Copyright 2007 Blackwell Munksgaard
Pediatr Transplantation 2007: 11: 24–30
Pediatric Transplantation
DOI: 10.1111/j.1399-3046.2006.00595.x
ABPM vs. office blood pressure to define
blood pressure control in treated
hypertensive paediatric renal transplant
recipients
Ferraris JR, Ghezzi L, Waisman G, Krmar RT. ABPM vs. office blood
pressure to define blood pressure control in treated hypertensive
paediatric renal transplant recipients.
Pediatr Transplantation 2007: 11: 24–30. 2007 Blackwell Munksgaard
Jorge R. Ferraris1, Lidia Ghezzi1,
Gabriel Waisman2 and Rafael T.
Krmar3
1
Servicio de Nefrologa Peditrica, Hospital Italiano,
Unidad de Hipertensin Arterial del Servicio de
Clnica Mdica, Hospital Italiano, Buenos Aires,
Argentina, 3Division of Paediatrics, Department for
Clinical Science, Intervention and Technology,
Karolinska Institutet, Karolinska University Hospital,
Huddinge, Sweden
2
Abstract: While 24-h ambulatory blood pressure monitoring (ABPM) is
an established tool for monitoring antihypertensive therapy in adults,
data in children are scarce. We retrospectively analysed whether office
blood pressure (BP) is reliable for the diagnosis of BP control in 26
treated hypertensive paediatric renal transplants. Controlled office BP
was defined as the mean of three replicate systolic and diastolic BP
recordings less than or equal to the 95th age-, sex- and height-matched
percentile on the three-outpatient visits closest to ABPM. Controlled
ABPM was defined as systolic and diastolic daytime BP £ 95th distribution adjusted height- and sex-related percentile of the adapted
ABPM reference. Eight recipients (30%) with controlled office BP were
in fact categorized as having non-controlled BP by ABPM criteria.
Overall, when office BP and ABPM were compared using the Bland and
Altman method, the 95% limits of agreement between office and daytime values ranged from )12.6 to 34.1 mmHg for systolic and )23.9 to
31.7 mmHg for diastolic BP, and the mean difference was 10.7 and
3.9 mmHg respectively. Office readings miss a substantial number of
recipients who are hypertensive by ABPM criteria. Undertreatment of
hypertension could be avoided if ABPM is applied as an adjunct to
office readings.
In renal transplant recipients, regardless of
patient age, hypertension is a common posttransplant complication (1–3) and has been
shown to be a risk for both rejection (4) and
graft dysfunction (5, 6). In addition, hypertension has been found to contribute to premature
cardiovascular disease (7, 8), which accounts for
one of the leading causes of graft loss among
adult renal transplant recipients (9). As a result,
close monitoring of BP has become an important
part of post-transplant medical care of adults
and children with renal allografts (3, 10).
Abbreviations: ABPM, ambulatory blood pressure monitoring; BP, blood pressure.
24
Key words: children – renal transplantation – office
blood pressure – ambulatory blood pressure – blood
pressure control
Rafael Toms Krmar, Division of Paediatrics,
Department for Clinical Science, Intervention and
Technology, Karolinska Institutet, Karolinska
University Hospital, Huddinge, S-141 86 Stockholm,
Sweden
Tel.: +46 8 58581480
Fax: +46 8 58581410
E-mail: [email protected]
Accepted for publication 24 July 2006
Investigations conducted in adult hypertensive
patients, showed that antihypertensive drug
therapy based on 24-h ABPM is associated with
more sustained BP control and less intensive
drug treatment than when pharmacologic therapy is guided upon office BP readings (11, 12).
Over the past decade, there has been much
focus on ABPM as a potential useful technique
for assessing the true BP in children with high
risk for hypertension (13), including paediatric
renal allograft recipients (14–18). However,
evaluating BP control in treated hypertensive
children with renal allografts, in whom
long-standing hypertension carries a risk of death
(19), has elicited few investigations (17, 18).
At our institution, ABPM was introduced in
1995 in clinical investigations and thereafter in
ABPM vs. office BP in paediatric renal transplants
patient care as a reference method to better
characterize a patient’s BP pattern. In this
retrospective study, we reviewed our experience
using ABPM and sought to assess whether sole
use of office BP readings are sufficiently reliable
in the diagnosis of BP control in treated hypertensive paediatric renal transplant recipients.
Patients and methods
Patients
Treated hypertensive children and adolescents who regularly attended the Paediatric Renal Transplant Section at
Hospital Italiano (Buenos Aires, Argentina), in whom
ABPM had been performed as part of a more comprehensive assessment of efficacy of ongoing antihypertensive
therapy, were considered to be potentially eligible for
inclusion and their records reviewed. Inclusion criteria for
further analysis were as follows: stable functioning renal
graft, defined as the absence of an increase in serum creatinine ‡20% during the three outpatient visits closest to
ABPM, and no change in recipient’s medication, including
antihypertensive or episode of infection during the same
period. In addition, a minimum of 70% valid readings
throughout the 24-h period of BP recordings was required
for data to be analysed. The analysis of the results was
performed retrospectively and the approval for this study
was granted by the Ethics Committee at Hospital Italiano
(Buenos Aires, Argentina).
Methods
At each outpatient clinic visit office BP was measured by
physicians and determined with a mercury sphygmomanometer on the right arm with cuffs of adequate size. The
first and the last Korotkoff sounds (K1 and K5) were taken
as systolic and diastolic BP respectively. The mean of three
replicate BP readings, taken approximately 1 min apart
with the recipient in a sitting position after ‡5 min of rest,
was used to determine the recipient’s office systolic and
diastolic BP. Seated office BP was always measured in the
morning and close after the recipients had taken their
medication(s), including antihypertensive drugs.
ABPM was recorded on the non-dominant arm using an
arm cuff of similar size to the one used for office BP and
carried out using a validated non-invasive portable oscillometric device (SpaceLabs model 90207; SpaceLabs Inc.,
Redmond, WA, USA) (20). The recorder was programmed
to measure BP every 10 min from 06:00 to 22:00 hours and
every 20 min from 22:00 to 06:00 hours. In order to improve
the quality of the BP recordings recipients were given tailored instructions on the procedure and encouraged to
maintain their usual activities. They were asked to keep still
at the time of measurements and to complete a diary of
events during the 24-h period, including their awake and
asleep times.
Nighttime was defined according to the period of nighttime sleep based on recipient’s diary. In recipient(s) who
reported daytime naps during their ABPM, daytime values
were calculated by excluding the period of nap, as previously described (21). The nocturnal percentage changes in
mean systolic and diastolic BP were calculated as follows:
[(mean daytime ) mean nighttime)/mean daytime] · 100.
Due to the lack of reference values for office and ambulatory BP in healthy Argentinean children and adolescents,
recipientsÕ BP readings were compared with other population norms. Consequently, recipient’s office BP was related
to the individual age-, sex- and height-related percentile of
the adapted reference standard (22). Mean ambulatory
daytime and nighttime BP values were related to the
recipient’s adjusted body dimensions- and sex-related percentile for day and night described in the published paediatric normative data for ABPM (23). For analysis purposes,
ABPM data from recipients with body height <120 cm
were included in the 120-cm group.
In the present analysis, Ôcontrolled office BPÕ, i.e. BP
within the normotensive range, was defined as the average
of three replicate seated systolic and diastolic office BP
recordings less than or equal to the 95th age-, sex- and
height-matched percentile of the adapted reference standard
(22) on the three outpatient visits closest to ABPM. Because
these reference values include no measurements of nighttime
BP, Ôcontrolled ambulatory BPÕ was defined as systolic and
diastolic daytime BP £ 95th distribution adjusted heightand sex-related percentile of the adapted paediatric ABPM
reference values (23). On the basis of these definitions, Ônoncontrolled office and daytime ambulatory BPÕ, i.e. BP
readings within the hypertensive range were defined as systolic and/or diastolic BP values exceeding the 95th percentile
of the respective adapted reference standards (22, 23).
Systolic and/or diastolic ambulatory nighttime hypertension was defined as mean BP value(s) above the 95th
distribution adjusted body dimensions- and sex-related
percentile for night (23).
According to data derived from healthy children and
adolescents (24), non-dippers were arbitrarily defined as
those recipients with a percent decline in BP of less than the
mean value ) 1 SD (i.e. <7% for systolic BP and/or <14%
for diastolic BP respectively).
Analysis
Results are presented as mean ± SD unless otherwise
indicated. Differences between groups were assessed by twosided unpaired t-test for continuous data, and by the analysis
of frequency distribution (chi-squared analysis) for categorical variables. The office and daytime mean values were
compared by Student’s paired t-test. Pearson correlation
coefficients were used to investigate the association of office
BP with ambulatory BP. Comparison of BP recorded by
physicians in the office and by ABPM was carried out as
suggested by Bland and Altman (25). By applying this approach, the difference between measurements by the two
methods can be examined and the discrepancy between the
actual measurements and the mean of the two methods can
be assessed. Thus, it is assumed that the smaller the SD the
better the agreement between the two methods. Accordingly,
the 95% limits of agreement were calculated as the mean
difference between ABPM and office measurements ±2 SD,
and the average of measurements evaluated by the two
methods were plotted against their difference for both systolic and diastolic BP. For statistical analysis purpose, office
BP recordings obtained over the three outpatient visits closest in time to ABPM were averaged to give a single value,
which was regarded as recipient’s office BP. A probability
value p < 0.05 was considered statistically significant.
Results
Twenty-six renal transplant recipients (18 males
and eight females) met the inclusion criteria for
25
Ferraris et al.
the analysis. ABPM was performed at the mean
age of 14 ± 3.2 years and a mean interval after
transplantation of 3.6 ± 3.3 years (range 0.4–
9.5 years). All recipients underwent their first
transplantation and received triple immunosuppressive treatments consisting of cyclosporin with
mycophenolate mofetil and corticosteroid (n ¼ 9)
or deflazacort (n ¼ 3), cyclosporine with azathioprine and corticosteroid (n ¼ 2) or deflazacort (n ¼ 2), tacrolimus with mycophenolate
mofetil and corticosteroid (n ¼ 8), and tacrolimus
with azathioprine and corticosteroid (n ¼ 2). In
11 recipients, antihypertensive drug therapy was
initiated before renal transplantation and within
1–15 months after transplantation in 15 recipients. Nineteen recipients were taking dihydropyridine calcium antagonists (nifedipine n ¼ 13,
amlodipine n ¼ 4) or angiotensin-converting enzyme inhibitors (enalapril n ¼ 2). In five additional recipients nifedipine was associated with
b-blocker (timolol, n ¼ 2), a-blocker (prazosin,
n ¼ 2) or enalapril (n ¼ 1). Two recipients were
taking amlodipine with b-blocker (atenolol) or
with atenolol and prazosin respectively. Overall,
only one recipient experienced an episode of acute
rejection before ABPM examination.
Eight recipients were categorized as having
controlled BP by both office and ambulatory
measurements and two recipients as having noncontrolled BP by either office or ambulatory
measurement. In eight recipients, BP was controlled when measured by office but not by
ABPM, with the opposite observed in three
recipients. In five recipients, office BP could not
be categorized since their office readings fluctuated in one or two of the three outpatient visits
closest in time to ABPM.
Recipients were further categorized, according
to their ambulatory daytime BP values, as having
controlled or non-controlled ambulatory BP.
The characteristics of both groups of recipients
are given in Table 1. There were no differences
between the groups regarding age, gender,
height, weight, body mass index, estimated
glomerular filtration rate, office systolic and
diastolic BP, donor source and primary diagnosis
for renal failure. There were no differences
between recipients with controlled and noncontrolled ambulatory BP regarding the time
elapsed from the transplantation to ABPM
examination, 4.1 ± 3.8 years and 2.9 ± 2.8
years, respectively, p ¼ 0.3. A summary of
ambulatory BP averages for recipients with
controlled and non-controlled ambulatory BP is
given in Table 2. Although the percentage of
successful recordings was higher in the former
group, the number of successful readings was
26
Table 1. RecipientsÕ characteristics
Variable
Age (years)
Sex (male/female)
Height (cm)*
Weight (kg)
BMI (kg/m2)
Overweight (n) eGFR (ml/min/1.73 m2)à
Office SBP (mmHg)§
Office DBP (mmHg)§
Pre-transplant dialysis (yes/no)
Donor source (n)
Living related
Deceased
Primary diagnosis (n)
Renal hypo/dysplasia
Congenital nephropathies
Acquired glomerulopathies
Controlled
ambulatory BP
(n ¼ 14)
Non-controlled
ambulatory BP
(n ¼ 12)
p-value
14.7 € 2.7
10/4
146.6 € 20.4
43.8 € 17.4
19.8 € 3.8
3
79.1 € 14.5
113.4 € 16
73.1 € 11.2
9/5
13.2 € 3.6
8/4
133.1 € 16.8
41.9 € 14.9
22.4 € 4.6
6
76.2 € 27.2
115.6 € 13.6
71.8 € 11
8/4
0.2
0.8
0.08
0.7
0.1
0.1
0.7
0.7
0.7
0.9
13
1
9
3
0.2
0.2
3
3
8
4
3
5
0.5
0.8
0.4
Values are mean € SD unless otherwise indicated.
BP, blood pressure; BMI, body mass index; eGFR, estimated glomerular filtration rate; SBP, systolic blood pressure; DBP, diastolic blood pressure.
*In two recipients with controlled ambulatory BP and in four recipients with
non-controlled ambulatory BP height was <120 cm (range 110–116 and 110–
116 cm respectively).
Overweight was defined by applying the cutoff points for BMI by sex (26).
à
eGFR was calculated according to the modified Schwartz Formula (27).
§
Represents the BP average recorded at clinic over the three outpatient visits
closest in time to ambulatory BP monitoring.
Table 2. Results of ambulatory BP monitoring
Variable
Controlled
ambulatory BP
(n ¼ 14)
Non-controlled
ambulatory BP
(n ¼ 12)
p-value
Successful recordings (n)
Successful recordings (%)
Nocturnal sleep (h)
24-h SBP
24-h DBP
Daytime SBP
Daytime DBP
Nighttime SBP
Nighttime DBP
Nighttime fall in SBP (%)
Nighttime fall in DBP (%)
96.7
97.4
7.4
117.3
67.7
119.3
69.3
112.6
63.9
6.4
9.2
105
94.5
7.8
127.3
79.2
131.9
83.2
118.4
70.2
10.1
16.4
0.2
0.01
0.4
0.006
0.0001
0.002
<0.0001
0.1
0.05
0.06
0.01
€
€
€
€
€
€
€
€
€
€
€
19.5
2.6
1.2
10.2
7.5
10.7
7.4
10.3
8.9
4.5
6.2
€
€
€
€
€
€
€
€
€
€
€
16.6
3.2
1.1
5.6
4.8
7.3
5
7.6
6.6
5.3
7.6
Values are mean € SD. Abbreviations as in Table 1.
similar in both groups. As expected from methodological definitions, systolic and diastolic daytime and 24-h BP values were significantly lower
among recipients with controlled than recipients
with non-controlled ambulatory BP.
Correlations between the two methods were
significantly >0 but <1 for systolic but not for
diastolic BP in recipients with both controlled
and non-controlled ambulatory BP, suggesting
that office systolic BP readings might be more
ABPM vs. office BP in paediatric renal transplants
Table 3. Correlation coefficients between office SBP and DBP and respective
ambulatory BP readings
Variable
Office SBP
24-h SBP
Daytime SBP
Nighttime SBP
Office DBP
24-h DBP
Daytime DBP
Nighttime DBP
Controlled
ambulatory BP
(n ¼ 14)
Non-controlled
ambulatory BP
(n ¼ 12)
r*
p-value*
r
p
0.74
0.78
0.43
0.002
0.001
0.1
0.50
0.57
0.13
0.9
0.04
0.6
0.18
0.28
0.11
0.5
0.3
0.70
0.04
0.13
0.12
0.8
0.6
0.6
Abbreviations as in Table 1.
*Data are values of correlation coefficients r and p respectively.
accurate than diastolic readings in predicting
daytime BP values (Table 3).
In terms of nighttime BP values, no significant
difference was observed between the two groups.
The percentage nighttime drop in both systolic
and diastolic BP was found to be higher in
recipients with non-controlled ambulatory BP,
Table 2. Overall, nighttime hypertension was
identified in 16 of 26 recipients, systolic and
diastolic nighttime hypertension in 12, and diastolic nighttime hypertension in four recipients
respectively. Non-controlled daytime BP and
nighttime hypertension, i.e. poor 24-h BP control
of hypertension, was found in six recipients and
isolated nighttime hypertension in 10 recipients.
Dipping status is summarized in Table 4.
When daytime vs. office BP values were
compared in the entire group, only daytime
systolic BP was statistically different than that
obtained by office measurements (125.1 ± 11.1
mmHg vs. 114.4 ± 14.7 mmHg; p < 0.0001 for
systolic BP, and 75.7 ± 9.4 mmHg vs. 71.8 ±
11.6 mmHg; p ¼ 0.1 for diastolic BP respectively). Agreement between the two methods of
measurements according to the Bland and Altman method is shown in Fig. 1. For systolic and
Table 4. Dipping status
Dipping status
Controlled
Non-controlled
ambulatory BP ambulatory BP
(n ¼ 14)
(n ¼ 12)
p-value
Dipper (n)
Systolic non-dipper (n)
Diastolic non-dipper (n)
Systolic and diastolic non-dipper (n)
3
–
4
7
8
1
–
3
0.02
0.3
0.06
0.2
Non-dipping status is defined as a per cent decline in BP of less than the mean
value ) 1 SD, i.e. <7% for systolic BP and/or <14% for diastolic BP respectively (24).
diastolic BP, the mean difference was 10.7 and
3.9 mmHg, respectively, and the 95% limits of
agreement of the difference were )12.6/
34.1 mmHg for systolic and )23.9/31.7 mmHg
for diastolic BP respectively.
Discussion
This study conducted through our retrospective
review of ABPM usage as a method of reference
in treated hypertensive paediatric renal transplant recipients establishes that almost one-third
of the test group, in whom BP appeared to be
controlled according to office BP recordings,
were in fact non-controlled by ABPM criteria.
In previous paediatric studies, the prevalence
of non-controlled ambulatory BP ranged from
45% to 82%, 14 of 31 recipients (18) and 18 of 22
recipients (17) respectively. However, it is noteworthy that these results cannot be deemed
comparable as the latter study defined noncontrolled ambulatory BP from normative data
for office BP readings instead of ABPM references values as defined in the former and our
study. In addition, contrary to the current
investigation, both studies defined non-controlled ambulatory BP by analysing mean daytime and nighttime values together. Moreover,
these studies did not report on the agreement
between office- and ambulatory-based definitions
of BP control as presented here. Despite these
discrepancies in data analysis, our investigation,
similar to the previous studies, shows that ABPM
is a useful tool for assessing true responders to
antihypertensive therapy.
Of note, in our study the BP threshold for
defining non-controlled office BP was arbitrarily
set at systolic and/or diastolic BP >95th age-,
sex- and height-matched percentile of the adapted reference standard (22). This limit, as it has
been comprehensively discussed in the literature,
is a statistical rather an outcome-based definition
as cardiovascular events secondary to arterial
hypertension are extremely rare in the paediatric
population. Furthermore, there are so far no
available prospective paediatric data showing
that long-term antihypertensive therapy, either
by lowering BP to less than 95th or 90th
percentile, may preclude or reverse hypertensive
end-organ damage as evaluated by means of
surrogate markers of cardiovascular disease, i.e.
structural or functional abnormalities regarded
as early markers of hypertension sequelae.
In comparison with earlier reports (14–18), we
also identified a large number of recipients with
nighttime hypertension, which like distorted
circadian BP rhythm cannot be detected by office
27
Ferraris et al.
Fig. 1. Comparison of systolic and diastolic daytime ambulatory and office blood pressure according the method of Bland
and Altman (SBP, systolic blood pressure; DBP, diastolic blood pressure).
BP readings. Thus, in treated hypertensive recipients, ABPM provides additional information on
BP control during nighttime. It should be
stressed that in the current study there were no
differences in nighttime BP values between
groups. This might explain the fact that a larger
per cent decline in nocturnal BP was observed
among recipients with non-controlled daytime
ambulatory BP compared to recipients with
controlled BP.
Although the clinical significance of blunted
physiological nocturnal fall of BP in paediatric
renal transplant recipients, i.e. non-dippers,
remains so far unknown (17) it has been suggested to indicate underlying renovascular pathology (14). However, the distinction between
dipper and non-dipper recipients as reported in
the present investigation remains questionable on
the basis of a single ABPM study (28).
Although nearly half of our study population
was found to have non-controlled daytime
ambulatory BP it cannot be said that the
antihypertensive therapy they received was ineffective as we cannot exclude the possibility that
non-adherence to treatment might have contributed to the poor control of BP (29). At our
institution, education about non-pharmacological and pharmacological measures is regularly
reinforced at every visit. RecipientsÕ parents are
usually motivated to play an active role in the
follow up, for instance, by reporting side effects
that might be related to the medication or if
agreeable, by recording BP at home. Due to these
measures, we hypothesize that non-compliance
28
would then not account for the difference in BP
observed between recipients with controlled and
non-controlled ambulatory BP. On the other
hand, it can also be speculated that if antihypertensive treatment has been based upon ABPM a
large number of recipients would have benefit
from a better control of BP.
The use of office BP recordings still remains
the routine screening tool to assess paediatric
population for hypertension (22, 30). An important consideration, while interpreting office BP
readings obtained by auscultatory methods, is
that BP measurements during office visits should
be of a high standard as improper BP measurement techniques can result in the overdiagnosis
or underdiagnosis of hypertension (22, 30).
However, one of the major limitations of BP
readings obtained on an intermittent basis is the
high variability of BP, i.e. the small number of
readings obtained at a clinic visit may not mirror
patient’s usual BP (31). In this regard, ABPM, by
carrying out repeated BP recordings over a 24-h
period and without being subject to observer
bias, provides more representative values of BP
than office recordings (32). For this reason, as
office BP and ABPM do not measure the same
BP, it is not surprising that a considerable
variation among recipients in the magnitude of
BP measurements obtained by the two methods
was observed (Fig. 1). This observation correlates with a previous study where the long-term
reproducibility of ABPM in children with renal
allografts was shown to be superior to that of
office measurements (28).
ABPM vs. office BP in paediatric renal transplants
Ambulatory BP monitoring also allows the
identification of children with white coat hypertension (33), a condition that can lead to overdiagnosis of hypertension and subsequent
unnecessary treatment, as well as the opposite
phenomenon, i.e. normal office BP but hypertension by ABPM criteria. As a consequence of this,
ABPM has been more widely used in the
transplant clinic in recent years and has been
suggested as a standard method for the diagnosis
and therapeutic monitoring of hypertension in
paediatric renal recipients (3, 34). However, the
latest recommendations for diagnosis, evaluation, and treatment of hypertension in children
and adolescents (22) do not indicate ABPM as a
clinical tool for the assessment of efficacy of
antihypertensive therapy.
Our study presents compelling evidence, which
shows that if office BP remains as the main
method of choice in the assessment of efficacy of
antihypertensive treatment, a substantial number
of recipients with non-controlled ambulatory BP
would be missed. In conclusion, we believe that
ABPM should be considered as an adjunct to
office BP readings to better characterize the
recipient’s BP pattern.
Acknowledgments
The authors would like to thank Professor Ulla B. Berg for
her critical review of this study. Dr Krmar was supported by
grants from the Freemason’s Stockholm Foundation for
Children’s Welfare and the Samariten Foundation.
Conflicts of interest
None.
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