Relationship of glomerular filtration rate and serum CK activity after resistance exercise in women
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Transcript of Relationship of glomerular filtration rate and serum CK activity after resistance exercise in women
NEPHROLOGY – ORIGINAL PAPER
Relationship of glomerular filtration rate and serum CKactivity after resistance exercise in women
Marco Machado • Elida N. Zini •
Samara D. Valadao • Mayra Z. Amorim •
Tiago Z. Barroso • Wilkes de Oliveira
Received: 11 January 2011 / Accepted: 30 March 2011 / Published online: 20 April 2011
� Springer Science+Business Media, B.V. 2011
Abstract The aim of study was to assess the corre-
lation between the changes in serum CK activity after a
resistance exercise and renal function measured by
glomerular filtration rate (eGFR). Twenty-nine trained
women (32 ± 10 years; 157 ± 4 cm; 58.8 ± 6.4 kg)
performed a resistance exercise session with 17
exercises with 3 9 12 repetitions in a circuit training
fashion. Subjects provided blood samples prior to
exercise session (PRE), and at 24, 48, and 72 h
following exercise session for creatine kinase (CK)
and creatinine. 24-Urine samples were collected before
and 72 h after exercises. eGFR was obtained by the
three most recommended methods (MDRD; MCQE;
Cockcroft-Gault). After the exercise session, serum
CK activity increase up 1.68 times (P \ 0.01). Serum
creatinine increased 25.5% (P = 0.0000) while uri-
nary creatinine decreased on average 6.4% (P =
0.0422). eGFR decreased in all formulas: MDRD by
21.5%, MCQE by 14.2%, and C-G by 17% (all with
P \ 0.01). Ccr also decreased (-22.9%, P \ 0.01).
The index of correlation was significant for MDRD
(r = -0.924; P \ 0.01), C-G (r = -0.884; P \0.01), and MQCE (r = -0.644; P \ 0.05). In conclu-
sion, we observed a significant negative correlation
between CK activity and the eGFR indices of renal
function.
Keywords Skeletal muscle micro-trauma �Muscular stress � Biochemical markers � Kidney �Creatinine
Introduction
Strenuous, overexertion exercise can result in muscle
damage evidenced by delayed-onset muscle soreness,
strength loss, weakness, tenderness, and increased
blood levels of muscle proteins such as creatine kinase
(CK), lactate dehydrogenase (LDH), and myoglobin
(Mb) [1, 2]. Exertional Rhabdomyolysis (ERB) is a
clinical condition where excessive muscle damage can
lead to renal failure [2]. Although CK and other
intramuscular proteins (LDH, aspartate aminotrans-
ferase, alanine aminotransferase) are cleared from the
blood by the reticuloendothelial system, myoglobin is
cleared by the kidneys. High blood myoglobin levels
can ‘‘spill over’’ into the urine, resulting in myoglo-
binuria and can also precipitate in the kidney tubules
potentially resulting in acute renal failure especially in
environmental conditions of heat stress and dehydra-
tion [1–3].
M. Machado
Department of Physical Education, Universitary
Foundation of Itaperuna, Itaperuna, Brazil
M. Machado (&) � E. N. Zini � S. D. Valadao �M. Z. Amorim � T. Z. Barroso � W. de Oliveira
Laboratory of Physiology and Biokinetic, Faculty of
Biological Sciences and Health, UNIG – Campus V,
BR 356 - Km 02, Itaperuna, RJ 28.300-000, Brazil
e-mail: [email protected]
123
Int Urol Nephrol (2012) 44:515–521
DOI 10.1007/s11255-011-9963-4
Serum creatine kinase (CK) activity has been
studied extensively and is considered a qualitative
marker for skeletal muscle micro-trauma [4–8].
Clarkson et al. [9] found in 203 subjects a strong
correlation (r = 0.80) between serum CK activity
and serum myoglobin concentration after an eccentric
(lengthening contractions) exercise session, and their
findings indicate no compromise in renal function.
Renal function was assessed by measuring serum
creatinine, blood urea nitrogen, potassium, osmolal-
ity, phosphorus, and uric acid. Even in a subject
who had very high levels of CK (80,550 U/l) and
myoglobin (2300 lg/l) in the blood, there was no
evidence of compromised renal function. The Clark-
son et al. [9] study did not assess glomerular filtration
rate (GFR).
GFR is considered the best overall index of kidney
function, and it is recommended for diagnosis and
monitoring of kidney disease. This rate can be obtained
through estimation by various formulas (estimated
GFR, eGFR) or through the creatinine clearance (Ccr),
but Ccr does not improve the estimate of GFR over
that provided by prediction equations [10–12]. The
decrease of GFR is important because in a clinical
setting its value is used to define possible kidney
damage. A decrease of*50% in GFR (\60 ml min-1)
is considered evidence of kidney compromise as in
cases of rhabdomyolysis, and a decrease of 75% is
indicative of renal impairment [11].
GFR may be a more sensitive indicator of potential
renal problems after strenuous exercise that results in
large increase in CK and myoglobin in the circulation.
We hypothesized that there would be a significant
correlation between CK and GFR whereby high
post-exercise CK activity is associated with greater
decreases in GFR, thus establishing GFR as a potential
indicator of renal compromise. Thus, the aim of this
study was to assess the correlation between the change
in serum CK activity after a workout and renal function
measured by glomerular filtration rate.
Materials and methods
Subjects
Twenty-nine trained women (32 ± 10 years old;
157 ± 4 cm; 58.8 ± 6.4 kg) volunteered to partici-
pate in the current study (convenience sample). All
subjects were healthy (no muscle, cardiovascular, joint
problems) and were not using ergogenic substances or
any other drugs. Subjects underwent a physical exam-
ination by a physician and were further screened for
any medications that might affect muscle damage or
renal function. Subjects were excluded if muscle
disease, diabetes mellitus, hypertension, or hyperthy-
roidism were known. All subjects had been participat-
ing in a structured training program (in the same fitness
classes) for a minimum of 12 months with a mean
frequency of three sessions per week. We tested trained
subjects because we wanted to simulate a ‘‘real life’’
situation when trained individuals perform unaccus-
tomed strenuous exercise. There are many cases in
the literature of trained women experiencing exer-
cise-induced rhabdomyolysis [1, 13]. The purpose
and procedures were explained to the subjects and
informed consent was obtained according to the
Declaration of Helsinki and in accordance with the
norms of the local Research Committee.
Experimental protocol
All subjects performed a 60 min resistance exercise
session with 17 exercises (Leg Press 45; Glute
Kickback on Swiss Ball; Bench Press; One-legged
Cable Kickback; Lunges; Cable Let pull down; Push
Ups; Leg Curl; Fly; Pec Deck Fly; Pull over; Lever
Seated Hip Abduction; Straight Led Deadlift; Cable
Lateral Raise; Standing Calf Raise; Seated Calf Raise;
Seated Biceps curl). Standard exercise techniques were
followed for each exercise [14]. All exercises were
performed with 3 sets with 12 repetitions with personal
choice load in a circuit training fashion (with minimum
rest intervals, less than 15 s). Each set was composed
of 12 complete movements (repetitions) of each
exercise; an exercise ‘‘circuit’’ is one completion of
all prescribed exercises in the program. When one
circuit is complete, one begins the first exercise again
for another circuit (3 circuits in total). The exercises
used in this session were used in the structured training
program but were never used with such short rest
intervals. The short intervals were used to increase the
magnitude of muscular stress [15]. A Borg-CR10 scale
as described by Borg [16] was used to check the effort
made by volunteers at the end of each set. The
environmental conditions were verified (25 ± 1�C and
70 ± 0% relative air humidity). The volunteers did not
516 Int Urol Nephrol (2012) 44:515–521
123
perform exercises for 96 h after the experimental
session.
Muscle soreness
The level of muscle soreness was assessed using
a visual analog scale consisting of a 100-mm line
representing ‘‘no pain’’ at one end (0 mm), and ‘‘very,
very painful’’ at the other (100 mm). The subjects were
asked to indicate the level of quadriceps muscle pain
along the line. The same investigator assessed the
muscle soreness over time for all subjects.
Blood collection and analysis
Subjects provided blood samples in a seated position
from the antecubital vein into plain evacuated tubes
after 8 h overnight fast prior to exercise session (PRE),
and at 24, 48, and 72 h following exercise session.
Immediately following collection, blood samples were
centrifuged at 16009g for 10 min. The serum was
removed and CK activity was analyzed with an
enzymatic method at 37�C (CK-UV NAC-optimized;
Biodiagnostica, Brazil) in a Cobas Mira Plus analyzer
(Roche - Germany). Serum creatinine was measured
with colorimetric assay (Biodiagnostica, Brazil). The
CK and creatinine analyses were made in triplicate (we
used the first value) and demonstrated high reliability
(intraclass R = 0.89 and 0.85, respectively). The
imprecision of creatinine and CK was\3%.
Urine collection and analysis
Before the exercise session, a 24 h urine sample was
collected in 1000-ml purpose-bottles. Bottles were
kept cold during the collection period. Immediately
after the return of the bottles, 50 ml of each whole urine
sample were collected and stored at -70�C before
analysis for creatinine and uric acid. The same
procedure (urine sample collection) was made 72 h
after first collection, whereas urinary creatinine and
uric acid were determined by a validated automated
colorimetric assay on a diagnostic autoanalyzer (Cobas
Mira Plus analyzer, Roche - Germany).
Estimated Glomerular Filtration Rate (eGFR) was
obtained by the three most recommended methods
[17]: (1) Modification of Diet in Renal Disease
(MDRD) Study, (2) Mayo Clinic Quadratic Equation
(MCQE), and (3) the Cockcroft-Gault (C-G) equation
[18]. The equation for the MDRD is [eGFR = 186.3 9
(serum creatinine-1.154) 9 (age-0.203) 9 1.212 (if
black) 9 0.742 (if female)]. MCQE formulae is
[eGFR = exp {1.911 ? (5.249/Serum Creatinine) -
(2.114/Serum Creatinine2) - 0.00686 9 age-0.205
(if female)}]. The C-G equation is [eGFR =
(140–age) 9 weight (kg)/(72 9 serum creatinine) 9
(0.85 if female)].
Creatinine clearance (Ccr) was calculated from the
concentrations of creatinine and the volume (con-
verted to ml/min) of the 24-h urine collection. We use
the formulae Ccr = (UCr 9 V)/SCr, where UCr is
urinary creatinine, V is total urine volume, and SCr is
serum creatinine.
Statistical analyses
Subjects were separated in two groups based on
serum CK activity responses: Normal Responders
(NR) and High Responders (HR). The difference
between baseline CK and peak CK (at 48 or 72 h), or
Delta CK, was considered the outcome measure.
A HR was defined as having a delta CK greater than
the 90th percentile (i.e., CK [757.9 U l-1) as
proposed by Heled et al. [19].
To analyze the relationship between exercise-
induced serum CK variations on the one hand and
eGFR and Ccr on the other, a regression analysis was
applied using the hyperbolic decay [y = y0 ? (ab/
b ? y)]. To compare serum CK activity and muscle
soreness over time, a 2 (groups) 9 4 (times) repeated
ANOVA was utilized. Significant main effects were
further analyzed using pairwise comparisons with a
Tukey’s post hoc test. Pre versus post blood and
urinary creatinine, eGFR, and Ccr were compared
with a Student’s t test. The alpha level was set at less
than 0.05 for a difference to be considered significant.
Statistical analysis was completed using SPSS� 17.0
for Windows (LEAD Technologies).
Results
After the exercise session, serum CK activity
increased 1.68, 4.87, and 5.48 times (at 24, 48 and
72 h, respectively) (P \ 0.05). There was no signif-
icant difference between the measurements obtained
at 48 and 72 h (P [ 0.05). Three individuals were
Int Urol Nephrol (2012) 44:515–521 517
123
classified as HR (Delta CK[757.9 U l-1). The deltas
CK for the three High Responders were 4377, 2025,
and 1062 U l-1 (Fig. 1).
The perceived exertion was 6.1 ± 0.8, 6.8 ± 0.8,
and 7.5 ± 0.7 after the first, second, and third set,
respectively (with a significant increase, P \ 0.01).
Muscle soreness significantly increased at 24, 48, and
72 h after the exercise session (P \ 0.05). There was
no significant difference between the measurements
obtained at 24 and 48 h (P [ 0.05). The perception of
muscle soreness decreased at 72 h after the exercise
session compared with 24 h (P \ 0.01) (Fig. 2).
Indices of renal function changed after the exercise.
Serum creatinine 72 h after exercise session increased
25.5% (P \ 0.01) while urinary creatinine decreased
on average 6.4% (P \ 0.04). eGFR decreased in all
formulas: MDRD by 21.5% (P \ 0.01), MCQE by
14.2% (P \ 0.01), and C-G by 17% (P \ 0.01). Ccr
also decreased by -22.9%, (P \ 0.01). There was no
statistically significant difference between renal func-
tion assessments (P [ 0.05) (Fig. 3).
Figure 4 shows the relationship of delta eGFR and
delta serum CK in NR (n = 26). The correlation was
significant for MDRD (r = -0.924; P \ 0.01), C-G
(r = -0.884; P \ 0.01), Ccr (r = -0.771; P \ 0.01),
and MQCE (r = -0.644; P \ 0.05).
Figure 5 shows the comparison of eGFR and Ccr
between NR and HR subjects. For all estimates of
GFR, there was a greater decrease in HR group when
compared with NR group (P \ 0.05).
Discussion
During heavy physical exercise, two phenomena are
concomitant: the decrease of GFR and the release
into the blood of some molecules from muscles. The
acute decrease of GFR is linked to the reduction of
renal blood flow and has been described in marathon
runners and cyclists [17]. The increase of molecules
as CK and myoglobin in the blood is linked to
muscular damage from increased permeability of or
damage to cellular membranes. The muscular-derived
Fig. 1 Serum CK activity (mean ± SD) PRE and 24, 48, 72 h
following the resistance exercise session. a Significantly higher
than PRE (P \ 0.01); b Significantly higher than 24 h
(P \ 0.01); *differences between groups (P \ 0.05). NR is
Normal Responders (N = 26) and HR is High responders
(N = 3)
Fig. 2 Muscle soreness (mean ± SD) PRE and 24, 48, 72 h
following the resistance exercise session. a Significantly higher
than PRE (P \ 0.01); b Significantly less than 24 h (P \ 0.01).
NR is Normal Responders (N = 26) and HR is High responders
(N = 3)
Fig. 3 Percentage change in indices of renal function
(mean ± SD) 72 h post exercise session. *Significant differ-
ence 72 h post vs. baseline (P \ 0.01). SCrn Serum creatinine;
UCrn Urine Creatinine; UAA Urinary Uric Acid; eGFR(MDRD) estimated Glomerular Filtration Rate MDRD; eGFR(MDRD) estimated Glomerular Filtration Rate MCQE; eGFR(C-G) estimated Glomerular Filtration Rate Cockcroft-Gault;
Ccr Creatinine Clearance
518 Int Urol Nephrol (2012) 44:515–521
123
molecules are usually cleared from blood by the
reticulo-endothelial system, except for myoglobin that
is cleared by the kidneys. Myoglobin is usually filtered
and excreted in urine, but renal function could be
impaired when myoglobin becomes concentrated in
the kidney tubules. Blood CK activity is commonly used
for evaluating recovery from exertion in athletes;
chronically elevated CK could indicate overtraining
and/or muscular trauma. A ten-fold increase of CK is
common in athletes after exercise, even professional
athletes [20–22]. However, extremely high levels of CK
(usually [10,000 U/l) may indicate rhabdomyolysis,
which could be accompanied by renal impairment.
The main finding of this study was the significant
correlations between serum CK activity and the eGFR
indexes of renal function. Previous studies have shown
that major increases in CK activity are associated with
altered renal function by action of myoglobin, which
increases similarly to CK in the blood [1, 9]. Clarkson
and colleges [9] reported a strong correlation between
the increases of CK and Myoglobin after 2 sets of 12
Fig. 4 The relationship between estimated Glomerular Filtration Rate (eGFR) and serum CK activity for NR (n = 26). a MDRD;
b MCQE; c C-G; d Ccr
Fig. 5 Comparison of delta eGFR between HR with NR.
a Significant difference between HR vs. NR (P \ 0.01);
b Significant difference between HR vs. NR (P \ 0.05)
Int Urol Nephrol (2012) 44:515–521 519
123
repetitions unilateral eccentric elbow flexion exercise
(biceps bracchi lengthening contraction). However,
despite the dramatic increases in CK and Myoglobin
(up to 80,550 U/l and 2300 lg/l, respectively), these
increases were not accompanied by serum creatinine
elevation. In this study, the concentration of creatinine
in urine decreased slightly (*6%), but serum creati-
nine significantly increased (*25%). When we ana-
lyze the Ccr and eGFR, calculated using the serum
creatinine, we found a significant reduction in these
variables. According to the ‘‘Clinical Practice Guide-
lines for Chronic Kidney Disease’’ [11], eGFR is a
more sensitive indicator of the filtration capacity of the
kidneys and is a strong predictor of the time to onset of
kidney failure as well as the risk of complications of
chronic kidney disease. There was a reduction in
eGFR’s calculated by all the equations but no decrease
below normal population values [11]. The reduction in
the values of eGFR occurred because of a greater
baseline eGFR found in trained individuals, as
described in Lippi et al. [18]. Thus, the values post-
exercise were still normal and the decrease was only
14.4–21.5%. Although this decrease does not indicate a
compromise in renal function, it may become clinically
significant if this type of activity is performed in a hot,
humid environment and a person is dehydrated [1–3].
An essential difference between the current study
and that of Clarkson et al. [9] is the exercises performed
and the methodology used. Clarkson et al. [9] had
subjects exercise a single muscle group (elbow flex-
ors), while the current study used various exercises
with multiple joints. Our measurements were per-
formed 24–72 h after exercise session, which is shorter
than those used by Clarkson et al. (4, 7 and 10 days).
Another factor that must be taken into consideration is
the influence of body temperature by the proposed
exercises; the exercises in our study involved many
muscle groups that likely could increase body temper-
ature more than exercise of a single muscle group as
performed in the Clarkson et al. study [9]. The high
body temperature plus the increase in myoglobin may
impair renal function and result in increased creatinine
in the blood and decreased eGFR.
The use of equations for eGFR has been recom-
mended [10, 11]. The CG equation proposed some
years ago has been substituted by the MDRD equation
[10, 23]. The MDRD equation could be of particular
value in sports medicine because it is not influenced by
body mass. There are few reports of eGFR by an
equation in athletes. The results of these studies
indicate that the most widely used creatinine-based
formulas yield significant variations in the eGFR in a
population of athletes during training regimens [18,
23]. In this context Milic et al. [23] suggest that the CG
equation might have been more suitable than the
MDRD because this equation appears more robust
against variations in training regimen.
This study shows data obtained exclusively from
women, unlike the studies of Banfi et al. [17] and
Lippi et al. [18] that were conducted with men and
women. It is well described in the literature that
women have a lower serum CK activity compared to
men [8]. Thus, the relationship observed in the
current study may only hold true for women.
Moreover, Springer and Clarkson [13] reported on
two women, both well educated and experienced in
fitness as our voluntaries, who were encouraged by
exercise leaders in a local health club to overexertion
during their exercise routine leading to ERB. Their
findings show the clinical relevance of this study in
the development and prescription of exercise for
women, that they are physically well conditioned (as
in this study and the study above).
Our findings display a strong correlation between
CK increase and decrease eGFR. Moreover, the three
individuals classified as HR showed significantly
larger changes in renal function. CK is cleared from
the blood by the reticuloendothelial system, but
myoglobin is cleared by the kidneys, and it is toxic to
glomeruli. We can assume that Mb increased pro-
portionately to CK based on previous findings of a
significant correlation of serum CK and Mb after
exercise damage [9].
A recent study [15] showed that some individuals
with greater exercise-induced serum CK activity may
have their condition worsened by shorter rest inter-
vals between sets and exercises. This study used a
minimum interval between exercises and demon-
strated that CK HR was associated with a reduction in
renal function (Fig. 5). The rise in CK activity was
less than that proposed for a diagnosis of rhabdomy-
olysis. However, this type of exercise with short rest
intervals may pose a risk of impaired renal function
particularly in HR. The perception of muscle pain
was not significantly different between NR and HR,
this finding shows that despite the great difference in
CK concentration, there seems to be no difference in
the magnitude of muscle damage.
520 Int Urol Nephrol (2012) 44:515–521
123
The mechanisms to explain a higher response for
some subjects is unknown [19]. The data from this
study show that muscle pain does not differ greatly
between HR and NR, which suggests that the greater
release of enzymes is not linked to mechanisms that
explain pain. CK activity in the blood is a net result of
release of CK by the muscle and clearance of CK by the
reticuloendothelial system. Clarkson et al. [24] postu-
lated that subjects may have different clearance veloc-
ities. This may explain why pain is not related to the
increase in CK activity in the blood after exercise.
Our data clearly show a relationship between CK
elevation after physical exercise and reduced eGFR.
Moreover, subjects who were HR demonstrated even
lower eGFR values. A limitation of this study is the
lack of using a more specific marker of glomerular
filtration rate as NGAL [25], therefore, further studies
are needed to confirm the hypothesis that a strenuous
exercise session can bring acute reduction of GFR.
Acknowledgments For Priscilla Clarkson for helpful comments
on the manuscript. For Felipe Sampaio-Jorge for your help in
statistics.
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