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: marcomachado1@gmail.com

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

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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

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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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