Effects of Exercise on Protein Metabolism

Chapter 10
Effects of Exercise on Protein Metabolism
PETER W.R. LEMON
Introduction
For at least 150 years, scientists have studied fuel
use during various types of physical exercise.
Over this time, there has been considerable
debate relative to the importance of dietary
protein for individuals who exercise regularly.
In fact, the understanding of protein’s role in
exercise metabolism has changed dramatically
several times since the middle of the 19th
century. In the mid-1800s it was thought that
protein was the major fuel for muscle contraction
(von Liebig 1842) and, consequently, it is understandable that large amounts of protein were
consumed by the athletes of that time. However,
a number of studies completed later in the 19th
century and during the first part of the 20th
century (reviewed in Cathcart 1925) indicated
that protein played a much smaller role in terms
of exercise fuel (contributing less than 10% of the
energy expended during exercise). As a result,
at least in the scientific community, the belief
regarding the importance of protein in exercise
metabolism was essentially totally reversed
(going from the major contributor to virtually
no contribution). Based on these data, it was
believed that exercise did not increase one’s
need for dietary protein. It is unknown why the
observed protein contribution was considered
unimportant, but likely it was an over-reaction
to the new information which was so vastly
different from the prevailing view of the time or
perhaps simply the belief that the amount of
protein typically consumed was sufficient to
cover this small increased need. In any event, the
understanding that dietary protein needs were
unaffected by physical exercise became so dominant that the vast majority of the exercise metabolic work throughout the first three-quarters of
the 20th century concentrated on carbohydrate
and fat and, as a result, almost totally ignored the
role of protein (Åstrand & Rodahl 1977).
Beginning in the 1970s, first sporadically (Felig
& Wahren 1971; Poortmans 1975; Haralambie &
Berg 1976; Dohm et al. 1977; Lemon & Mullin
1980; Lemon & Nagle 1981; White & Brooks 1981;
Lemon et al. 1982), but recently more regularly
(for review, see Lemon 1997), studies began to
appear which suggested that protein intakes
in excess of sedentary recommendations may
be beneficial for those who regularly engage in
strenuous physical exercise. However, the issue
of exercise effects on protein need is extremely
complex and still there is no absolute consensus
(Lemon 1987, 1991, 1996; Butterfield 1991; Evans
1993; Millward et al. 1994; Rennie et al. 1994;
Wagenmakers & van Hall 1996). Further complicating this issue is the fact that the current
dietary recommendations for protein in several
countries do not adequately address this topic
because they are based primarily on studies of
subjects who were essentially sedentary. Moreover, some recommendations have not been
kept up to date. For example, not only were the
current recommendations in the United States
published a number of years ago but, in addition,
they do not contain a single reference relating
to the possible influence of chronic exercise on
133
134
nutrition and exercise
(a)
protein requirements after 1977 (US Food and
Nutrition Board 1989). As a great many studies
have examined the question of exercise effects on
dietary protein needs since then, the rationale for
this strategy is unclear. Interestingly, over this
entire time period (in fact, going as far back as
there are records), regardless of the scientific
opinion, many athletes, especially those
involved in heavy resistance (strength/power)
activities, have consumed routinely vast
amounts (300–775% of the recommended daily
allowance (RDA)) of dietary protein (Steen 1991;
Kleiner et al. 1994).
With this background in mind, this chapter
reviews some of the more recent experimental
results, outlines several methodological concerns
that may compromise some of the experimental data, examines the limited information on
whether supplemental protein can enhance
exercise performance, and considers a variety of
potential underlying mechanisms responsible, in
an attempt to understand how physical exercise
affects dietary protein needs.
(b)
Fig. 10.1 Athletes in both strength and endurance
events have a greater dietary protein requirement than
sedentary individuals. (a) Photo © Allsport / J.
Jacobsohn. (b) Photo © Allsport / G.M. Prior.
Protein metabolism simplified
A brief outline of how the body metabolizes
protein is shown in Fig. 10.2. Although the free
amino acid pool(s) contain(s) only a very small
percentage of the body’s amino acids (the vast
majority are in tissue protein), the important role
of the body’s free amino acid pool(s) (through
effects of exercise on protein metabolism
or flux) can be measured. This requires only
minimal invasiveness because tissue values
(enrichment) can be estimated from blood (reciprocal pool model; Matthews et al. 1982; Horber
et al. 1989) or urine samples (assumption is that
the urinary enrichment is representative of the
end product of protein breakdown). By combining these data with dietary intake (and infusion
rate, if applicable), and/or measures of oxidation
(requires breath sampling), it is possible to
estimate whole-body protein degradation rates
(Picou & Taylor-Roberts 1969):
which all amino acids must pass) is indicated by
the size and central location of its sphere in Fig.
10.2. Physiologically, there are only three ways
amino acids can enter the free pool(s) (from
dietary protein during digestion, from tissue
protein breakdown, or as dispensable — that is,
non-essential — amino acids formed in the body
from NH3 and a carbon source; numbers 1, 2 and
3, respectively, in Fig. 10.2). Of course, some consumed amino acids are never absorbed (lost in
faeces) and a fourth method of input is possible,
at least in the laboratory (via intravenous infusion of amino acids). When studying indispensible (essential) amino acids, route 3 is
eliminated, as these amino acids cannot be
formed in the body. Once in the free pool(s), there
are also four ways amino acids can leave (secretion into the gut, incorporation into tissue
protein, oxidation — amino acid nitrogen lost in
urine or sweat; carbon in breath — or incorporation into carbohydrate or fat for storage energy —
amino nitrogen lost in urine; letters a, b, c and d,
respectively, in Fig. 10.2). During exercise, routes
a (due to blood redistribution) and d (due to the
overall catabolic stimulus) are considered unimportant. Over time, following constant infusion
or repeated ingestion of a labelled representative
indicator amino acid (tracer), an isotopic equilibrium can be obtained, i.e. input into the free
pool(s) equals output, and movement of the
tracer amino acid through the system (turnover
Fig. 10.2 Simplified diagram of
protein metabolism. Amino acid
entry into the free pool is shown by
numbers and exit from the free
pool by letters. Nitrogen status
(balance) measures involve
quantifying the difference between
all nitrogen intake and excretion
while protein turnover measures
allow estimates of the component
process involved, i.e. whole-body
protein synthesis and degradation.
Adapted from Lemon (1996).
Dietary
protein
(amino
acids)
turnover (or flux) – intake + infusion
= degradation
or whole-body protein synthetic rates (i.e. nonoxidative loss):
turnover – oxidation or urinary excretion
= synthesis
Traditionally, whole-body nitrogen status has
been evaluated by a technique known as nitrogen balance. This involves measuring duplicate
meals to those consumed by the experimental
subjects in order to accurately quantify nitrogen
intake (protein intake is estimated by assuming
that the average nitrogen content of food protein
is 16%, i.e. multiplying the nitrogen intake by
6.25), all routes of nitrogen excretion (typically
only urine and faeces are measured and miscellaneous losses, including through the skin, are
Infusion
(amino acids)
CHO or fat C
+NH3
4
3
1
Urine (N)
Faeces
(C and N)
b
Synthesis
Degradation
2
1
c,d
C oxidized
to CO2
c
Free amino
acid pool(s)
a
Gut
135
d
c
Sweat (N)
C converted to
CHO or fat
Tissue
protein
136
nutrition and exercise
estimated), and then calculating the difference
between the two. Estimating the miscellaneous
nitrogen losses is usually appropriate because in
sedentary individuals they are small, quite consistent and extremely difficult to measure completely. However, with exercise, dermal nitrogen
loss via sweating should be quantified, as it can
be substantial (Consolazio et al. 1963; Lemon &
Mullin 1980). When intake of nitrogen exceeds
the total excreted, one is in positive nitrogen
balance (negative nitrogen balance if excretion
exceeds intake). This latter situation cannot continue for very long without losses of essential
body components because, unlike carbohydrate
and fat, the body does not contain an energy
reserve as protein (all body protein has a structural or functional role). Although ‘negative’ and
‘positive’ as descriptors of balance are commonplace in the literature, it is recommended that
‘status’ be used instead of ‘balance’, to avoid the
terms ‘positive balance’ or ‘negative balance’,
which seem nonsensical.
Nitrogen balance (status) is a classic technique
which has been used in the vast majority of
studies considered by the expert committees in
many countries when determining the recommended dietary allowance for protein (US Food
and Nutrition Board 1989). However, it should
be understood that this method has a number of
limitations (inconvenient for the subjects, labour
intensive for the investigators, tends to overestimate the nitrogen that is actually retained,
i.e. generally overestimates intake and underestimates excretion), and due to its ‘black box’
nature cannot provide specific information about
the various component parts of protein metabolism (Lemon et al. 1992; Fuller & Garlick 1994).
Also, nitrogen status (balance) is affected by
energy balance (Munro 1951), which can confound the data, especially in exercise studies
where this is not always tightly controlled.
Further, a number of potential confounders frequently exist, including: inadequate adaptation
time to changing experimental diets (Scrimshaw
et al. 1972), exercise-induced changes in the time
course and/or relative importance of the various
routes of nitrogen excretion (Austin et al. 1921;
Lemon & Mullin 1980; Dolan et al. 1987), technical problems making complete collections of
nitrogen excretion difficult (Lutwak & Burton
1964; Bingham & Cummings 1983; Lemon et al.
1986; Dolny & Lemon 1988), and the inappropriate use of linear regression to estimate protein
need with either very high or very low protein
diets, i.e. when the response is curvilinear
(Rennie et al. 1994). As a result, the literature
must be examined very critically.
More recently, investigators have utilized the
metabolic tracer technique, where the component parts of the protein metabolism ‘black box’
can be investigated (Waterlow 1995). As alluded
to above, this means one can estimate wholebody protein synthetic rates, if oxidation rates or
urinary excretion are measured, and whole-body
protein degradation rates, if dietary/infusion
rates are measured. Although this technique has
great promise to help elucidate how exercise affects protein metabolism, it too has several limitations, including expense, invasiveness and the
validity of its various assumptions (Young et al.
1989; Wolfe 1992; Garlick et al. 1994; Rennie et al.
1994; Tessari et al. 1996). Although technically
more difficult, muscle protein synthesis, which
represents about 25–30% of whole-body protein
synthesis, can also be measured by quantifying
isotope enrichment in muscle samples obtained
via the needle biopsy technique (Nair et al. 1988;
Chesley et al. 1992; Biolo et al. 1995; MacDougall
et al. 1995).
Evidence that protein needs are
increased with physical exercise
In recent years, a variety of experimental data
which suggest that exercise has dramatic effects
on protein metabolism have begun to accumulate. For example, several investigators have
measured losses in rodent muscle (Varrik et al.
1992) and/or liver protein (Dohm et al. 1978;
Kasperek et al. 1980) following exercise, especially with prolonged endurance exercise (Fig.
10.3). Consistent with these observations, we
effects of exercise on protein metabolism
have measured a 113% increase in the active
muscle urea nitrogen content (268 ± 68 to 570 ± 89
mg · g–1 muscle wet mass) of rodents immediately
following 1 h of running exercise at 25 m · min–1
(unpublished data). Moreover, increased rates
of muscle protein degradation (Kasperek &
Snider 1989) and significant muscle damage
(Armstrong et al. 1983; Newman et al. 1983;
Friden et al. 1988; Evans & Cannon 1991; Kuipers
1994) with exercise are well documented in
several mammalian species (including humans),
especially when the exercise has a significant
eccentric component. Lysosomal proteases, i.e.
cathepsins, have been implicated in this exercise
catabolic response (Seene & Viru 1982; Tapscott et
al. 1982; Salminen et al. 1983; Salminen & Vihko
1984) but some believe (Kasperek & Snider 1989)
these do not play a major role. Recently it has
been suggested (Belcastro et al. 1996) that nonlysosomal proteases, perhaps a calciumactivated neutral protease (calpain), stimulated
by an exercise-induced increased intracellular
calcium may be primarily responsible for the
initial damage which occurs immediately after
exercise. Evidence for this comes not only from
the observation that isozymes of calpain increase
22–30% with exercise (Belcastro 1993) but also
because the pattern of exercise-induced myofibrillar damage is similar to that induced by
calpain (Goll et al. 1992). Lysosomal protease
137
activity may play an more important role in the
muscle damage that is seen later (several days)
following exercise (Evans & Cannon 1991;
MacIntyre et al. 1995). Whether increased protein
intake can reduce this damage or speed the
subsequent repair processes are interesting
questions.
Together, the large efflux of the amino acids
alanine (Felig & Wahren 1971) and glutamine
(Ruderman & Berger 1974) from active muscle, as
well as the frequently observed accumulation/
excretion of protein metabolism end products,
urea (Refsum & Stromme 1974; Haralambie &
Berg 1976; Lemon & Mullin 1980; Dohm et al.
1982) and ammonia (Czarnowski & Gorski 1991;
Graham & MacLean 1992; Graham et al. 1995)
provide strong indirect evidence that significant
increases in branched-chain amino acid (BCAA)
metabolism occur with endurance exercise (Fig.
10.4). Further, this has been confirmed using
direct oxidation measures (Fig. 10.5) by a number
of independent investigations (White & Brooks
1981; Hagg et al. 1982; Lemon et al. 1982; Babij
et al. 1983; Meredith et al. 1989; Phillips et al.
1993). This is likely the result of an exercise intensity-dependent activation of the limiting enzyme
(branched-chain oxoacid dehydrogenase) in the
oxidation pathway of the BCAA (Kasperek &
Snider 1987). This response is apparently directly
proportional to BCAA availability (Knapik et al.
Fig. 10.3 Effect of prolonged
endurance exercise (10 h
swimming in rodents) on protein
concentration in the red portion of
the quadriceps muscle. Note the
decrease immediately following
the exercise bout. *, P < 0.05.
Adapted from Varrik et al. (1992).
Protein concentration (mg.100 g–1)
24
22
20
18
*
16
14
12
10
Sedentary
controls
0
2
6
Time after exercise (h)
24
48
138
nutrition and exercise
1991; Layman et al. 1994) and inversely proportional to glycogen availability (Lemon & Mullin
1980; Wagenmakers et al. 1991), although other
factors may also be important (Jackman et al.
1997). This suggests that dietary protein, dietary
carbohydrate, prior exercise and time since the
previous meal are probably all important determinants of BCAA oxidation during exercise.
The magnitude of this increased BCAA oxidation could be important relative to daily BCAA
requirements because a single bout of moderate
.
exercise (2 h at 55% Vo2max.) can produce an oxidation rate equivalent to almost 90% of the daily
requirement for at least one of the BCAA (Evans
et al. 1983). In addition, it is possible that this oxidation rate could be even higher in endurancetrained individuals because at least two studies
Branched-chain
amino acids
2-oxoglutarate
with rodents have shown that the endurance
training process results in further increases
in BCAA oxidation both at rest and during
endurance exercise (Dohm et al. 1977; Henderson
et al. 1985). With endurance exercise, this increase
is proportional to exercise intensity (Babij et al.
1983) but, despite the extremely intense nature of
strength exercise, BCAA oxidation appears to be
largely unaffected by this exercise stimulus (Fig.
10.6) (Tarnopolsky et al. 1991). This is likely due
to the fact that strength exercise is so intense that
a major portion of the necessary energy must be
derived via anaerobic metabolism, i.e. stored
phosphagens and muscle glycogen, rather than
via oxidative pathways.
Interesting data are also available from several
elegant nitrogen status (balance) experiments
Urea formation (liver)
GDH
BCAAAT
Alanine (released
from muscle)
Branched chain
oxoacids
Glutamate
GS
BCOADH
Whole-body leucine flux oxidized (%)
Oxidation (CO2)
AAT
Pyruvate
NH+4
Glutamine
(released from muscle)
Urea formation
(liver)
Fig. 10.4 Overview of branchedchain amino acid metabolism
showing the production of alanine
and glutamine in muscle, as well
as the formation of urea in the
liver. AAT, alanine amino
transferase; BCAAAT, branchedchain amino acid amino
transferase; BCOADH, branchedchain oxoacid dehydrogenase;
GDH, glutamate dehydrogense;
GS, glutamine synthetase; NH+4 ,
ammonium.
100
80
60
40
20
0
10
20
30
40
50
60
70
80
.
Exercise intensity (%VO2max)
90
100
Fig. 10.5 Effect of endurance
.
exercise intensity (Vo2max.) on the
oxidation of one of the branchedchain amino acids (leucine) in
four human subjects. Note the
linear increase in oxidation with
increasing exercise intensity. r =
0.93; y = 0.71x + 8.44. Adapted
from Babij et al. (1983).
effects of exercise on protein metabolism
suggesting that dietary protein needs are elevated with both endurance and strength exercise.
The data of Gontzea et al. (1974) suggest that
dietary protein needs are elevated with an
aerobic exercise programme (Fig. 10.7) but subsequent work by the same group (Gontzea et al.
1975) indicates that this might be true only
transiently during the first few weeks of
an endurance exercise programme (Fig. 10.8).
139
However, the data in this second investigation
may have been confounded by an exercise training effect because the exercise stimulus remained
constant over the 3-week period when nitrogen
status was assessed. In other words, the im.
proved endurance capacity (Vo2max.) likely experienced as the study progressed by these
previously untrained subjects would mean that
the same absolute exercise bout represented a
Fig. 10.6 Effect of a strenuous,
whole-body heavy resistance
exercise bout on oxidation of the
branched-chain amino acid
leucine in humans. Note that
despite the vigorous nature of the
training session, there is little
effect on leucine oxidation either
during the exercise or during 2 h of
recovery. Adapted from
Tarnopolsky et al. (1991).
Whole-body leucine oxidation
(µmol.kg–1.h–1)
120
100
80
60
40
Strength
exercise
Pre-exercise
Recovery
20
0
–50
0
50
100
Time (min)
150
200
Nitrogen balance (g.day–1)
4
2
0
–2
Sedentary
–4
2
4
Exercise
6
8
10
Sedentary
12
14
Time (days)
Fig. 10.7 Effect of an acute endurance exercise bout on nitrogen status (balance) while consuming differing protein
intake in humans. Note that the overall pattern of nitrogen status with exercise is similar with both protein intakes
and that with the lower protein intake (125% of the recommended dietary intake for protein) nitrogen status
becomes negative with the exercise programme, suggesting that this amount of dietary protein, while adequate for
the sedentary individual, is inadequate for exercise. 䊉, 1 g protein · kg–1 body mass · day–1; 䊐, 1.5 g protein · kg–1
body mass · day–1. Adapted from Gontzea et al. (1974).
140
nutrition and exercise
Nitrogen balance (g.day–1)
1
0
–1
–2
–3
–4
–2
0
2
4
6
8
10
Time (days)
12
14
16
18
20
Fig. 10.8 Effect of adaptation to an exercise programme on nitrogen status while consuming 1 g protein · kg–1 · day–1
(125% of the recommended protein intake) in humans. Note that nitrogen status (balance) appears to recover over
several weeks of the same exercise stimulus. These data have been interpreted to mean that this protein intake,
although inadequate for a few days at the beginning of an endurance exercise programme, becomes adequate over
a few weeks as a result of some adaptation. However, this apparent improved nitrogen status could also be an
artifact of a decreased exercise stimulus due to an increasing endurance capacity over the several weeks of training.
Adapted from Gontzea et al. (1975).
lower relative exercise intensity, and perhaps as a
result, an improved nitrogen status. To examine
this possibility, we decided to repeat the initial
investigation of Gontzea et al. (1974) with a
few minor but significant changes. First, we
studied experienced endurance runners (> 5
years’ training experience, 94 ± 21 km · week–1,
.
Vo2max. = 71 ± 5 ml · kg–1 · min–1) and, second, we
used an exercise bout which simulated their
daily training load. We observed a negative
nitrogen status in the trained runners when they
consumed 0.9 g protein · kg–1 · day–1 and a positive nitrogen status when they consumed 1.5 g ·
kg–1 · day–1 (Friedman & Lemon 1989). The fact
that these experienced endurance runners
responded similarly to the untrained subjects
who were unaccustomed to the exercise stimulus
in the Gontzea et al. (1974) study indicates that
the negative nitrogen status in the endurance
runners on the diet of 0.9 g protein · kg–1 · day–1
reflects an inadequate protein diet rather than a
transient response to the initiation of an exercise
programme.
In another study, Tarnopolosky et al. (1988),
using various protein intakes (1.0–2.7 g · kg–1 ·
day–1) and the nitrogen status (balance) technique, not only observed an increased protein
need in the endurance athletes studied, agreeing
with the other studies mentioned above, but also
in a group of strength athletes (see discussion
of strength studies below; Fig. 10.9). Typically,
regression procedures, i.e. protein intake that
elicits nitrogen balance plus a safety margin
(twice the standard deviation of the subject
sample) to cover the needs of 97.5% of the population of interest (US Food and Nutrition Board
1989), are used with these kinds of data to determine a recommended dietary allowance (RDA).
In this study the investigators used this procedure but utilized only 1 SD to arrive at recommended protein intakes of 1.6 g · kg–1 · day–1
for endurance athletes and 1.2 g · kg–1 · day–1 for
strength athletes (167% and 112% of the current
RDA in the United States, respectively). This
conservative approach was used because they
wanted to minimize any overestimation that
might result when extrapolating from protein
intakes as high as 2.7 g · kg–1 · day–1 to those
effects of exercise on protein metabolism
141
Fig. 10.9 Estimated dietary
requirements (protein intake
necessary to elicit nitrogen
balance) in endurance athletes
(䉬), strength athletes (䊐) and
sedentary men (䊉). Note that
both athlete groups have protein
requirements (y intercepts)
greater than those of their
sedentary counterparts. Adapted
from Tarnopolsky et al. (1988).
Protein intake (g.kg–1.day–1)
3.2
Runners
2.8
2.4
Body builders
2.0
1.6
1.2
0.8
0.4
0.0
Sedentary
–2
required for nitrogen balance. Finally, inclusion
of the sedentary group in this study is noteworthy because any methodological errors
would be similar across all three groups and
therefore the differences in protein intake necessary to elicit nitrogen balance (0.73, 0.82 and
1.37 g · kg–1 · day–1 for sedentary, strength athlete
and endurance athlete groups, respectively)
should reflect true differences in the dietary
protein need of these groups.
Shortly thereafter, Meredith et al. (1989) used
both the traditional nitrogen status (balance)
technique and protein turnover measures (oral
doses of 15N-glycine every 3 h for 60 h) to assess
dietary protein needs in young (26.8 ± 1.2 years)
and middle-aged (52.0 ± 1.9 years) endurancetrained men (> 11 years’ training). These nitrogen
status data indicate that protein needs were
elevated similarly in both age groups (by 37%)
relative to the data of a previously published
study on sedentary individuals from the same
laboratory. When these data were used to calculate a recommended dietary allowance for
protein based on regression procedures (as
described above; except here, twice the sample
SD was added because the protein intakes used
were near the requirement, i.e. 0.61, 0.91 and
1.21 g protein · kg–1 · day–1) the obtained value
was 1.26 g protein · kg–1 · day–1 (157% of the
current RDA in the United States). In addition,
0
2
4
6
8
10
12
14
16
18
20
Nitrogen balance (g.day–1)
further support for the advantage of the higher
protein intake was found in the protein turnover
data which showed that the protein synthetic
rate was higher in both age groups when 1.21 vs.
0.61 g protein · kg–1 · day–1 was consumed.
The subsequent data of Phillips et al. (1993),
who found a negative nitrogen status (balance)
in endurance runners (>5 years’ training experi.
ence, 43–50 km · week–1, Vo2max. = 66–68 ml · kg–1
fat free mass · min–1), adapted to a protein intake
of 0.8–0.94 g · kg–1 · day–1 provide further support
that protein needs are elevated in trained
endurance athletes. In addition, a greater negative nitrogen status (balance) in the male vs. the
female subjects was noted in this study and this
apparent gender difference in protein use was
confirmed by greater leucine oxidation rates (Fig.
10.10) in the men both at rest and during exercise
(Phillips et al. 1993). Apparently, this gender difference is related to reduced glycogen and/or
enhanced fat use in women, perhaps as a result of
differing hormonal responses (Tarnopolsky et al.
1995). These observations, if confirmed with subsequent work, provide another example where
data derived on male subjects may not be directly
applicable to women.
At least two groups (Lemon et al. 1992;
Tarnopolsky et al. 1992) have observed even
higher protein needs in strength athletes (Fig.
10.11) and based on nitrogen balance data have
142
nutrition and exercise
70
recommended intakes of 1.7 and 1.8 g protein ·
kg–1 · day–1, respectively. Moreover, Fern et al.
(1991) found a greater gain in mass over 4 weeks
of training in body builders who consumed 3.3
vs. 1.3 g protein · kg–1 · day–1. This study is fascinating because it supports the age-old (but
poorly documented) belief of strength athletes
that very large amounts of dietary protein (and
the resulting highly positive nitrogen balance)
in combination with the anabolic stimulus of
strength exercise may be able to stimulate muscle
growth (Lemon 1991). However, amino acid oxidation also increased by 150% in this study, suggesting that the optimum protein intake was
likely exceeded. Subsequently, Tarnopolsky et al.
(1992) observed an increase in whole-body
protein synthesis (Fig. 10.12) when athletes
participating in a strength training programme
increased their protein intake from 0.9 to
1.4 g · kg–1 · day–1. Interestingly, there was no
additional increase when they consumed a diet
Leucine oxidation (µmol.kg–1.g–1)
**
60
*
50
40
*
30
20
10
0
Exercise
Rest
Fig. 10.10 Effect of gender on oxidation of the amino
acid leucine both at rest and during an endurance
exercise bout in humans. Note that exercise increases
leucine oxidation (*, P < 0.01, exercise vs. rest) and that
both at rest and during exercise the leucine oxidation
rate is greater in the men (**, P < 0.01, men vs. women).
䊐 , men; , women. Adapted from Phillips et al.
(1993).
Protein intake (g.kg–1.day–1)
4
3
2
1
0
–10
–5
0
5
10
15
Nitrogen balance (g.day–1)
Fig. 10.11 Estimated dietary requirements (protein intake necessary to elicit nitrogen balance) in novice bodybuilding men. Note that while consuming 0.99 g protein · kg–1 body mass · day–1 (125% of the recommended dietary
intake for protein) (䊐), all subjects had a negative nitrogen status and a strong linear relationship between protein
intake and nitrogen status (r = 0.82, P < 0.01, y = 0.13x + 1.43). Using these data, the estimated dietary requirement for
protein ( y intercept) is 1.43 g protein · kg–1 · day–1. Typically, recommendations for protein are equal to this value (y
intercept) plus a safety buffer equal to 2 SD of the sample mean (in order to account for the variability in the
population relative to the sample studied). Here, the recommendation would be 1.63 g protein · kg–1 · day–1 (204% of
the current recommendation). The linear relationship between protein intake and nitrogen status is lost at the high
protein intake studied (2.62 g protein · kg–1 · day–1) (䊉) and the nitrogen status was highly positive indicating that
this intake exceeded protein need (r = 0.11; P < 0.05; y = – 0.93x + 2.76). For both treatments combined, r = 0.86;
P < 0.01; y = – 0.11x + 1.53. Adapted from Lemon et al. (1992).
effects of exercise on protein metabolism
containing 2.4 g protein · kg–1 · day–1. Further,
amino acid oxidation increased with the 1.4 and
2.4 g · kg–1 · day–1 diet in the sedentary group but
only with the 2.4 g · kg–1 · day–1 diet in the
strength athletes. This suggests that at an intake
of 1.4 g protein · kg–1 · day–1, the amino acids consumed in excess of needs were removed from the
body via oxidation in the sedentary subjects but
were used to support an enhanced protein synthesis rate in the strength group. Obviously with
time this should lead to increases in muscle
mass and potentially in strength. These results
confirm the Fern et al. (1991) data (that increased
dietary protein combined with strength exercise
enhances muscle growth over training alone)
and further indicate that 2.4 g protein · kg–1 · day–1
is excessive. These data and the nitrogen balance
data (Lemon et al. 1992; Tarnopolsky et al. 1992)
indicate that optimal protein intakes for male
strength athletes are likely about 1.4–1.8 g
protein · kg–1 · day–1 (175–225% of current recommendations). Finally, it should be understood
143
that these studies all involved men who were not
taking any anabolic substances. Although not
condoned due the potential adverse side-effects,
it is possible that the ceiling effect relative to
muscle growth observed in the vicinity of 1.4–
1.8 g protein · kg–1 · day–1 might be extended to
higher intakes if combined with pharmacologic
manipulations known to enhance muscle development (Bhasin et al. 1996). If so, this could
explain why the athletes’ beliefs about the benefits of very high protein diets differ from the
scientific data. Finally, these studies need to be
repeated in women to assess whether there are
gender differences in the protein needed to
enhance muscle growth.
Campbell et al. (1995) studied protein turnover
and nitrogen status (balance) in older men and
women (ages, 56–80 years) consuming either 1.62
or 0.8 g protein · kg–1 · day–1 while participating in
a 12-week, whole-body, heavy resistance training
programme. They observed a negative nitrogen
status and a tendency for whole-body protein
Whole-body protein (mg.kg–1.h–1)
300
250
b
b
200
a
150
a
a
a
100
50
0.9
1.4
2.4
Protein intake (g.kg–1.day–1)
Fig. 10.12 Whole-body protein synthesis in sedentary (䊐) vs. strength-trained ( ) men consuming 0.9, 1.4 or 2.4 g
protein · kg–1 · day–1 (112%, 175% and 300% of the current recommended protein intake). Note that the protein
synthetic rate increased in the strength-trained men when going from 112% to 175% of the current recommended
protein intake, indicating that this latter protein intake would facilitate mass and strength development. However,
there was no additional increase when protein intake was further increased to 300%, suggesting that this quantity
exceeded the optimal protein intake. Note also that strength training is necessary to increase the protein synthetic
rate with additional dietary protein, as no increase was observed in the sedentary men. Unlike letters, P < 0.05.
Adapted from Tarnopolsky et al. (1992).
144
nutrition and exercise
plus mineral mass to decrease (– 3.5%) on the
lower protein diet. In contrast, subjects (no
gender difference was apparent) on the higher
protein diet had a greater protein synthetic rate
and a tendency to increase whole-body protein
plus mineral mass (+ 1.9%). These data agree
with the findings in younger subjects (discussed
above) and further suggest that higher protein diets are beneficial for older individuals who
strength train. This is especially important
because as the benefits of strength training for
seniors become more apparent (Fiatarone et al.
1990; Fiatarone et al. 1994), the number of older
individuals adding this type of exercise training
to their fitness/wellness programmes is growing
significantly.
There is other supportive evidence for the suggestion that physically active individuals need
additional dietary protein (Consolazio et al. 1963,
1975; Celejowa & Homa 1970; Laritcheva et al.
1978; Marable et al. 1979; Dragan et al. 1985;
Meredith et al. 1992) and, taking these together
with the recent nitrogen balance and protein
turnover results, it is difficult to deny that protein
intakes in excess of the current recommendations
(0.8 g · kg–1 · day–1 in most countries) are beneficial for those who are physically active. It
appears that the optimal protein intake for
strength athletes may be as high as 1.7–1.8 g ·
kg–1 · day–1 and for endurance athletes slightly
less, perhaps 1.2–1.4 g protein · kg–1 · day–1.
However, as mentioned, these data have been
collected primarily on men. The limited data
available on female endurance athletes suggest
that dietary protein needs for women may be
somewhat less but this is not well documented.
Moreover, there are almost no data on female
body builders. Consequently, these nitrogen
balance and tracer studies need to be repeated
with female subjects to confirm the apparent
gender differences with endurance exercise and
to establish protein intake recommendations for
female strength athletes.
Currently, despite anecdotal claims to the
contrary, there is little good evidence that high
protein intakes (> 1.3–1.4 g protein · kg–1 · day–1)
actually enhance muscle performance (Dragan
et al. 1985; Brouns et al. 1989; Vukovich et al. 1992;
Fry et al. 1993). Moreover, we did not observe
an enhanced endurance running performance
with supplemental protein in rodents undergoing endurance training (Cortright et al. 1993) nor
could we document greater muscle strength or
mass gains in strength athletes with supplemental protein (2.6 g · kg–1 · day–1) despite improved
nitrogen status (Lemon et al. 1992). Further, our
studies with differing protein types (soy, casein,
whey) and strength training have not revealed
any obvious performance advantage of any
particular type of protein (Appicelli et al. 1995).
However, our studies have only investigated the
initial response (4–8 weeks) to training and it is
possible that over longer time periods an advantage could become apparent. Given the fantastic
claims and the obvious potential monetary benefits in the athletic arena, it is somewhat surprising that this area has received such little attention
among scientists.
Are these moderately high protein
recommendations healthy?
Many believe high protein diets are hazardous
but it is difficult to document an adverse effect
except in patients with impaired kidney function
(Brenner et al. 1982). Clearly, high dietary protein
increases the work of the kidneys because of the
additional nitrogen load that must be excreted,
but this does not seem to be a problem for
healthy individuals. In addition, serious adverse
effects have not been observed in rodents that
consumed extremely high protein diets (80% of
energy intake) for more than half their lifespan
(Zaragoza et al. 1987). These data are particularly
interesting not only because of their longitudinal
nature but also because this diet represents at
least three times the protein percentage observed
in the highest protein diets of athletes. Finally,
the absence of reports of kidney problems in
middle-aged weight lifters/body builders suggests that the dangers of high protein diets in
healthy individuals have probably been over-
effects of exercise on protein metabolism
estimated because many of these athletes have
consumed high protein diets regularly for 20–30
years or more.
Similarly, the association between high protein
diets and atherogenesis is likely overstated. For
example, it appears that the well-documented
positive relationship between animal protein
and plasma cholesterol observed in animals
doesn’t apply to humans (West & Beynen 1985)
and, as a result, the association between dietary
fat and blood fats is much weaker than once
thought (McNamara et al. 1987; Clifton & Nestel
1996). Furthermore, even if these relationships
are strong in sedentary individuals, the fate of
ingested fat may be substantially different
in physically active individuals (used as a fuel
rather than stored in blood vessel walls or
adipose tissue; Muoio et al. 1994; Leddy et al.
1997).
At one time it appeared that high protein diets
resulted in an obligatory loss of calcium in the
urine (Allen et al. 1979) and, if so, this could
be problematic, especially for women, because
of the potential to accelerate the development
of osteoporosis. However, this appears to be a
concern only with purified protein supplements
because the phosphate content of protein food
apparently negates this accelerated calcium loss
(Flynn 1985).
There are, however, at least two areas of
concern with high protein diets. First, the additional water excretion associated with the nitrogen loss via the kidneys could be detrimental
in physically active individuals (especially
endurance athletes) because of their already
increased fluid losses as sweat. The resulting
dehydration could adversely affect exercise performance (Armstrong et al. 1985) and, if severe
enough, even threaten health (Adolph 1947;
Bauman 1995). For this reason, it is critical that
rehydration be adequate in athletes who ingest
high protein diets. The best way to do this is by
regularly monitoring changes in body mass. Dramatic acute weight changes in athletes consuming high protein diets indicate that additional
rehydration is required. Second, the intake of
145
megadoses of individual amino acids (which has
only become possible in recent years with the
widespread commercial development of individual amino acid supplements) could potentially be detrimental. The ergogenic benefits of
these food supplements are promoted to athletes
very successfully because of the intense desire
of most athletes to excell. Although many of
the theoretical benefits sound convincing (especially to the non-scientist), few are documented,
despite considerable investigation (Brodan et al.
1974; Kasai et al. 1978; Isidori et al. 1981; Maughan
& Sadler 1983; Segura & Ventura 1988; Wessen
et al. 1988; Bucci et al. 1990; Blomstrand et al.
1991; Kreider et al. 1992, 1996; Fogelholm et al.
1993; Lambert et al. 1993; Newsholme & ParryBillings 1994; Bigard et al. 1996; Wagenmakers &
van Hall 1996; Suminski et al. 1997), and substantial potential complications exist (Harper et al.
1970; Benevenga & Steele 1984; Yokogoshi et al.
1987; Tenman & Hainline 1991). As a result,
it is recommended that these supplements be
avoided until such time as their safety as well as
their ergogenic benefits are proven.
Protein supplementation:
is it necessary?
Protein supplementation is probably not necessary for the vast majority of physically active
individuals because the amounts of protein
found to be necessary (1.2–1.8 g · kg–1 · day–1) can
be obtained in one’s diet assuming total energy
intake is adequate. For example, a sedentary
individual consuming about 10.5 MJ · day–1
(2500 kcal · day–1), of which 10% is protein, would
be consuming about 63 g protein daily. Assuming
a body mass of 70 kg, this would be about 0.9 g
protein · kg–1 · day–1 or about 112% of the current
protein RDA in most countries. Should this individual begin an exercise programme and, consequently, double his/her energy intake to 21 MJ
(5000 kcal) while maintaining 10% protein
intake, the resulting protein intake would also
double to 1.8 g · kg–1 · day–1. This would be sufficient to cover the increased needs of all the
146
nutrition and exercise
studies mentioned in this review. Moreover,
despite the emphasis on carbohydrate in the diet
of most athletes, maintaining 10% (2100 kJ or
500 kcal) of energy intake as protein should not
pose a problem because, if fat intake was
30% (6300 kJ or 1500 kcal), 12.6 MJ (3000 kcal)
would remain, enabling this hypothetical
athlete to consume about 750 g of carbohydrate
(10.7 g · kg–1). This quantity of carbohydrate is
certainly more than sufficient for any carbohydrate loading programme.
Inadequate protein intake in active individuals
is most likely to occur in those who have other
pre-existing conditions that interact with the
exercise effect to increase the quantity of dietary
protein required — for example, during periods
of rapid growth, e.g. in adolescents, children,
women who are pregnant, etc.; in situations
where total energy intake is inadequate, e.g.
dieters, those in body mass-restricted activities,
etc.; or in those who do not consume a diet from a
wide variety of food sources, e.g. many adolescents, vegetarians, women, seniors, etc. For some
athletes, insufficient energy intake occurs (and
therefore perhaps protein, as well) because of the
sheer bulk of food and fluids required to maintain energy and fluid balance. In such situations,
the use of a liquid meal replacement formula
may be advantageous.
If dietary inadequacies are suspected it is best
to complete a diet analysis (typically a 3–7-day
food record is analysed with commercially available software) in order to verify that there is
in fact a problem. Unfortunately, in free living
humans these analyses can be grossly inadequate
not only because the subjects are sometimes
given poor instructions but also because some
subjects modify their diet in an attempt to please
the investigator. In addition, use of inadequate
methods to accurately quantify serving size is a
common problem (weigh scales must be used),
as is simply forgetting to record all food consumed. Finally, 3 days may not be representative
of one’s true diet especially if weekends are
excluded (food intake may differ substantially
between week and weekend days) and 7-day
records are not always better because less-
motivated subjects can become bored with
the process and, consequently, fail to report accurately. For all these reasons, extreme care must
be used in the interpretation of this kind of
information.
Assuming that care has been taken to obtain an
accurate representation of an individual’s diet
and an insufficient protein intake is found, one
can usually correct the problem with a few minor
adjustments in the individual’s food selections.
This means that, despite the fact that regular
participation in an exercise programme (either
strength or endurance) will apparently increase
protein requirements, special protein supplements (which are considerably more expensive
than food protein per kilogram of protein mass)
are rarely necessary. Further, if it is determined
that it is not possible to consume sufficient
protein in food and a decision is made to use
a supplement, one of the best and most costeffective approaches would be to fortify one’s
food with a high-quality, low-cost protein such as
skim milk powder. Finally, there is even less
support for the commonly used practice of
individual amino acid supplementation. Until
such time as it is clear that one or a few individual amino acids in high dosages are both beneficial and safe, this latter strategy is definitely
contraindicated.
Conclusion
After reviewing the literature, it is possible to
make a case that protein needs are elevated
in physically active individuals, apparently to a
greater extent with those actively engaged in
regular strength exercise than with endurance
exercise. The limited available information suggests that the exercise effect on protein needs
may be greater in men than in women. In addition, the increased protein need is likely greatest
in situations where other factors compound the
exercise effect. However, there is still considerable debate regarding the magnitude of this exercise effect on protein requirements. This debate
centres on a variety of methodological concerns
which compromise a significant amount of the
effects of exercise on protein metabolism
experimental data that have been collected. As a
result, it is likely that a definite answer to the
question of the optimal quantities of protein necessary for athletes must await the arrival of
more definitive measures to assess protein
requirements. Until that time, it appears that the
increased protein needs (perhaps 50–125% of
the current recommended intakes in many countries) can be met via appropriate food selections
without consuming expensive protein supplements. Finally, few data exist to support the fantastic performance effects frequently attributed
to extremely high protein diets and this is an area
that needs much more attention.
Acknowledgements
The ongoing support of the author’s laboratory
by the Joe Weider Foundation is gratefully
acknowledged.
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