βmvivo and βmvitro with high-intensity training, and
Table 2. Changes in muscle buffering capacity before and after high-intensity training in human
Values are expressed as means.Muscle buffering capacity, mmol・kg1 dry muscle・pH1; TE, training at 4.19 rad・s1; TS, training at 1.05 rad・s1
a Calculated from the conversion factors as given in table 1b Calculated form the difference of mean values between pre- and post-trainingc Significantly increased from pre-training value
Type of Ttaining Muscle Sample MethodMuscle Buffering
Capacity % increaseb Reference
pre post
one-leggedsprint trainingfor 7 wk vastus lateralis in vitro 217a 251a +15.7c Bell & Wegner 1988
sprint training for 8 wk vastus lateralis in vitro 178a 170a 4.5 Bevan et al. 1986
isokinetic knee extensiontraining for 16 wk
quadriceps femoris in vitroTF 159TS 154
160165
+0.6+7.1
Mannion et al. 1994
sprint training for 8 wk vastus lateralisin vitroin vitro
293a
225a422a
237a+44.0+ 5.3
Nevill et al. 1989
sprint training for 8 wk vastus lateralis in vitro 194a 265a +36.6c Sharp et al. 1986
interval training for 4 wk vastus lateralis in vitro 207 240 +15.9c Weston et al. 1997
11Buffering Capacity in Human Skeletal Muscle: A Brief Review
found that βmvivo showed a tendency to be increased despite the fact that βmvitro
was unchanged after high-intensity training. As mentioned earlier, βmvitro
includes only physico-chemical buffering but excludes metabolic buffering
actions and transmembrane fluxes of H+ or HCO3 ions during exercise
(Mannion et al., 1993). Hirakoba et al. (1992) reported that the contribution
of bicarbonate buffer system to total buffering actions would be increased by
high-intensity training, presumably owing to the greater transmembrane fluxes
of H+ or HCO3 ions in post-training status compared with pre-training. If,
for example, physico-chemical buffering was unchanged but metabolic buffering
and transmenbrane fluxes of H+ or HCO3 ions were increased by training,
it could be thought that although βmvitro maintains a constant value, an increase
in βmvivo occurs after training. Therefore, it is conceivable that conflicting
results could be induced when estimating βm by either in vivo or in vitro.
Sahlin (1994) has also stated that the reason for this discrepancy between
studies is unclear but may be due to methodological differences. Another
possible explanation for this is that βm is significantly related to the cross
-sectional area occupied by type II fibers (Parkhouse et al., 1985, Sewell et al.,
1991, Weston et al., 1996). Although human vastus lateralis is often used to
estimate βm, this muscle is acknowledged to have very heterogeneous fiber
type composition with large inter-individual variation (Johnson et al., 1973).
Values are expressed as means.Muscle buffering capacity, mmol・kg1 dry muscle・pH1; TE, training at 4.19 rad・s1; TS, training at 1.05 rad・s1
a Calculated from the conversion factors as given in table 1b Calculated form the difference of mean values between pre- and post-trainingc Significantly increased from pre-training value
Type of Ttaining Muscle Sample MethodMuscle Buffering
Capacity % increaseb Reference
pre post
one-leggedsprint trainingfor 7 wk vastus lateralis in vitro 217a 251a +15.7c Bell & Wegner 1988
sprint training for 8 wk vastus lateralis in vitro 178a 170a 4.5 Bevan et al. 1986
isokinetic knee extensiontraining for 16 wk
quadriceps femoris in vitroTF 159TS 154
160165
+0.6+7.1
Mannion et al. 1994
sprint training for 8 wk vastus lateralisin vitroin vitro
293a
225a422a
237a+44.0+ 5.3
Nevill et al. 1989
sprint training for 8 wk vastus lateralis in vitro 194a 265a +36.6c Sharp et al. 1986
interval training for 4 wk vastus lateralis in vitro 207 240 +15.9c Weston et al. 1997
Kohji Hirakoba12
There have been no direct studies to clarify the mechanisms by which
βm is increased. Many proteins in intracellular fluid act as buffers and its
incorporation into skeletal muscle with training may result in a higher ratio of
protein to weight of muscle. This response to training would account partly for
the increased βm. Parkhouse et al. (1985) pointed out that the high βm in
anaerobically trained athletes may be associated with elevated carnosine levels
in their skeletal muscles, because a significant, positive correlation (r=0.69)
was found between βm and carnosine levels. Moreover, Harris et al. (1990)
have suggested that the higher βm in horse and dog, compared with man,
is predominantly due to higher muscle contents of histidine containing
dipeptides in these species. This idea has been supported by the study of
Sewell et al. (1991) in which non-carnosine muscle buffering capacity (mea-
sured as the difference between βm and carnosine buffering capacity) was
constant at all fiber compositions in horse and pony. However, these results in
the cross-sectional studies are indirect evidences to verify the mechanisms
of the increased βm due to high-intensity training. There have been found no
changes in carnosine levels in human muscle after eight weeks of anaerobic
sprint training (Bevan et al., 1986) and 16 weeks of isokinetic training of knee
extensors (Mannion et al., 1994). Sahlin and Henriksson (1984) indicated
that even if a maximal buffering power of carnosine was assumed, its
contribution was only 2-4 slykes or < 7% of buffering capacity in human
muscle. Therefore, another explanations should be sought for the adaptive
MECHANISMS RELATED TO INCREASED m WITH HIGH
INTENSITY EXERCISE TRAINING
13Buffering Capacity in Human Skeletal Muscle: A Brief Review
mechanisms related to the increased βm observed after training in man.
CONCLUSIONS
It is inferred that the results of βm between studies may be different,
depending on the methods for estimating βm (in vivo or in vitro methods).
It is important to establish the components of buffering being measured by
either in vivo or in vitro methods as indicated by Mannion et al. (1993) and the
methods for estimating βm should be carefully chosen according to the purpose
of the study, particularly when determining the longitudinal changes in βm
after training.
There have been no direct assessments on the adaptive mechanisms of
the increased βm due to high-intensity training and it is unclear about the
mechanisms by which the training-induced increase in βm occurs. However,
several previous studies have indicated that the higher βm found
predominantly in sprint-trained athletes may be a critical factor of anaerobic
exercise performances accompanied by La accumulation and suggested that
proton buffering proteins (carnosine) levels could be responsible for the in-
creased βm due to training. It is possible that the higher carnosine content in
skeletal muscle and the higher βm may be due to exposure to prolonged
periods of hypoxia and acidosis with high-intensity exercise training, but there
is only indirect evidence to support this possibility. It is necessary to prove
the obvious relation of cause and effect regarding the increased βm with
training. Consequently, more detail studies should be carried out to clarify
as to which buffer constituent contributes to the increased βm observed with
high-intensity training.
Kohji Hirakoba14
ACKNOWLEDGEMENTS
REFERENCES
Adams GR, Foley JM, Meyer RA (1990) Muscle buffer capacity estimated
from pH changes during rest-to-work transitions. Journal of Applied
Physiology 69: 968-972
Allsop P, Williams C (1990) Continuous intramuscular pH measurement
during the recovery from brief, maximal exercise in man. European
Journal of Applied Physiology 59: 465-470
Bate-Smith EC (1938) The buffering of muscle in rigor: protein, phosphate
and carnosine. Journal of Physiology (London) 92: 336-343
Bell GJ, Wenger HA (1988) The effect of one-legged sprint training on
intramuscular pH and nonbicarbonate buffering capacity. European Journal
of Applied Physiology 58: 158-164
Bevan L, Sharp RL, Stanford PD (1986) The effects of eight weeks of sprint
training of the concentration of carnosine in human skeletal muscle.
Medicine and Science in Sports and Exercise(Abstract) 17: 192
Costill DL, Barnett AR, Sharp R, Fink WJ, Katz A (1983) Leg muscle pH
following running. Medicine and Science in Sports and Exercise 15: 325
-329
Donaldson SKB, Hermansen L, Bolles L (1978) Differential, direct effects
The author would like to thank Associate Professor Kent Sahlin of Departmentof Physiology and Pharmacology (Physiology III), Karolinska Institute, Sweden for hisvaluable and helpful suggestions and Mr. Mikael Tonkonogi for his technical assistancewith the measurement for muscle buffering capacity.
15Buffering Capacity in Human Skeletal Muscle: A Brief Review
of H+ on Ca2+-activated force of skinned filügers from the soleus, cardiac
and adductor magnus muscles of rabbits. Pflügers Archiv 376: 55-65
Fredholm B, Hjemdahl P (1976) Inhibition by acidosis of adenosine 3’-5’-
cyclic monophosphate accumulation and lypolysis in isolated rat fat cell.
Acta Physiologica Scandinavica 96: 160-169
Green S, Dawson BT, Goodman C, Carey MF (1996) Anaerobic ATP
production and accumulated O2 deficit in cyclists. Medicine and Science in
Sports and Exercise 28: 315-321
Gordon SE, Kraemer WJ, Pedro JG (1991) Increased acid-base buffering
capacity via dietary supplementation: Anaerobic exercise implications.
Journal of Applied Nutrition 43: 40-48
Harris RC, Marlin DJ, Dunnett M, Snow DH, Hultman E (1990) Muscle
buffering capacity and dipeptide carnosine in the Thoroughbred horse,
Greyhound dog and man. Comparative Biochemistry and Physiology 97A:
249-251
Hirakoba K, Maruyama A, Inaki M, Misaka K (1992) Effect of endurance
training on excessive CO2 expiration due to lactate production in exercise.
European Journal of Applied Physiology 64: 73-77
Hirche H, Hombach V, Langor HD, Wacker U, Busse J (1975) Lactic acid
permeation rate in working gastrocnemii of dogs during metabolic
alkalosis and acidosis. Pflügers Archiv 356: 209-222
Hultman E, Sahlin K (1980) Acid-base balance during exercise. In: Exercise
and Sport Sciences Reviews (eds) Hulton RS, Millar DL, Franklin
Institute Press, USA, 8: 41-128
Johnson MA, Polger J, Weightman D, Appleton D (1973) Data on the
Kohji Hirakoba16
distribution of fiber types in thirty-six human muscles - An autopsy study.
Journal of Neurological Science 18: 111-129
Kemp GJ, Taylor DJ, Styles P, Radda GK (1993) The production, buffering
and efflux of protons in human skeletal muscle during exercise and
recovery. NMR in Biomedicine 6: 73-83
Mannion AF, Jakeman PM, Willan PLT (1993) Determination of human
skeletal muscle buffer value by homogenate technique: methods of
measurement. Journal of Applied Physiology 75: 1412-1418
Mannion AF, Jakeman PM, Willan PLT (1994) Effects of isokinetic training of
the knee extensors on high-intensity exercise performance and skeletal
muscle buffering. European Journal of Applied Physiology 68: 356-361
Mannion AF, Jakeman PM, Willan PLT (1995) Skeletal muscle buffer value,
fiber type distribution and high intensity exercise performance in man.
Experimental Physiology 80: 89-101
Marlin DJ, Harris RC (1991) Titrimetric determination of muscle buffering
capacity (βmtir) in biopsy samples. Equine Veterinary Journal 23: 193
-197
McCutcheon LJ, Kelso TB, Bertocci LA, Hodgson DRJ, Bayly WM, Gollnick
PD (1987) Buffering and aerobic capacity in equine muscle: Variation and
effect of training. In: Equine Exercise Physiology 2 (eds) Gillespie JR,
Robinson NE, ICEEP Publications, California, pp348-358
Mizuno M, Juel C, Bro-Rusmussen T, Mygind E, Schibye B, Rusmussen B,
Saltin B (1990) Limb skeletal muscle adaptation in athletes after training
at altitude. Journal of Applied Physiology 68: 496-502
Nakamura Y, Schwarts A (1972) The influence of hydrogen ion concentration
17Buffering Capacity in Human Skeletal Muscle: A Brief Review
on calcium binding and release of skeletal muscle sarcoplasmic reticulum.
Journal of General Physiology 59: 22-32
Nevill ME, Boobis LH, Brooks S, Williams C (1989) Effect of training on
metabolism during treadmill sprinting. Journal of Applied Physiology 67:
2376-2382
Nevill ME, Bogdanis GC, Boobis LH, Lokomy HKA, Williams C (1996)
Muscle metabolism and performance during sprinting. In: Biochemistry
of Exercise IX (eds) Maughan RJ, Shirreffs SM, Human Kinetics Pub-
lishers Inc, Champain, Illinois, pp243-259
Parkhouse WS, McKenzie DC, Hochachka PW, Ovalle WK (1985) Buffering
capacity of deproteinized human vastus lateralis muscle. Journal of
Applied Physiology 58: 14-17
Sahlin K, Alvestrand A, Brandt R, Hultman E (1978) Intracellular pH and
bicarbonate concentration in human muscle during recovery from exercise.
Journal of Applied Physiology 45: 474-480
Sahlin K (1978) Intracellular pH and energy metabolism in skeletal muscle of
man with special reference to exercise. Acta Physiologica Scandinavica
455 (Suppl): 1-56
Sahlin K (1983) Effects of acidosis on energy metabolism and force generation
in skeletal muscle. In: Biochemistry of Exercise (eds) Knuttgen HG,
Vogal JA, Poortman J, Human Kinetics Publishers Inc, Champain, Illinois,
pp 151-160
Sahlin K, Henriksson J (1984) Buffer capacity and lactate accumulation in
skeletal muscle of trained and untrained men. Acta Physiologica
Scandinavica 122: 331-339.
Kohji Hirakoba18
Sahlin K (1994) Acid-base balance during high intensity exercise. In: Oxford
Textbook of Sports Medicine (eds) Harries M, Williams C, Stanish WD,
Micheli LJ, Oxford University Press Inc, New York, pp46-52
Sahlin K, Söderlund K, Tonkonogi M, Hirakoba K (1997) Phosphocreatine
content in single fibers of human muscle after sustained submaximal
exercise. American Journal of Physiology 273 (Cell Physiol 42): C172
-C178
Saltin B, Sjogaard G, Gaffney FA, Rowell B (1981) Potassium, lactate and
water fluxes in human quadriceps muscle during static contractions.
Circulation Research 48: 118-124
Schalder M (1967) Proportionale aktivierung von ATPase activitat und
kontraktionsspannung durch calciumionen in isoliterten contractilen
strukturen verschiedener muskeltarten. Pflügers Archive 296: 70-90
Seisjö BK, Messeter K (1971) Factors determining intracellular pH. In: Ion
Homeostasis of the Brain (eds) Seisjö BK, Sorensen SC, Copenhagen:
Munksgaard
Sewell DA, Harris RC, Dunnett M (1991) Carnosine accounts for most of the
variation in physico-chemical buffering in equine muscle. Equine Exercise
Physiology 3: 276-280
Sharp RL, Costill DL, Fink WJ, King DS (1986) Effects of eight weeks of
bicycle ergometer sprint training on human muscle buffer capacity.
International Journal of Sports Medicine 7: 13-17
Spriet LL, Söderlund K, Thomson JA, Hultman E (1986) pH measurement in
human skeletal muscle samples: effect of phosphagen hydrolysis. Journal
of Applied Physiology 61: 1949-1954
19Buffering Capacity in Human Skeletal Muscle: A Brief Review
Troup JP, Metzger JM, Fitts RH (1986) Effect of high-intensity exercise
training on functional capacity of limb skeletal muscle. Journal of Applied
Physiology 60: 1743-1751
Van Slyke DD (1922) On the measurement of buffer values and on the
relationship of buffer value to the dissociation constant of the buffer and
the concentration and reaction of the buffer solution. Journal of Biological
Chemistry 52: 525-570
Weston AR, Wilson GR, Naokes TD, Myburgh KH (1996) Skeletal muscle
buffering capacity is higher in the superficial vastus than in the soleus
of spontaneously running rats. Acta Physiologica Scandinavica 157: 211
-216
Weston AR, Myburgh KH, Lindsay FH, Dennis SC, Naokes TD, Hawley JA
(1997) Skeletal muscle buffering capacity and endurance performance
after high-intensity interval training by well-trained cyclists. European
Journal of Applied Physiology 75: 7-13