Nephrol Dial Transplant ( 1997) 12: 128–132
Nephrology
Dialysis
Transplantation
Original Article
Muscular strength and bone mineral density in haemodialysis patients
A. Spindler1, S. Paz1, A. Berman1, E. Lucero1, N. Contino2, A. Peñalba2, S. Tirado2, M. Santana3 and
A. Correa Zeballos3
1Centro de Estudios de Osteoporosis and Facultad de Medicina, Universidad Nacional de Tucumán; 2Centro de Riñón y
Diálisis, Tucumán; 3Section of Statistic, Facultad de Medicina, Universidad Nacional de Tucumán, Argentina
Abstract
Purpose. The objective of this study was to determine
the relationship between muscular strength and bone
mineral density ( BMD) in patients undergoing regular
haemodialysis.
Methods. The BMD was measured in the lumbar spine
( L –L ) and in the proximal femur (femoral neck and
2 4
trochanter) with dual-energy X-ray absorptiometry
DEXA (Lunar DPX ). Muscular strength of the
extensors, flexors and abductors muscles of the femur
( proximal muscles) and the extensors muscles of the
back was measured with an isometric dynamometer.
Thirty patients, 15 women with a mean age of 33.7
years ( 18–43 ) and 15 men with a mean age of 45.5
years (18–65) were included in the study.
Results. There was a positive and significant correlation between the BMD of the femoral neck and muscular strength of the flexors (r=0.490, P<0.005), the
extensors (r=0.658, P<0.01) and the abductors
muscles of the femur (r=0.671, P<0.0008), as well as
between the muscular strength of the flexors (r=0.413,
P<0.02) and extensors muscles of the femur (r=0.433,
P<0.01) with BMD of the trochanter. There was no
correlation between the muscular strength of the back
extensor muscles and the BMD of the lumbar spine
(r=−0.119, P NS). There was no correlation between
the BMD and the number of years of haemodialysis
therapy (r=−0.032, P NS), the patient’s age (r=
−159, P NS ), or the value of serum PTH (r=0.369,
P NS) respectively. However, there was a significant
correlation between the BMD of the femoral neck with
muscular strength (r=0.602, P<0.05).
Conclusion. This study reveals the close relationship
that exists between muscular strength of the proximal
muscles and the BMD of proximal femur in patients
undergoing haemodialysis.
Key words: bone mineral density; haemodialysis; muscular strength
Correspondence and offprint requests to: Dr A. Spindler, Centro de
Estudios de Osteoporosis, Córdoba 172, 4000, Tucumán, Argentina
Introduction
Patients undergoing haemodialysis present various
musculoskeletal complications, including renal osteodystrophy. Renal osteodystrophy is primarily characterized by a decreased synthesis of 1–25 (OH )
2
Vitamin D, hypersecretion of PTH, a reduced absorption of calcium, hyperphosphataemia, and an increase
in aluminium deposition in bone [1–6 ]. It was demonstrated that patients with renal osteodystrophy suffer
from bone demineralization [7]. In healthy persons,
main determinants of bone mass are race, sex, heredity,
hormonal status, nutrition, and physical activity. Of
these, genetic factors play a major part, accounting for
60% of the variance [8]. Forty percent of the variance
may be due to environmental factors such as nutrition
and physical activity, which is important because these
factors can be easily controlled. It has been demonstrated that physical exercise stimulates osteoblastic
activity [9–13]. Conversely, a sedentary life and a lack
of pressure forces diminishes muscular strength and
bone mass, causing an imbalance between formation
and resorption [14]. The importance of physical activity in maintaining adult bone mass is widely recognized
[8,15]. However, the effect of physical activity on
patients on dialysis has not received attention. To our
knowledge, there are no publications regarding the
effects of physical activity or muscular strength on the
bones of patients undergoing haemodialysis. The goal
of this study is to investigate the relationship between
muscular strength and bone mineral density in patients
undergoing regular haemodialysis.
Subjects and methods
Thirty haemodialysis patients, including 15 women with a
mean age of 33.7 years (18–43 ) receiving haemodialysis for
a mean time of 39.8 months (12–98), and 15 men with a
mean age of 45.5 years ( 18–65) on haemodialysis for 43.7
months ( 12–108) were the subjects. The renal diseases
responsible for renal failure were hypertensive nephropathy
(11 patients), glomerulonephritis ( 6 patients), chronic pyelonephritis (5 patients), polycystic kidney ( 1 patient), amyloidosis (1 patient), and unknown cause (6 patients)
( Table 1 ). Exclusion criteria were ingestion of drugs or
© 1997 European Renal Association–European Dialysis and Transplant Association
Muscular strength and bone mineral density in HD patients
Table 1. Demographic data (n=30)
Sex
Age
(xÅ years)
Haemodialysis Renal failure aetiologies
(xÅ months)
Hypertensive nephropathy 11
Glomerulonephritis
6
Chronic pyelonephritis
5
M 15 45.5 (18–65) 43.7 ( 12–108) Polycystic kidneys
1
Amyloidosis
1
Unknown cause
6
F 15 33.7 (18–43) 39.8 ( 12–98)
conditions which might affect the skeleton (corticosteroids,
anticonvulsants, fluoride, lithium, immunosuppression treatment, or rheumatic, endocrine, liver, and gastrointestinal
disease). Patients were dialysed for 4 h, three times a week.
Water for haemodialysis was treated by reverse osmosis.
Heparin doses were between 5000 and 10 000 U per patient.
The prescribed diet included sodium and potassium restriction and protein intake limited to a range of 1–1.5 g/kg per
day. Serum phosphataemia was controlled by diet and calcium carbonate as phosphate binder. The patients received
calcium carbonate 4 g/day, folic acid 7500 mg/day, and
ferrum 330 mg/day. Fifty percent of the patients required
erythropoietin. The calcitriol dose was regulated according
to the post-dialysis PTH level (1–3 mg). Blood haemoglobin,
calcium, and bicarbonate concentrations, plasma concentrations of albumin, urea, creatinine, phosphorus, and basal
aluminium, serum concentration of ferritin, and plasma
alkaline phosphatase were measured using standard
techniques.
Serum intact parathyroid hormone ( PTH ) levels were
measured by radioimmunoassays. Moreover Kt/V urea was
calculated [16 ]. Bone mineral density (BMD) was measured
using dual-energy X-ray absorptiometry DEXA (Lunar
DPX, Madison, WI ) at the lumbar spine (L –L ) and right
2 4
proximal femur (femoral neck and trochanter). All scanning
and analyses were made by the same operator with a
coefficient of variation of 1.5% at both the lumbar spine and
femoral neck. The results were compared with those found
in reference populations. Previous studies showed that the
BMD of our healthy population in Argentina and United
States were similar [15,17,18]. The isometric strength of the
back extensor muscles and femoral extensors, flexors, and
abductors muscles was measured with a strain-gauge
dynamometer, which converted the force into digital readout
in kilograms by electronic amplifier. The reproducibility of
measurements performed on 3 separate days by the same
technician was assessed in normal volunteers. The coefficient
of variation was 6.9%. The muscular strength values were
not statistically related with age or sex. The muscle strength
was evaluated during the interval between dialysis sessions.
129
trochanter was xÅ =1.182 g/cm2, SD=0.235, xÅ =
0.929 g/cm2, SD=0.185, and xÅ =0.843 g/cm2, SD=
0.211 respectively. The BMD of the normal population
was higher, but the difference was not statistically
significant. There was greater muscular strength in the
normal population compared with the haemodialysis
patients: back extensors, xÅ =15.909 kg, SD=4.2 vs xÅ =
10.678 kg SD=5.2, P<0.01; abductors, xÅ =23.562 kg,
SD=3.2 vs xÅ =19.565 kg, SD=6.8, P<0.02; extensors
of the femur, xÅ =23.2 kg, SD=4 vs xÅ =17.800 kg, SD=
6.7, P<0.06; flexors, xÅ =20.132 kg, SD 3.8 vs xÅ =
19.637 kg, SD=6.6, p NS. The PTH value was xÅ =
522 pg/ml, SD=454. The Spearman coefficient correlation showed that there exists a positive and significant
correlation between the BMD of the femoral neck and
the muscle strength of the flexors (r=0.490, P<0.005),
Table 2, Figure 1, the extensors (r=0.658, P<0.01),
Figure 2, and the abductors (r=0.671, P<0.0008),
Figure 3, as well as between the muscle strength of the
flexors (r=0.413, P<0.02) and the extensors (r=0.433,
P<0.01) with BMD of the trochanter. There was no
correlation between the back extensors muscles and
the BMD of the lumbar spine (r=−0.119, P=NS ).
The correlation of BMD with muscle strength is similar
between the sexes. In females, a positive and significant
correlation exists between flexor muscular strength (r=
0.736, P<0.01), abductors (r=0.760, P<0.05), and
extensors (r=0.704, P<0.01) with BMD of femoral
neck, and between extensor muscles (r=0.410,
P<0.01) and flexors (r=0.516, P<0.05) with BMD
of trochanter. In males, a positive correlation exists
between flexor muscular strength (r=0.566, P<0.05),
abductor (r=0.594, P<0.05) and extensor (r=0.615,
P<0.05) with BMD of femoral neck and between
abductor muscles and BMD of trochanter (r=0.518,
P<0.05). In both sexes there was no correlation
between back extensor muscles and BMD of the
lumbar spine. In analyses of the linear correlation
Table 2. Correlation coefficient between muscular strength and bone
mineral density
Muscular strength
Bone mineral density r
(P-value)
Flexors
Femoral neck
Abductors
Femoral neck
Extensors
Femoral neck
Flexors
Trochanter
Abductors
Trochanter
Extensors
Trochanter
Extensors muscles of the spine
Lumbar spine
Statistical analysis
Regression analysis was performed using Spearman’s
correlation analysis. The significance of the differences
between mean values was assessed by the Mann–
Whitney U Test. The value P<0.05 was considered to
be significant. Pearson rank correlation coefficient was
used for testing relationships between variables.
Results
In the 30 patients who had undergone haemodialysis,
the BMD of the lumbar spine, femoral neck and
0.490
(0.005 )*
0.671
(0.0008 )*
0.658
(0.01 )*
0.413
(0.02 )*
0.189
(0.17 )
0.433
(0.01 )*
−0.119
(0.28 )
A significant association exists (*) between the strength of flexors,
extensors, and abductors muscles with BMD of femoral neck, as
well as the BMD of trochanter with flexors and extensors muscles.
None at the spinal level.
130
Fig. 1. There is a positive linear correlation between the strength of
flexors muscles and BMD of the femoral neck.
A. Spindler et al.
Fig. 3. There is a positive linear correlation between the strength of
abductors muscles and BMD of the femoral neck.
muscular strength of abductors (r=0.624, P<0.05)
and extensors (r=0.536, P<0.05).
Discussion
Fig. 2. There is positive linear correlation between the strength of
extensors muscles and BMD of the femoral neck.
between the BMD of the spine, the femoral neck and
the trochanter with the age of the patients, the time of
dialysis, serum albumin, calcium, phosphorus, PTH,
and muscular strength, the Pearson coefficient of correlation only showed a significant association between
the BMD of femoral neck and trochanter with the
strength of the femoral muscles (r=0.602, P<0.05).
No significant correlation was found between the BMD
of the femoral neck or trochanter with the time of
dialysis, patient age, calcium, phosphorus, albumin,
and the PTH serum values ( Table 3 ). In the lumbar
spine the BMD did not correlate with any of these
variables ( Table 4). The Kt/V urea was correlated with
In recent years there has been an increasing interest in
the effects of physical activity on bones and the relationship between muscular strength and bone density.
Studies regarding animals and humans have found an
increase of BMD after weight-bearing exercise
[9,19–22]. These findings have been related to Frost’s
theory of ‘mecanostat’, which postulates that mechanical overload increases the modelling and diminishes
the remodelling [14]. In addition to biomechanical
factors, humoral and hormonal mechanisms play a
role in bone changes secondary to immobilization and
exercise. In the serum of rats that returning from space
flight, PTH, phosphorus, creatinine, and magnesium
were somewhat higher compared to the control group
and the basal values. The humoral picture was interpreted within the context of acute renal insufficiency
[23]. Franck et al. [24] found diminution of PTH after
8 weeks of an organized programme of physical activity. In our knowledge about patients undergoing
haemodialysis, findings have been published only
regarding the influence of exercise on depression and
psychosocial functioning [25], patient sensitivity to
insulin [26 ], metabolism [27], hypertension [28 ], and
lipoproteins [29 ]. Until now there have been no publications that have studied the correlation between
muscular strength with the BMD in patients undergoing regular haemodialysis. In the present study we
found a significant correlation between the strength of
the femoral flexor, extensor, and abductor muscles
with the BMD in the femoral neck, as well as between
the femoral flexor and extensor muscles with the BMD
in the trochanter in both sexes. However, we found no
Muscular strength and bone mineral density in HD patients
131
Table 3. Pearson (r) correlation coefficients between the BMD of the femoral neck with age, time of dialysis, albumin, Ca, P, PTH, and
muscle strength
BMD
Age
Time of dialysis
Albumin
Ca
P
PTH
Muscle strength
Femoral neck
r=−159
NS
r=−0.032
NS
r=0.209
NS
r=0.086
NS
r=0.122
NS
r=−0.369
NS
r=0.602
P<0.05
There is a significant correlation of BMD of femoral neck with muscle strength.
Table 4. Pearson (r) correlation coefficients between the lumbar spine BMD with age, time of dialysis, albumin, Ca, P, PTH, and
muscle strength
BMD
Age
Time of dialysis
Albumin
Ca
P
PTH
Muscle strength
Lumbar spine
r=0.243
NS
r=0.272
NS
r=0.142
NS
r=0.419
NS
r=0.074
NS
r=0.245
NS
r=0.24
NS
There is no correlation between the lumbar spine BMD and age, time of dialysis, albumin, Ca, P, PTH, and muscular strength.
relationship between strength of the extensors muscles
of the back with BMD in the spine. This lack of
relationship may be due to various factors, one of
which is that patients with chronic renal failure may
develop predominantly vertebral osteosclerosis secondary to hypersecretion of PTH [30]. Another cause may
be the effect of the line of gravity that passes through
the proximal femur away from the lumbar vertebral
bodies [31 ]. Moreover, the proximal femur muscles
are stronger and they insert nearer to the area in which
the BMD is measured. Gender, age, time of haemodialysis and serum PTH were not associated with the
BMD. This may be due to the fact that the rate which
haemodialysis patients lose bone mass varies widely
[32 ]. Even though there is no publication that associates Kt/V urea with muscular strength, we think that
the significant correlation we find between Kt/V and
strength of some muscles reflects a better nutritional
state. The deterioration of bone in patients undergoing
haemodialysis is a complex process [33 ], for which it
is necessary to take special precautions in order to
prevent skeletal damage after the initiation of dialysis
treatment. Given the relationship we observed between
BMD and muscle strength in regular haemodialysis
patients, we believe that this parameter should be
evaluated.
Acknowledgements. We wish to thank Mrs Silvana Spindler for her
excellent technical assistance.
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Received for publication: 22.2.96
Accepted in revised form: 19.9.96