Osteoporos Int (2002) 13:353–357ß
2002 International Osteoporosis Foundation and National Osteoporosis Foundation
Skeletal Status in Children, Adolescents and Young Adults with End-Stage Renal Failure Treated with Hemo- or Peritoneal Dialysis
W. Pluskiewicz1, P. Adamczyk2, B. Drozdzowska3, K. Szprynger2, M. Szczepanska2, Z. Halaba4 andD. Karasek11Department and Clinic of Internal Diseases, Diabetology and Nephrology – Metabolic Bone Diseases Unit, 2Dialysis Division,Department of Pediatrics, Clinic of Nephrology, Endocrinology and Metabolic Disorders of Childhood, and 3Department andChair of Pathomorphology, Silesian School of Medicine in Katowice, Poland; and 4Outpatient Medical Care, Zabrze, Poland
Abstract. The skeletal status in 30 children, adolescents
strongly affected by ESRF. Both QUS and BMD
and young adults (18 females, 12 males) with end-stage
measurements show an ability to express skeletal
renal failure (ESRF) aged 9-23 years (mean 15.8 + 3.6
changes in a similar manner, though the QUS parameter
years) was evaluated using measurements of bone
seems to be more sensitive at revealing changes due to
mineral density (BMD, g/cm2) at the spine and total
body (TB) (Lunar DPX-L, USA), quantitative ultrasound(QUS) of the hand phalanges (DBM Sonic 1200, IGEA,
Keywords: Adolescents; Bone mineral density; Chil-
Italy) and laboratory investigations (parathyroid hor-
dren; End-stage renal failure; Quantitative ultrasound;
mone, serum total and ionized calcium, serum phos-
phate). Eleven subjects were treated with hemodialysisand 19 with peritoneal dialysis. The mean value of theamplitude-dependent speed of sound (Ad-SoS, m/s)measured by QUS was signiﬁcantly decreased incomparison with the value obtained in a group of 686
age-matched controls (1942 74 m/s vs 2050 77 m/s,p<0.0001). BMD measurements were also decreased in
Renal osteodystrophy is one of the most important
comparison with mean values for the healthy population
complications of chronic renal failure, and bone loss is
(Z-scores for spine 71.47, and for TB 71.53). Duration
frequently seen already in the early phase of the disease
of dialysis correlated signiﬁcantly with spine-BMD, TB-
. Renal osteodystrophy may result in considerable
BMD and Ad-SoS (r = 70.37, r = 70.45, r = 70.55,
morbidity for patients with end-stage renal failure
respectively, p<0.05), while duration of ESRF did not
(ESRF). Bone biopsy with tetracycline labeling is still
have such an inﬂuence. Laboratory investigations did not
considered the ‘gold standard' for the assessment of
correlate with skeletal parameters. Ad-SoS correlated
renal osteodystrophy [2,3]. Bone biopsy, being an
signiﬁcantly with spine-BMD (r = 0.45, p<0.05) and TB-
invasive method, can not be widely used for assessing
BMD (r = 0.56, p<0.01). Both QUS and BMD values
the skeletal status in subjects with ESRF. Lately, bone
correlated signiﬁcantly with Tanner stages (r ranged
mineral density (BMD) measurements have more often
from 0.59 to 0.69, p<0.001) and did not increase with
been applied for the diagnosis of renal osteodystrophy
age except for correlation between age and TB-BMD. In
[4–6]. More recently, quantitative ultrasound (QUS)
conclusion, skeletal status in the population studied is
methods were introduced for the diagnosis of skeletalchanges due to ESRF [4,7–11]. QUS measurements can
Correspondence and offprint requests to: Wojciech Pluskiewicz,
be performed in several sites of the skeleton, the most
MD, Head of Metabolic Bone Diseases Unit, 3 Maja 13/15 Street, 41-
common being the calcaneus. In 1992 a new ultrasound
800 Zabrze, Poland. Tel/fax: +48 32 2718110. e-mail: firstname.lastname@example.org
(US) technology was developed for measurements of the
W. Pluskiewicz et al.
hand phalanges (DBM Sonic 1200, IGEA, Carpi, Italy).
The control group for QUS examinations was
In some studies [4,7,8] these measurements allowed the
recruited randomly from pupils of local schools and
detection of skeletal alterations in ESRF.
students of the Silesian School of Medicine. Prior to and
The aim of the present study was the evaluation of
during the evaluation there were no factors in the
skeletal status in children, adolescents and young adults
controls known to affect bone metabolism (either
with ESRF using BMD measurements, QUS of the hand
medications or diseases). The controls were selected
phalanges and laboratory investigations.
from a group of 1010 subjects and matched with thepatients for age and gender. It was not possible to obtaina control group comparable with the patients with regard
Subjects and Methods
to weight and height because the patients in ESRF had amean body size much lower than the normal, healthy
population. The local ethics committee gave itspermission for the study protocol.
The study group consisted of 30 patients (18 females, 12males) and 686 controls (423 females, 263 males). Theclinical characteristics of the patients and controls are
given in Table 1. The population studied included allsubjects (children, adolescents, young adults) with ESRF
Skeletal status was assessed by dual-energy X-ray
from the Silesian region of Poland with about 4 million
absorptiometry (DXA) examinations of the spine BMD
inhabitants. Eleven patients were treated with regular
(spine-BMD, g/cm2) and total body BMD (TB-BMD,
hemodialysis, receiving two or three dialysis sessions per
g/cm2) using a DPX-L densitometer (Lunar, Madison,
week; the duration of hemodialysis was 6–15 h per
WI) and by US measurements of the proximal hand
week. Nineteen patients were on peritoneal dialysis (18
phalanges using a DBM Sonic 1200 (IGEA, Carpi,
on automatic peritoneal dialysis and 1 on continuous
Italy). Comparison between BMD values in patients and
ambulatory peritoneal dialysis). The average duration of
in the normal, healthy population was provided using Z-
renal replacement therapy was 3.1 + 2.5 years, and the
scores. All DXA measurements were done by the same
mean time since the diagnosis of chronic renal failure
operator. The coefﬁcient of variation (CV % = SD/mean
(CRF) was 6.2 + 4.1 years. All subjects remained on
6 100%) for BMD measurements was 1.1% for spine-
drug therapy for CRF receiving calcium carbonate, 1a
BMD and 0.6% for TB-BMD.
hydroxycholecalciferol and erythropoietin. Ten subjects
The US unit consists of two probes mounted on an
received corticosteroid therapy: 5 patients before the
electronic caliper: one emitter and one receiver. The
study, and 5 during the study. The mean duration of this
latter records the US energy after it has crossed the
treatment was 60 months (range 2–169 months), and the
phalanx. We determined the amplitude-dependent speed
dose was 0.5–1 mg of prednisone per 1 kg of body
of sound (Ad-SoS, m/s) in the distal metaphyses of the
weight daily. The reasons for CRF were: chronic
proximal phalanges of the second through ﬁfth ﬁngers of
pyelonephritis in 11 patients, chronic glomerulonephritis
the dominant hand. As was previously shown, no
in 6, lupus nephritis in 2, polycystic kidney disease in 2,
statistically signiﬁcant differences between measure-
rapidly progressive glomerulonephritis, familial nephro-
ments of the extremity with and without a ﬁstula exist
nophthisis, bilateral renal hypoplasia, Wegener's gran-
. Speed of sound in bone tissue was calculated
ulomatosis, amyloidosis, congenital nephrotic syndrome
considering the ﬁrst signal with an amplitude of 2 mV at
and toxic injury in 1 each, and unknown causes in 2.
the receiving probe; thus, the measured speed of sound is
Sexual maturity was assessed using Tanner stages. There
amplitude-dependent. Acoustic coupling was achieved
were 5 subjects without any symptoms of puberty, 4 in
using a standard US gel. All measurements were done by
Tanner stage I, 3 in Tanner stage II, 3 in Tanner's stage
the same operator. The CV% was 0.64%.
III, 9 in Tanner stage IV and 5 in Tanner stage V. No
The following laboratory tests were performed: serum
past fractures were noted in the dialysis patients.
intact parathyroid hormone (i-PTH), phosphorus andtotal and ionized calcium serum concentrations. All
Table 1. Clinical characteristic of patients and controls
blood samples were taken just before hemodialysis, or inthe morning in the patients treated with peritoneal
Patients (n = 30)a
Controls (n = 686)b
Duration of CRF (years)
Duration of dialysis (years)
All calculations of means and standard deviations (SDs)
as well as linear correlations were done using theStatistica program run on an IBM PC. Correlations
Values are mean + SD.
between Tanner stages and skeletal values were
CRF, chronic renal failure.
a.Eighteen females, 12 males.
performed using the Spearman rank correlation test.
b.Four hundred and twenty-three females, 263 males.
Because of the small size of the population studied we
Skeletal Status in End-Stage Renal Failure
did not calculate statistical relationships separately for
cant correlation with Ad-SoS (r = 70.29, p = 0.13).
gender and for the type of dialysis; all analyses were
Skeletal measurements were also correlated with the
performed for whole group. Statistical signiﬁcance was
duration of renal failure, duration of dialysis, age,
achieved with p<0.05.
weight, height and Tanner stages. These data arepresented in Table 3. All three bone parameterscorrelated negatively and signiﬁcantly with duration of
dialysis, though the Ad-SoS value was affected morethan the BMD values. Duration of CRF did not correlate
Table 2 shows the results of bone measurements and
with Ad-SoS and BMD of the spine and TB. Age
laboratory data in patients. BMD of the spine and total
correlated signiﬁcantly and positively with TB-BMD,
body are expressed in grams per square centimeter and
while spine-BMD and Ad-SoS showed a weaker,
Z-scores. Such data allow comparison of our results with
nonsigniﬁcant positive relationship with age. In the
normal values for age and gender.
controls, Ad-SoS correlated signiﬁcantly with age
Ad-SoS was signiﬁcantly lower in the dialysis patients
(r = 0.73, p<0.0001). Weight, height and data expressing
in comparison with controls (1942 + 74 m/s vs 2050 +
sexual maturation assessed by Tanner stages correlated
77 m/s, p<0.0001). Also BMD values were decreased in
signiﬁcantly with all three skeletal parameters in dialysis
comparison with the normal healthy population (Z-score
for spine-BMD was 71.47 and for TB-BMD was71.53). Ad-SoS correlated signiﬁcantly with spine-BMD (r = 0.45, p<0.05) and TB-BMD (r = 0.56,
p<0.01), and spine- and TB-BMDs correlated with eachother (r = 0.81, p<0.0001). The mean value of i-PTH was
The study has shown the serious abnormalities of
increased in the dialysis patients, while serum total and
skeletal status in the population studied. To our
ionized calcium, and phosphate, were in the normal
knowledge no studies using BMD and QUS measure-
range. Correlations of skeletal measurements with
ments in persons with ESRF aged less than 17 years have
laboratory data were calculated and no signiﬁcant
previously been published. Generally, there is a
relationships were obtained except for the correlation
signiﬁcantly greater number of adults than young
between ionized calcium and spine-BMD (r = 70.37,
subjects with ESRF treated with dialysis. In 1998 in
p = 0.05). i-PTH showed a weak, negative, nonsigniﬁ-
the whole of Poland 6878 persons were on dialysis .
Among them 242 subjects were younger than 20 years.
Table 2. Results for skeletal and laboratory measurements in patients
This means that our group constitutes of about 12% of
with end-stage renal failure
Polish dialysis patients (we had only 2 subjects olderthan 20 years). Because of the lack of other data it is not
possible to compare current results with other studies
performed in subjects of a comparable age. Results of
QUS measurements in our study were compared with
data for a large sample of the control group and have
shown that skeletal status in our subjects is strongly
affected by the disease. The difference between Ad-SoS
Total serum calcium (mmol/l)
in patients and controls was 108 m/s and this difference
Ionized serum calcium (mmol/l)
expressed in standard deviations is 1.45 (calculated as
108 m/s; 74 m/s is the SD value in the dialysis patients),which is very close to the Z-scores obtained for spine-
Values are mean + SD.
TB, total body; Ad-SoS, amplitude-dependent speed of sound; i-PTH,
and TB-BMDs in our population. In the study by Rico et
intact parathyroid hormone.
al.  performed with a DBM Sonic, a difference
Table 3. Correlations between skeletal parameters and age, body size, durations of chronic renal failure and dialysis, and Tanner stages
Values are correlation coefﬁcients (r), with p values in parentheses. CRF, chronic renal failure; TB, total body; Ad-SoS, amplitude-dependentspeed of sound.
NS, not signiﬁcant.
W. Pluskiewicz et al.
between hemodialyzed patients and controls expressed
some DXA evaluations were done (hand, ultradistal
in Z-scores was about 1. In another study investigating
radius, radial shaft) in a group of adults with ESRF.
Correlations between US and BMD measurements were
hemodialysis patients the difference between the value
higher (r = 0.46–0.68) than in our study (r = 0.45–0.55),
for healthy controls and patients was 119 m/s. If the
which can probably be explained by the similar cortical/
latter value were expressed as a Z-score it would be
trabecular ratio in sites measured in this study. The
71.4, which is very close to our data. A greater
duration of dialysis correlated with QUS (r = 70.41)
reduction in Z-score was observed by Foldes et al. 
and BMD values (r = 70.35 to 70.53), which is very
for speed of sound at the tibia (72.0), which can
close to our data, and duration of renal failure
probably be explained by the fact that cortical bone is
signiﬁcantly affected both US and BMD values, which
more sensitive to the inﬂuence of an increase in i-PTH
was not observed in the current study. Some differences
were noted in the comparison of current relationships
Also important information is provided by the
between i-PTH and skeletal parameters; we did not
comparison of age-related increase in Ad-SoS in the
ﬁnd such connections, while in Przedlacki et al.'s study
dialysis patients with the same relationships in controls.
i-PTH correlated signiﬁcantly with Ad-SoS in men (r =
In subjects with ESRF Ad-SoS did not increase
70.54), and with DXA of the hand (r = 70.38) and
signiﬁcantly with age, while in controls this correlation
radial shaft (r = 70.49). In the study by Przedlacki et al.
is signiﬁcant (r = 0.73, p<0.0001). This means that we
ionized calcium correlated signiﬁcantly with Ad-SoS
can expect the peak value of Ad-SoS in a patient with
only, while in the current study only spine-BMD was
ESRF to be lower than in healthy, control subjects.
correlated signiﬁcantly with serum ionized calcium. The
Correlations between age and BMD measurements
lack of signiﬁcant correlations between i-PTH and
provide a similar result. Only TB-BMD increased
skeletal parameters may suggest that hyperparathyroid-
signiﬁcantly with age in our subjects. In the study by
ism associated with a high level of i-PTH has no marked
Sabatier et al.  performed in a large population of
inﬂuence on bone status in our patients. A similar
574 persons aged 10–24 years, spine BMD correlated
observation is derived from the study in which no
signiﬁcantly with age (r = 0.49). Even stronger relation-
correlation between i-PTH and bone osteopenia was
ships were reported by Bonjour et al.  who obtained,
found . Another study showed that BMD of the total
in a population of 207 young subjects aged 9–18 years,
body and arm were inversely correlated with i-PTH .
correlations of spine BMD with age of 0.78 for males
The limitations of our study were: (1) the lack of
and 0.8 for females, and 0.63–0.87 and 0.7–0.84,
analyses performed separately for gender and type of
respectively for hip BMD. Our nonsigniﬁcant correlation
dialysis, due to the relatively small sample size, and (2)
of spine-BMD with age (r = 0.33) is weaker than those
the cross-sectional design. Despite these limitations it
obtained in these other studies. We did not ﬁnd any study
can be concluded that skeletal status in the population
presenting a correlation between TB-BMD and age, so
studied is strongly affected by ESRF. Both QUS and
direct comparison is not possible. Only Zanchetta et al.
BMD measurements show an ability to express skeletal
 in a study performed in a cohort of 900 subjects
changes in a similar manner, though the QUS parameter
aged 2–20 years assessed whole body mineral content. In
seems to be more sensitive to changes due to renal
this study, however, no exact value of correlation
failure because of a stronger negative relationship
between age and whole body mineral content was
between Ad-SoS and duration of dialysis.
presented, despite the fact that this relationship wassigniﬁcant. On the basis of our data we suspect thatneither spinal nor total body peak BMD in subjects with
ESRF will reach the level attained in a normal, healthypopulation. This may result in increased fracture risk in
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study by Montagnani et al. , who noted r = 70.28
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Received for publication 12 July 2001
Accepted in revised form 8 November 2001
Vestnik zoologii, 38(5): 57–66, 2004© I. A. Akimov, S. V. Benedyk, L. M. Zaloznaya, 2004 COMPLEX ANALYSIS OF MORPHOLOGICALCHARACTERS OF GAMASID MITEVARROA DESTRUCTOR (PARASITIFORMES, VARROIDAE) I. A. Akimov, S. V. Benedyk, L. M. Zaloznaya Schmalhausen Institute of Zoology NAS Ukraine,vul. B. Khmelnits'kogo, 15, Kyiv, 01601 Ukraine Accepted 23 October 2003 Complex Analysis of Morphological Characters of Gamasid Mite Varroa destructor (Parasitiformes, Var-roidae). Akimov I. A., Benedyk S. V., Zaloznaya L. M. — The study of seasonal variability of miteV. destructor was carried out. The summer generation of mites appears to be characterized by the largestmorphological variability whereas the winter one has stable characters. We failed to evolve the complexof morphological characters that would allow us to identify, with high level of reliability, certainphenotype of the mite. Significant stability of morphological characters of V. destructor in the course oftime was determined. The mean values of the length and width of the body allow to consider theUkrainian population of Varroa mite, which parasitize the honey bee Apis mellifera Linnaeus, as theKorean haplotype of Varroa destructor Anderson et Trueman, 2000.
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