Journal of Human Hypertension (1999) 13, 179–183

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ORIGINAL ARTICLE
Baroreflex control of heart rate is impaired
in pre-eclampsia
P Molino1, F Veglio1, G Cat Genova1, R Melchio1, C Benedetto2, L Chiarolini2,
F Rabbia1, T Grosso1, P Mulatero1 and L Chiandussi1
1
Department of Medicine and Experimental Oncology, and 2Department of Obstetric and Gynecology,
University of Turin, Italy

Autonomic nervous dysfunction, such as parasympa- cross-spectral analysis of systolic blood pressure and
thetic and sympathetic impairment, has been suggested pulse interval. The result was that baroreflex gain at rest
as possible cause of pre-eclampsia, but the studies are was lower in pre-eclamptic women both compared to
not conclusive. Our purpose was to assess non-invas- non-pregnant and healthy pregnant subjects (P ⬍ 0.05).
ively if pre-eclampsia is associated with a decreased Moreover, a decrease of the baroreflex sensitivity was
baroreflex function. Nine women with pre-eclampsia present in all pregnant women in the orthostatic pos-
(PE), eight normotensive pregnant women, and seven ition (P ⬍ 0.05). In conclusion pregnancy per se is asso-
healthy normotensive non-pregnant women were stud- ciated with a decrease in the baroreflex control of the
ied. Continuous finger blood pressure was recorded by heart, whereas in pre-eclampsia, the baroreflex sensi-
a Portapres device in the left lateral recumbent position tivity is impaired further.
and active standing. Baroreflex gain was evaluated by

Keywords: baroreflex; autonomic nervous system; pre-eclampsia

Introduction The interest in baroreflex activity is due to the

blood pressure lability and enhanced responsive-
Pre-eclampsia is a multisystemic disorder of preg- ness to angiotensin that characterises pre-eclampsia,
nancy characterised by proteinuria, and a marked which could reflect, at least in part, baroreflex dys-
increase in peripheral vascular resistance, which, in function.7 Furthermore, in pre-eclampsia the endo-
turn, causes an increase in blood pressure. The
thelial dysfunction may represent a possible cause
pathophysiological mechanism is still unknown,
of the baroreflex sensitivity impairment.8,9
although some reports suggest an autonomic ner-
The aim of our study was to assess non-invasively
vous dysfunction such as sympathetic and parasym-
the baroreflex sensitivity in pre-eclamptic patients
pathetic impairment.1–3 Most studies have investi-
gated autonomic nervous function by non-invasive (PE) compared to normal pregnant, and normotens-
evaluations using standard cardiovascular tests (ie, ive non-pregnant women. The study was performed
deep breathing, standing up, cold pressure tests and with the Portapres device, a portable battery-oper-
Valsalva manoeuvre), or by measuring the sympath- ated device for the continuous non-invasive
etic nerve activity in the blood vessels of the skeletal measurement of blood pressure in the finger.10
muscle with intraneural microelectrodes.1 Few stud- Power spectral analysis of arterial blood pressure
ies used spectral analysis of blood pressure and and interbeat interval was performed in the fre-
heart rate variability to evaluate autonomic nervous quency domain; this represents a powerful and non-
system function in pre-eclampsia and pregnancy- invasive tool which appears to provide a quantitat-
induced hypertension, showing conflicting results ive evaluation of the efferent arc of the autonomic
ranging from decreased vagal control of the heart to nervous system activity modulating cardiac function
increased sympathetic and parasympathetic control and systemic circulation, allowing the dissection of
of heart rate and blood pressure.2,4,5 In addition, the effects of the sympathetic and parasympathetic
baroreflex control has not been investigated to date sections of the autonomic nervous system on the
in a dynamic way, by the frequency domain cardiovascular function. When applied to the heart
approach, such as cross-spectrum analysis and cal- rate, power spectral analysis allows for the detection
culation of ␣-index, which has become a useful and of the low frequency component (LF, marker of sym-
non-invasive assessment of the spontaneous barore- pathetic activity), and of the high frequency compo-
flex gain.5,6 nents (HF, related to the respiratory activity, which
is mediated by the vagus nerve).11–14 The ratio
between the LF and HF components (LF/HF) is,
Correspondence: Dr Franco Veglio, Cattedra di Medicina Interna, therefore, an index of the sympatho-vagal balance.15
Ospedale San Vito, Strada San Vito 34, 10133 Torino, Italy
Received 5 November 1998; revised and accepted 31 December
1998
 Baroreflex in pre-eclampsia
P Molino et al

180
Materials and methods beat basis, according to the arterial volume-clamp
method of Penaz.17–19
Subjects
Twenty-four women were analysed: nine PE Computations of haemodynamic parameters
women; eight normotensive pregnant women
matched for age, week of gestation and body weight Data were analysed by the Beatfast program (TNO,
with the pre-eclamptic women; and seven healthy Amsterdam, NL) to identify systolic and diastolic
normotensive non-pregnant women of similar age blood pressure values and interbeat intervals for
(Table 1). each cardiac cycle: after digital low pass filtering at
Pre-eclampsia was defined according to the cri- 17 Hz, systolic blood pressure is stored as the high-
teria of the International Society for the Study of est pressure level during the ejection. Diastolic
Hypertension in Pregnancy:16 no previous history of blood pressure is arterial end-diastolic pressure just
hypertension, cardiovascular or renal disease before before the next upstroke begins. Interbeat interval is
pregnancy; blood pressure values exceeding 140/90 the time difference between two following systolic
mm Hg after the 20th week of gestation, confirmed pressures.
by two consecutive readings at least 6 h apart; pro-
teinuria ⬎0.300 g/dei.
Spectral analysis and baroreflex gain
The PE women were hospitalised because of an
increase in blood pressure in the third trimester; A stationary sequence of 5 min (about 300 to 500
none of these received antihypertensive medication. data points), for left lateral recumbent and upright
The patients were normotensive before the actual position, was analysed.15 Mean values of systolic
pregnancy and during eventual previous pregnancy. and diastolic blood pressure, and interbeat interval
Normotensive pregnant and all normotensive non- were calculated. Power spectral analysis of these
pregnant women were members of the medical staff. parameters was performed in the frequency domain
None of these women had histories of hypertension, by an autoregressive method (Burg method) using
cardiovascular or renal disease, or were taking anti- custom software implemented on MATLAB pro-
hypertensive medication. gram, after linear interpolation of data at 1 Hz fre-
There was no statistical difference of the body quency (to obtain equispaced data) and detrending.
mass index (BMI) in all studied patients before preg- The order of the autoregressive method was chosen
nancy. All pregnant women gave their informed by Akaike criterion for values ⬎15, whereas it was
consent to participate in the study, that was considered =15 if lower than 15.
approved by our Ethical Commitee. The total power was divided into low frequency
(0.025–0.14 Hz) and high frequency (0.14 –0.4 Hz)
components, markers respectively of sympathetic
Protocol and signal recordings
and parasympathetic activity. The power is
The study was performed in a quiet room between expressed in normalised units, which are obtained
2 pm and 5 pm, at least 2 hours after a meal. At first by dividing the power of each component by total
the subjects were studied in the left lateral recum- variance from which direct current has been sub-
bent position: after 20 min of bed rest, continuous tracted, and multiplying this value by 100.15
finger blood pressure was recorded for 15 min by To assess the statistical link between heart rate
Portapres Model-2 device (TNO, Amsterdam, NL) at and systolic blood pressure series at any given fre-
200 Hz sampling frequency. Then the procedure was quency, coherence was measured. Cross-spectral
repeated, using the same finger, during 10 min of analysis was performed by means of bivariate auto-
orthostatic position. regressive identification and was used to compute
Portapres is a portable, battery-operated device for a squared coherence function (ie, the square cross-
the continuous, non-invasive, 24-h ambulatory spectrum amplitude normalised by the product of
measurement of blood pressure in the finger.10 It is the spectra of the two signals). Coherence is
based on the Finapres, a stationary device for the expressed as a number between 0 and 1 and only
measurement of finger arterial pressure on a beat-to- values ⬎0.5 were considered significant. In our

Table 1 Clinical data of the studied groups

Non-pregnant Healthy pregnant Pre-eclamptic pregnant

(n = 7) (n = 8) (n = 9)

Age (years) 27 (26–33) 31 (30–34) 32 (29–33)

BMI (kg/m2) 20.43 (19.69–22.10) 27.23 (24.14 –31.21)* 27.11 (26.56–30.29)*
Week of gestation — 32.5 (28.5–36.5) 35.0 (32.0–36.0)
Proteinuria (g/d) 0 0 2.4 (1.8–3.4)
Primigravida (No. of women) — 6 7
Systolic blood pressure at rest (mm Hg) 118.30 (112.60–124.58) 109.85 (95.15–117.22) 151.80 (142.00–154.90)*†
Diastolic blood pressure at rest (mm Hg) 61.23 (51.40–67.80) 56.41 (48.11–64.44) 94.21 (83.38–100.06)*†
Resting heart rate (bpm) 69.9 (64.46–72.74) 87.35 (84.11–89.59)* 88.67 (77.60–89.50)*

Data are expressed as Median (25th centile–75th centile). *P ⬍ 0.05 vs non-pregnant, †P ⬍ 0.05 vs healthy pregnant by Mann–
Whitney test.
 Baroreflex in pre-eclampsia
P Molino et al

181
patients coherence was always ⬎0.5, either in rest towards lower ␣-index values in the healthy preg-
and upright position. nant group at rest compared to non-pregnant
The baroreflex gain was computed as alpha index, women. The ␣-index decreased in all groups after
ie the square root of the ratio of the powers of standing, but this reduction was significant only in
interbeat interval in the low frequency range to cor- non-pregnant and normal pregnant women. In all
responding spectral components of systolic blood pregnant women the ␣-index in the upright position
pressure, if coherence was ⬎0.5: was significantly lower than in non-pregnant
␣-index =
women.
冑low frequencyinterbeat interval/low frequencysystolic blood pressure
Spectral components of IBI variability
Low and high frequency, expressed in normalised
Statistical analysis units, did not differ between the groups, in the
Data are expressed as median (25th–75th centile). resting position.
Statistical evaluation was performed by Statistical In orthostatic position, all pregnant women
Analysis System (SAS Institute Inc, Cary, NC, USA). showed significantly lower low frequency values
For comparison of unpaired data, a non-parametric than non-pregnant women, whereas high frequency
analysis of variance (Kruskal–Wallis test) was first were significantly higher compared to non-pregnant
used followed by the Mann–Whitney test in case of women. Low frequency increased and high fre-
significance. For comparison of paired data, a Stud- quency decreased significantly after standing only
ent’s t-test for paired data was used. Differences in non-pregnant women.
were considered significant at P ⬍ 0.05. The LF/HF ratio was similar in all groups at rest;
it significantly increased after standing only in non-
Results pregnant women, whereas it was unchanged com-
pared to the resting position in all pregnant groups
Main clinical and haemodynamic parameters are and significantly lower compared to non-pregnant
shown in Table 1. Systolic and diastolic blood press- women.
ure were significantly higher in PE women, com-
pared to non-pregnant and normal pregnant women.
Heart rate was significantly higher in normal preg- Spectral components of blood pressure variability
nant and PE women compared to non-pregnant A comparison between the non-pregnant women
women. BMI was significantly lower in non-preg- and the two pregnant groups, showed no significant
nant women compared to other groups. differences in systolic and diastolic blood pressure
Table 2 summarises data on baroreflex gain and variability with respect to high frequency or low fre-
spectral analysis of pulse interval and blood press- quency bands, both in the recumbent and ortho-
ure variability. static position.
Baroreflex gain
Discussion
The ␣-index was significantly lower in PE women
at rest if compared both to normal pregnant and non- The major finding of the present study is the
pregnant women (Table 2). There was a trend decrease of the baroreflex gain, measured as ␣-index,
Table 2 Baroreflex gain and power spectral analysis of interbeat interval and blood pressure variabilty

Non-pregnant (n = 7) Healthy pregnant (n = 8) Pre-eclamptic pregnant (n = 9)

Rest Standing Rest Standing Rest Standing

BRG
(␣-index) (ms/mmHg) 12.16 (9.02–19.17) 10.22 (8.21–15.36)‡ 7.98 (6.71–9.93) 5.70 (5.24 –7.18)*‡ 5.60 (5.25–6.90)*† 4.07 (3.70–6.92)*

IBI variability
LF power (ms2) 1235 (754 –1799) 3181 (1664 –6052) 388 (268–620) 686 (310–1016)* 488 (361–769) 690 (455–715)*
HF power (ms2) 906 (194 –1084) 346 (290– 462) 371 (155– 492) 323 (170–547) 194 (101– 486) 336 (281– 456)
LF (NU) 0.62 (0.50–0.76) 0.89 (0.69–0.91)‡ 0.48 (0.35–0.76) 0.62 (0.47–0.76)* 0.62 (0.47–0.69) 0.56 (0.48–0.66)*
HF (NU) 0.35 (0.22–0.48) 0.08 (0.06–0.19)‡ 0.31 (0.16–0.56) 0.29 (0.15–0.45)* 0.30 (0.23–0.40) 0.27 (0.27–0.45)*
LF/HF 1.80 (1.05–3.42) 10.94 (3.78–13.27)‡ 1.53 (0.63–5.08) 2.23 (1.12–5.03)* 2.03 (1.14 –2.88) 2.04 (1.04 –2.44)*

SBP variability
LF power (mm Hg2) 6.9 (3.2–15.9) 24.6 (17.7–29.5) 8.2 (6.4 –13.4) 14.1 (11.6–23.7) 14.0 (9.6–16.1) 37.3 (29.7– 41.8)‡
HF power (mm Hg2) 1.5 (1.0–2.5) 4.3 (3.5–11.1)‡ 2.6 (1.5–3.6) 7.0 (3.5–10.5) 1.5 (1.1–3.8) 7.9 (5.1–9.1)‡

DBP variability
LF power (mm Hg2) 7.5 (3.8–8.3) 13.0 (5.1–14.3) 2.9 (2.5–3.7) 6.7 (4.6–9.8) 4.8 (32.–6.9) 15.1 (10.8–15.3)‡
HF power (mm Hg2) 0.7 (0.2–1.0) 2.4 (1.1–2.9)‡ 0.9 (0.6–1.4) 1.3 (1.1–3.3) 1.1 (0.9–1.5) 3.0 (2.1–3.9)‡

Data are expressed as Median (25th centile–75 centile).

*P ⬍ 0.05 vs non-pregnants, †P ⬍ 0.05 vs healthy pregnants by Mann–Whitney test; ‡P ⬍ 0.05 vs rest by Student’s t-test.
BRG: baroreflex gain; IBI: interbeat interval; SBP: systolic blood pressure; DBP: diastolic blood pressure; HF: high frequencies; LF: low
frequencies; NU: normalised Units.
 Baroreflex in pre-eclampsia
P Molino et al

182
in pre-eclampsia, compared to non-pregnant and quence rather than a precursor of severe pre-eclamp-
healthy pregnant women. Furthermore, in pregnant sia, which cannot be demonstrated as an impair-
groups we showed a reduction of the baroreflex gain ment of spectral components in early stages of the
in the orthostatic position compared to non-preg- disease. This could explain why our patients
nant women. These results provide evidence that showed an impaired sympathovagal balance only
pregnancy per se is associated with a decrease of the after standing: this simulus might point out an alter-
baroreflex sensitivity, but this is further impaired in ation which is not still evident in basal conditions.
pre-eclamptic subjects. Previous attempts to study autonomic nervous
Several studies concerning baroreflex function in system function by means of plasma and urinary cat-
pregnant women reported conflicting results.20–23 echolamine concentrations did not give conclusive
On the contrary, many animal studies24,25 showed results.23,30,31 A substantial increase in sympathetic
pregnancy to be associated with an impaired barore- vasoconstrictor activity has been found by Schobel
flex sensitivity, and an attenuated ability to increase et al,1 measuring the postganglionic sympathetic-
sympathetic outflow above baseline levels during a nerve activity in the blood vessels of skeletal mus-
hypotensive challenge. cle. Since five of the nine pre-eclamptic patients
On the other hand, it is known that in hyperten- received dihydralazine at the time of the study, we
sive humans and animals there is a diminished baro- have to assume that pre-eclampsia was at a greater
reflex control of the heart,26 which may be due to a level of severity than in our patients. Moreover, the
reduction in the vagal range.27 Furthermore, endo- use of a direct vasodilator per se may be a stimulus
thelial dysfunction and altered release of paracrine to enhance sympathetic activity.
factors contribute significantly to the decreased The method we used in this study allows the
baroreceptor sensitivity in hypertension and athero- dynamic assessment of the baroreceptor heart rate
sclerosis.28 Previous studies have described a vascu- reflex, and evidence in both animals and humans
lar endothelial dysfunction in pre-eclampsia, with indicates that this reflex function may not always
decreased vasodilatatory prostacyclin and increased reflect baroreceptor control of peripheral circulation
vasoconstrictor thromboxane synthesis.7 In and blood pressure.32,33
addition, there is evidence for placental release of Also in normal pregnancy, several human and
circulating substances able to alter endothelial animal studies have demonstrated an impairement
cells,8 with a reduced production of vasodilatatory of both vagal and sympathetic functions, which
autocrine and paracrine factors such as nitric oxide have been found to be variably altered.34
and prostacyclin.29 Hence a loss of the excitatory In our study, non-pregnant women showed an
influence of endogenous prostanoids in pre-eclamp- increase in low frequency and a decrease in high
tic women could represent a possible mechanism for frequency components of heart rate variability with
the impaired baroreflex gain found in our study.
standing indicating a stimulation of the sympathetic
Studies concerning autonomic nervous function
nervous system, whereas in all pregnant women the
in pre-eclampsia have reported inconclusive results.
increase was not significant. Moreover, in ortho-
A study which used spectral analysis showed a sig-
static position heart rate and diastolic blood press-
nificant reduction of high frequency of interbeat
ure variability of healthy pregnants were lower com-
interval variability, indicating that pre-eclampsia is
associated with decreased vagal control of the pared to non-pregnant women, confirming the
heart.2 On the contrary, Ekholm et al4 showed possibility of changes in the baroreflex control and
increased heart rate and blood pressure variability increased maternal blood volume to be involved.20
in women with pregnancy-induced hypertension Nevertheless, in our study, normal pregnant and
and proteinuria, suggesting increased of both sym- pre-eclamptic women showed significantly
pathetic and parasympathetic components. The dis- increased heart rate with standing, also if the
cordant results could be due both to the different increase was lower compared to non-pregnant
conditions of breathing (spontaneous and controlled women (9.8% and 13.8%, vs 21.9%, respectively).
breathing respectively) and to the different order of In conclusion, the innovative aspect of our study
the autoregressive method chosed for the spectral was the assessment of the baroreflex function in nor-
analysis; besides the two groups of pre-eclamptic mal pregnancy compared to pre-eclamptic women,
women studied showed unlike values of resting by a non-invasive method, such as ␣-index calcu-
heart rate. lated on finger blood pressure measurement. This
In our study no differences between the groups method provides a global quantification of the spon-
were present at rest regarding blood pressure and taneous baroreflex control of heart rate, avoiding
heart rate variability. When the orthostatic position most of the limitations of pharmacological methods,
was assumed pre-eclamptic women showed a and requiring little subject cooperation or stress.
reduction in the low-frequency and an increase in Therefore, it is of great utility in patients such as
the high-frequency components of the heart rate pre-eclamptic women, in which the avoidance of
variability and the LF/HF ratio was also reduced stress is an important part of the therapy.
compared to non-pregnant women. Finally, we think that longitudinal studies will be
Airaksinen et al3 showed a decreased resting vagal useful to evaluate if the baroreflex function is
activity in normal pregnancy, and only in severe restored after delivery and if it could provide prog-
pre-eclampsia were both the sympathetic and para- nostic information to enable the early identification
sympathetic reflexes impaired. The authors suggest of pregnant women at greater or probable risk to
that autonomic nervous dysfunction is a conse- develop pre-eclampsia.
 Baroreflex in pre-eclampsia
P Molino et al

183
Study limitations ment, physiological interpretation, and clinical use.
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