(Hypertension. 1997;30:1162-1168.)
© 1997 American Heart Association, Inc.
Articles |
Sodium, Blood Pressure, and Arterial Distensibility in Insulin-Dependent Diabetes Mellitus
From the Departments of Internal Medicine (J.L., F.J. van I., M.A., E.J.P., A.J.M.D., C.D.A.S.) and Nuclear Medicine (R.P., E.F.I.C.), Academisch Ziekenhuis Vrije Universiteit, and the Institute for Cardiovascular Research, Vrije Universiteit, Amsterdam, Netherlands.
Correspondence to J. Lambert, MD, Department of Internal Medicine, Academisch Ziekenhuis Vrije Universiteit, PO Box 7057, 1007 MB Amsterdam, Netherlands.
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Abstract |
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Abstract We investigated 24-hour ambulatory blood pressure and arterial distensibility, a marker of biophysical vessel wall properties, in 32 normoalbuminuric type I diabetic patients and 32 healthy control subjects on diets containing 50 mmol and 200 mmol sodium per day. The increase in daytime diastolic blood pressure from 50 to 200 mmol sodium was significantly higher in the diabetic patients than in the control subjects (2.3±4.9 versus 0.2±3.7 mm Hg, P<.05). On a high sodium regimen, femoral artery distensibility was decreased in the diabetic patients compared with the control subjects (19.2±7.6 versus 24.1±9.3 10-3/kPa, P<.05). Angiotensin-converting enzyme inhibition in the diabetic patients on a high sodium diet decreased daytime diastolic blood pressure and increased femoral artery distensibility. The blood pressure decrease in response to angiotensin-converting enzyme inhibition correlated significantly with the blood pressure increase to sodium (for 24-hour systolic and diastolic blood pressure, r=.72, P<.001 and r=.76, P<.001). In addition, we found that in the diabetic patients on a high sodium diet, the renal blood flow response to exogenous angiotensin II was not bimodally distributed, as is the case in essential hypertension, in which a subgroup of the patients are characterized by sodium sensitivity of the blood pressure and an abnormal renal blood flow response to exogenous angiotensin II ("nonmodulator phenotype"). These results show that blood pressure in insulin-dependent diabetes mellitus is sodium sensitive, but that this is not related to the nonmodulator phenotype, and suggest that in IDDM a relatively high sodium intake may be a factor that predisposes to the development of diabetic vascular disease.
Key Words: diabetes mellitus, insulin-dependent • elasticity • renal circulation • angiotensin II • sodium
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Introduction |
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Microangiopathy in IDDM is associated with increased capillary pressure and flow, which may be caused by precapillary vasodilation in response to hyperglycemia.1 In addition, the regulation of capillary pressure in response to systemic blood pressure changes in IDDM may be impaired.1 Thus, small changes in systemic blood pressure might be important in the development of diabetic microangiopathy.1 2 It is unclear whether systemic blood pressure is elevated in short-term uncomplicated IDDM. Studies using 24-hour ABPMs have yielded conflicting results.3 4 5 6 Sodium intake was not reported in these studies. Differences in sodium intake might be responsible for some of the observed differences, especially because blood pressure in IDDM may be sodium sensitive.7 8 9
Arterial stiffness may also be sodium sensitive. Nondiabetic borderline hypertensive subjects who are sodium sensitive with regard to blood pressure have decreased arterial distensibility compared with sodium-resistant subjects.10 A decreased arterial distensibility, reflecting structural or functional alterations in the vascular wall, results in an increased systolic and a decreased diastolic blood pressure. It thus is a major determinant of an increased pulsatile pressure, which has implications for cardiovascular disease that are distinct from those of an elevated mean arterial pressure.11 Specifically, vascular stiffening may result in systolic hypertension,12 ventricular hypertrophy,13 and impaired myocardial perfusion,14 conditions that are common in the advanced stages of IDDM.15
We hypothesized that sodium sensitivity of blood pressure and of large artery properties might occur early during the course of IDDM, ie, before the development of micro- and macroangiopathy. To test this hypothesis, we studied whether blood pressure and large artery properties are sodium sensitive in patients with uncomplicated, reasonably well-controlled IDDM of short duration compared with healthy volunteers. In addition, we investigated whether, in IDDM, sodium sensitivity of blood pressure was related to the renal blood flow response to exogenous angiotensin II, analogous to sodium sensitivity in so-called nonmodulating essential hypertension, which is characterized by an abnormally small decrease in effective renal plasma flow (ERPF) in response to exogenous angiotensin II in the sodium-replete state.16 17 Finally, we investigated whether, in IDDM, the response of blood pressure (and of large artery properties) to short-term administration of an ACE inhibitor was related to the ERPF response to angiotensin II, as is the case in nonmodulating essential hypertension.18
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Methods |
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Subjects
We studied 32 patients with IDDM (onset before the age of 40 years and insulin dependency) and 32 healthy control subjects comparable for age, sex, and body mass index (Table 1
). Selection criteria for the patients
included normal urinary albumin excretion (<30 mg/24 h
on three occasions), normotension (<140/90 mm Hg), normal
fundoscopy, no clinical signs of neuropathy, and diabetes
duration of 7 years or less. Except for oral contraceptives (8 women in
the diabetic group and 7 in the control group) and insulin in the
diabetic group (mean, 43.9±19.7 U/d), no participant took any
medication with a known hemodynamic action. All
subjects performed a 24-hour urine collection for estimation of the
daily sodium intake on their regular diets. Hemodynamic
investigations were performed during three regimens (for logistical
reasons in the following order and with 2 to 10 days between the end of
the preceding and the beginning of the subsequent regimen), a high
sodium diet, a low sodium diet, and a high sodium diet in combination
with the ACE inhibitor perindopril. The high sodium diet
consisted of a 200 mmol sodium–containing regimen for at least 5
days (range, 5 to 8) and consisted of the regular diet with sodium
chloride supplementation if necessary. The low sodium diet consisted of
a 50 mmol sodium–containing regimen for at least 5 days (range, 5
to 8) and was prescribed by a dietician. Thereafter, a high sodium
intake as described above was combined with perindopril (4 mg once per
day) during the last 3 days (analogous to a protocol published
previously.18 A 24-hour urine collection was obtained on
the last day of each regimen. The hemodynamic
measurements were performed after at least 5 days of each regimen. For
reasons related to availability of equipment, the number of subjects
per study differs (Table 2). The protocol
was approved by the ethics committee, and informed consent was obtained
from all participants.
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Blood Pressure Measurements
ABPM was performed every 15 minutes from 7 AM to 11
PM and every 20 minutes from 11 PM to 7
AM with an oscillometric portable monitor (Spacelabs
90207). Daytime, nighttime, and 24-hour blood pressure values were
calculated as the means of the hourly averages of the 10- to 23-hour,
the 1- to 7-hour, and the 24-hour periods, respectively. These daytime
and nighttime periods provide reliable estimates of the true blood
pressure values during waking and sleeping.19 The
nocturnal decrease in blood pressure was defined as the difference
between daytime and nighttime divided by the daytime blood pressure.
There were no shift workers among the participants. Measurements were
performed on a normal working day. Analyses of the ABPM
profiles were performed by an observer unaware of the pertaining
regimen. Sodium sensitivity of blood pressure was defined as the
difference between the values recorded during the high and the low
sodium regimens. For comparison with results reported by
others,9 we also analyzed the data with a 3-mm Hg
increase in blood pressure during the high sodium regimen as the cutoff
for sodium sensitivity.
Arterial Distensibility
Distensibility parameters were obtained from the
right CCA and FA with a noninvasive vessel wall movement detector
system (Wall Track System, Neurodata), which consists of an ultrasound
imager (Ultramark IV, ATL) and a data processing unit capable of
measuring distensibility parameters with high accuracy and
precision.20 The participants refrained from smoking and
from the use of caffeine-containing beverages for at least 4 hours
before the start of the measurements, which were performed at the same
time of day in the IDDM and control groups. Blood pressure, pulse
pressure (dP, distending pressure), and heart rate were recorded on
the left arm with an automated device (BP-8800, Colin). Distensibility
coefficients (DC) and compliance coefficients (CC) were calculated from
end-diastolic diameter (D), arterial wall
distension during the heart cycle (dD), and dP (DC=2xdD/DxdP;
CC=
xdDxD/2xdP). The within-subject coefficients of variation for
D, DC, and CC are 3.1%, 7.7%, and 8.3% for the CCA and 3.8%,
17.0%, and 15.2% for the FA (J.L., M.A., unpublished data, 1993),
which are similar to those found by others using the same
method.21 The DC reflects the elastic properties of the
artery and the CC its buffering capacity. Many definitions of
arterial stiffness are used in the
literature.22 The formulas above are defined as fractional
change and change of vessel cross-sectional area, respectively. The DC
as defined above is the inverse of Peterson's elastic modulus, which
can be applied for arterial stiffness measurements in
vivo.23 Sodium sensitivity of DC, CC, and D was defined as
the difference between the measurements during the high and low sodium
regimens.
Renal Blood Flow
ERPF and GFR were determined using the urinary clearances of
131I-hippuran (IOH, Amersham) and
125I-iothalamate(IOT, Amersham), respectively;
day-to-day coefficients of variation are 5.0% and 2.2%,
respectively.24 25 Baseline values for GFR and ERPF were
calculated at 5.5 hours.24 25 Next, infusion with
angiotensin II (3 ng · kg-1 ·
min-1, Ciba-Geigy) was started, followed by calculation of
GFR and ERPF during angiotensin II infusion at 7.5 hours.
The diabetic patients arrived after having fasted and had not taken
their morning insulin injections. They refrained from smoking during
the experiment. The measurements started between 8 AM and 9
AM in the morning in a temperature-controlled room (23°C
to 24°C). The blood glucose level was clamped at 5 to 6
mmol/L with a constant insulin infusion at a rate of 1 U/h
(Velosulin, Novo Nordisk) and variable glucose 10% infusions,
because hyperglycemia can alter ERPF.26 Blood glucose
concentration was measured by a glucose oxidase method (Yellow Springs
glucose analyzer). The radioactivity concentrations of IOT and
IOH were determined by a well-type scintillation counter (1282
CompuGamma, LKB Wallac).
Analytical Methods
Glycated hemoglobin (HbA1c) was determined by
high-performance liquid chromatography (Bio-Rad
Laboratories BV, Veenendaal; normal range, 4.3% to 6.1%). Serum and
urine sodium concentrations were determined with an ion-selective
electrode after dilution (Boehringer Mannheim/Hitachi 747).
Serum and urine creatinine were determined by a modified
Jaffé method. Albuminuria was measured with
immunonephelometry (Array Protein System, Beckman Instruments).
Statistical Analysis
Results are expressed as mean±SD unless otherwise indicated.
The data were checked for a normal distribution. Two-sample Student's
t tests were used to compare the IDDM and the control
groups. One-sample t tests were used to compare the diabetic
patients before and after treatment with perindopril and to compare
data during high and low sodium intake in each group. Pearson's
coefficients were computed for correlation analysis where
appropriate. Two-sided values of P<.05 were considered to
be statistically significant. All statistical testing was performed
with the SPSS statistical software package 7.0 for Windows.
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Results |
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Table 3
shows that in both
groups, 24-hour blood pressure was higher during a high compared with a
low sodium regimen, except for DBP in the control subjects. In the IDDM
group, daytime SBP and DBP were higher during a high compared with a
low sodium intake; in the control group, nighttime SBP and DBP were
higher during a high compared with a low sodium intake. Nighttime SBP
and DBP during a low sodium intake tended to be higher in the IDDM than
in the control group (P=.12 and P=.08,
respectively). The increase in daytime DBP from a 50 to a 200
mmol/d sodium–containing diet was significantly greater in the
IDDM than in the control group (2.3±4.9 versus 0.2±3.7 mm Hg,
P<.05). For comparison,9 we repeated the
analyses with a 3-mm Hg increase in blood pressure during a
high sodium regimen as the cutoff point for sodium sensitivity. These
analyses yielded essentially the same results (prevalence of
sodium sensitivity of daytime DBP, 50% in the IDDM versus 25% in the
control group [P=.04]; no other statistically significant
differences). Sodium sensitivity of the blood pressure was not related
to body mass index. We found no differences in the percentage of
nocturnal decrease of the SBP or DBP (for either sodium regimen)
between the IDDM and the control groups.
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Figs 1 and 2 show that compliance and distensibility
of the FA, but not of the CCA, during a high sodium regimen were
significantly lower in the IDDM than in the control group. There were
no differences if the changes in DC and CC between a high and a low
sodium diet were compared between the groups. Table 3
shows that D and dD in the FA were
(nonsignificantly) smaller in the IDDM than in the control group but
that dP was greater. Reanalyzing arterial stiffness by
using the stiffness index,27 which might be less dependent
on blood pressure than the DC, yielded essentially the same results
(data not shown).
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During the ERPF, measurements >95% of the blood glucose values were
between 5 and 7 mmol/L. Table 4 shows ERPF, GFR, and filtration
fraction before and during angiotensin II infusion. The
decrease and percentage decrease in ERPF during angiotensin
II infusion were 158±46 mL/min per 1.73 m2 and
31.6±8.0%. Fig 3 shows that the
decrease in ERPF (in mL/min per 1.73 m2) during
angiotensin II infusion in the diabetic group was not
bimodally distributed. There was a trend toward an inverse relationship
between the percentage decrease in ERPF and the increase of the daytime
DBP on a high sodium diet (r=-.30, P=.12).
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In 19 diabetic patients on a high sodium diet, ACE inhibition was
associated with a decrease of the daytime DBP and with an increase of
the CC and the DC (Table 5). By using the
stiffness index,27 we found no difference between the
presence or absence of ACE inhibition in the carotid artery (6.35±1.54
versus 6.77±1.08, P=.11) or in the femoral artery
(10.75±5.14 versus 11.58±5.18, P=.26). In these patients,
sodium excretion during ACE inhibition did not differ from that without
ACE inhibition (219±72 versus 227±68 mmol/24 h,
P=.78). The increase of blood pressure on a high sodium diet
alone as compared with a low sodium diet (24-hour SBP, 1.4±6.1;
24-hour DBP, 1.8±5.0 mm Hg) correlated significantly with the
blood pressure decrease in response to ACE inhibition (24-hour SBP,
3.0±5.4; 24-hour DBP, 3.6±3.9 mm Hg; r=.72,
P<.001 and r=.76, P<.001,
respectively). There was no relation between urinary sodium excretion
during ACE inhibition and blood pressure response to ACE
inhibition.
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Discussion |
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This study demonstrates an increased sodium sensitivity of daytime DBP and an increased FA stiffness during high sodium intake in patients with uncomplicated, reasonably well-regulated IDDM of short duration compared with healthy control subjects.
An increased sodium sensitivity of the blood pressure in uncomplicated IDDM is supported by several observations. First, proximal tubular reabsorption of sodium, total body exchangeable sodium, and extracellular fluid volume are increased in IDDM.7 8 Second, in animal studies, sodium sensitivity has been shown to play a major role in the response of the blood pressure to insulin.28 IDDM patients are usually hyperinsulinemic; our data raise the possibility that treatment with insulin might contribute to sodium sensitivity of the blood pressure, particularly in insulin-resistant subjects. Finally, Strojek et al9 found in a group of normo- and microalbuminuric IDDM patients that MAP increased by 3 or more mm Hg in a significantly greater proportion of the IDDM than of the control subjects when changing from a low (20 mmol/d) to a high (220 mmol/d) sodium diet under inpatient conditions. Our study shows that also under outpatient conditions and with a smaller difference between a high and a low sodium intake, which was instituted in a sequence opposite to that of Strojek's study, blood pressure appears to be sodium sensitive in uncomplicated IDDM. Importantly, because of the short duration of diabetes in our study, sodium sensitivity is likely to be a feature of IDDM per se.
The mechanism of impaired sodium handling in IDDM is unclear. In nondiabetic essential hypertensive patients, a subgroup (the so-called nonmodulators) has been defined by an abnormal angiotensin II–mediated control of the ERPF, an abnormal renal sodium handling, and sodium sensitivity of the blood pressure.16 These nonmodulators can be easily identified because the ERPF response to angiotensin II during a high salt intake is clearly bimodally distributed between modulators and nonmodulators,18 the latter having an abnormally small decrease in ERPF. This characteristic is thought to be genetically determined,29 may be caused by inappropriately high intrarenal angiotensin II generation,18 and can be corrected by short-term ACE inhibition.18 Because diabetic nephropathy will develop in 30% to 40% of IDDM patients and clusters in families,30 we hypothesized, as have others,17 that the nonmodulating phenotype might predispose IDDM patients to hypertension and nephropathy. We therefore investigated the response of the ERPF to angiotensin II in the diabetic group but found no evidence of a bimodal distribution, no matter which of the proposed cutoff points (100 and 125 mL/min per 1.73 m2 decrease of the ERPF16 18 29 ) was applied. Moreover, the percentage decrease of the ERPF, which takes differences in baseline ERPF into account, also was not bimodally distributed (data not shown). We wished to investigate a possible bimodal distribution of the ERPF response to angiotensin II in IDDM and therefore limited these studies to the diabetic patients. Nevertheless, the response of the ERPF to angiotensin II in the IDDM group was in the same range as values in healthy control subjects reported elsewhere.16 31 Therefore, our results clearly do not support the hypothesis that abnormalities of blood pressure regulation in IDDM are related to the nonmodulator phenotype. In contrast, Fioretto et al17 did observe an impaired ERPF decrease in response to angiotensin II in 9 normoalbuminuric, normotensive diabetic patients compared with 8 normotensive controls. Our results in IDDM of short duration suggest that the nonmodulator status is not a feature of IDDM per se. The discrepancy between the results of Fioretto et al and our study might be explained by selection of the patients, eg, by the longer diabetes duration in that study, which may suggest that the nonmodulator status can be acquired.
Stiffening of large arteries results in an increased pulse pressure,12 which might modulate the sensitivity of the endothelial cells to shear stress,32 in turn accelerating atherosclerosis. Furthermore, vascular stiffening increases systolic vascular wall tension12 and ventricular workload13 and impairs coronary blood flow.14 Vascular stiffness is increased in type II diabetes mellitus,33 hypertension,34 and aging.35 Most but not all36 studies in normoalbuminuric IDDM have reported vascular stiffness to be either increased or similar to that in healthy control subjects.37 38 39 40 Differences in sodium intake, which was not reported in these studies, may in part explain the divergent results. The difference between FA and CCA DC and CC in the present study is in agreement with our previous study in uncomplicated IDDM patients (on a regular diet, presumably about 200 mmol sodium/d), in whom we observed stiffness to be increased in the FA but normal in the CCA,37 and with results obtained by others.39 Importantly, our results show FA stiffness in early, otherwise uncomplicated IDDM to be increased and to be modulated by dietary sodium intake. Our data show a trend in the same direction for healthy control subjects. Although the change in arterial stiffness from a low to a high sodium diet did not differ significantly between the IDDM and the control groups, this does not detract from the fact that compliance and distensibility of the FA on a high sodium regimen were decreased in the diabetic patients. This may contribute to the higher incidence of macrovascular disease in IDDM because in a regular Western diet the sodium content approximates 200 mmol/d. We were unable to distinguish between a blood pressure–related decrease in arterial distensibility and other possible mechanisms, such as a direct effect of sodium on the viscoelastic properties of the vascular wall, as has been suggested in sodium-sensitive essential hypertension.10 In addition, in healthy subjects, aortic stiffness, estimated from pulse wave velocity, has been shown to decrease during a low sodium intake, an effect that was independent of blood pressure.41 Our data show a similar trend in the control subjects. As noted, in the IDDM patients the decrease in arterial distensibility during a high sodium intake was more prominent in the FA than in the CCA, a difference that may also suggest mechanisms that are in part independent of pressure. For example, sodium loading may increase intracellular calcium concentration in vascular smooth muscle cells, which may result in an increased vascular tone being more prominent in the muscular FA than in the elastic CCA. Alternatively, differences in pulse wave amplification, which are influenced by differences in blood pressure level,42 between the FA and CCA during a high sodium intake might also explain the divergent results for the DC and CC in these arteries.
In the IDDM patients, ACE inhibition was associated with a decrease in the elevated daytime DBP and an increase in arterial distensibility and compliance in both the CCA and FA, even in the presence of a sodium load. The increased distensibility and compliance seem to be caused by the decreasing blood pressure during ACE inhibition, because the stiffness index, which is less dependent on blood pressure,27 was not different with or without ACE inhibition in the CCA and FA.
Limitations of our study include the fixed sequences of high and low sodium–containing diets, although the opposite order of regimens resulted in comparable effects on blood pressure.9 The study also was not blinded, but the observer who performed the analyses of the ABPM profiles was. Blood pressure measurements were performed at the brachial artery and may not reflect the local distending pressure in the CCA and the FA. However, this is likely to result in a systematic error and thus does not detract from our conclusion that increased sodium intake may have a more adverse effect on the vasculature in IDDM patients than in control subjects. Finally, autonomic nerve function tests were not performed. However, disturbances in autonomic function resulting in changes in blood pressure regulation are unlikely in patients with diabetes of short duration. We therefore think that these limitations do not detract substantially from our main findings, ie, that arterial distensibility of the muscular FA is lower during a high salt intake and that blood pressure is sodium sensitive in uncomplicated IDDM of short diabetes duration. These results emphasize the possible beneficial effects of sodium restriction in normotensive, normoalbuminuric IDDM patients.
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This work was supported by a grant from the Dutch Prevention Fund (Het Praeventiefonds). C.D.A.S. is supported by a Clinical Research Fellowship from the Diabetes Fonds Nederland (Diabetes Research Fund) and the Netherlands Organisation for Scientific Research (NWO). We thank Servier Netherlands for financial support of the Wall Track System.
Received January 27, 1997; first decision February 10, 1997; accepted April 25, 1997.
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