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(Hypertension. 1997;30:603.)
© 1997 American Heart Association, Inc.
Articles |
Circadian Blood Pressure Variability in Healthy and Complicated Pregnancies
From the Bioengineering and Chronobiology Laboratories, ETSI Telecomunicación, University of Vigo, Campus Universitario, Vigo (D.E.A., R.C.H., A.M., J.R.F.); and the Obstetrics and Gynecology Department, Hospital General Clínico Universitario de Galicia, Medical School, University of Santiago, Santiago de Compostela (M.I.), Spain.
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Abstract |
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Abstract With the aim to describe the circadian pattern of noninvasive ambulatorily monitored blood pressure during the trimesters of pregnancy in clinically healthy women as well as in pregnant women who developed gestational hypertension or preeclampsia, we analyzed 759 blood pressure series sampled by ambulatory monitoring for about 48 hours every 4 weeks after the first obstetric visit in 71 women with uncomplicated pregnancies, 28 with gestational hypertension, and 14 with preeclampsia. The circadian pattern of blood pressure variation for each group (complicated versus uncomplicated pregnancies) and trimester of gestation was established by linear least-squares methods. A highly statistically circadian pattern is demonstrated for systolic and diastolic blood pressure for both groups of pregnant women in all trimesters (P<.001 in all cases). Blood pressure decreases from the first trimester to the second and rises again in the third for healthy pregnant women. For women who developed gestational hypertension or preeclampsia, blood pressure is stable during the first half of pregnancy and then continuously increases until delivery. The differences in circadian rhythm-adjusted mean between complicated and uncomplicated pregnancies are highly statistically significant in all trimesters (always P<.001). This study confirms and extends to ambulatory everyday life conditions the predictable circadian variability in blood pressure during gestation. The differences in blood pressure between healthy and complicated pregnancies can be observed as early as the first trimester of pregnancy. Those differences are found when both systolic and diastolic blood pressures for women with a later diagnosis of gestational hypertension or preeclampsia are well within the accepted normal physiological range of blood pressure variability.
Key Words: blood pressure • circadian rhythm • pregnancy • hypertension, gestational • preeclampsia
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Introduction |
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Isolated BP measurements during the second trimester perform poorly in selection of a population for potential detection of preeclampsia.1 2 3 4 5 6 Despite this, isolated BP measurement is the mainstay of the diagnosis of preeclampsia. However, the variability of BP, even among healthy individuals, is such that the identification and the proper definition of high BP is highly ambiguous when based mainly on single time-unspecified measurements. Even when based not on one or two but on a mean of several casual rather than systematic measurements, a BP value found to be "high" or "low" is often unreliable.7 This is due to both the large variability of BP and the circumstance that unusually high or low values may occur only at certain times that may not be covered by casual sampling,8 as in the case of nightly hypertension. While the differences between SBP and DBP have long been recognized and utilized, it is often not realized that the DBP at a given time can be higher than the SBP measured in the same person at another time on the same day.9 Both SBP and DBP vary in adulthood, on the average more than 50 mm Hg within each day.9 10 11 Such circadian BP variability also characterizes clinically healthy pregnant women, as well as pregnant women who develop gestational hypertension or preeclampsia. During gestation, another source of variability comes from the predictable pattern of BP changes during pregnancy.12 13 In clinically healthy pregnant women, BP steadily decreases up to the middle of gestation and then increases up to the day of delivery, with final BP values similar to those found early in pregnancy in the same women. Women with gestational hypertension or preeclampsia are characterized, however, by a continuous linear increase of BP with gestational age throughout the second half of pregnancy.13
Changes in circadian variation of BP may be used either to predict preeclampsia or to assess its severity.14 Although reference values are now available for 24-hour ABPM in nonpregnant patients,10 11 15 only a few studies have been made of the normal pattern of ABPM in uncomplicated pregnancies,16 17 18 19 20 21 but without comparison with the circadian pattern of BP in complicated pregnancies, an issue only occasionally addressed.14 20 22 Against the background of reliance on casual BP measurements for the diagnosis of preeclampsia, the approach of (1) evaluating the circadian predictable variability in BP for both uncomplicated and complicated pregnancies by the use of portable, noninvasive, and fully automatic devices and (2) the proper processing by chronobiologic methods of the time series thus obtained can be useful in assessing early cardiovascular disease risk in pregnancy. We have used this approach to examine and compare characteristics of circadian variability in the BP of clinically healthy pregnant women as well as women with gestational hypertension and preeclampsia who were systematically monitored during their pregnancies.
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Methods |
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Subjects
We studied 113 white pregnant women (71 with uncomplicated pregnancies, 28 who developed gestational hypertension, and 14 who developed preeclampsia, here defined as gestational hypertension and proteinuria, above 300 mg/24 h in urine, with or without edema). All women received obstetric care at the Obstetric Physiopathology Unit, Hospital General Clínico Universitario de Galicia, Santiago de Compostela, Spain. All issues related to ABPM, including handling and preparation of the monitors, individualized explanation about their use to each patient, and processing of the data provided by any given pregnant woman after monitoring, were always carried out by the same members of the research group in one room of the unit. Conventional obstetric examinations of the pregnant women, usually done on the same day just before starting ABPM, were carried out by other members of the research group in different rooms of the unit. Diagnosis of gestational hypertension (conventional BP values above 140/90 mm Hg for SBP/DBP without clinical record of hypertension previous to pregnancy) or preeclampsia (as defined above) was made using information from the conventional obstetric examinations and routine analyses of urine. Inclusion criteria were absence of any condition requiring the use of antihypertensive medication, age (18 to 40 years), and gestational age (less than 16 weeks at the time of inclusion). Exclusion criteria were, among others, multiple pregnancy, chronic hypertension, chronic liver disease, any disease requiring the use of anti-inflammatory medication, diabetes, and any other endocrine disease such as hyperthyroidism, as well as the inability to tolerate the use of an ambulatory BP monitor. The Ethical Committee of Clinical Research from the Medical School approved the study. All volunteers signed consent forms before entering the study.
BP Assessment
The SBP and DBP of each subject were automatically monitored
every 30 minutes during the day (9 AM to 10 PM)
and hourly during the night for 48 hours with an ABPM-630 Colin device
at the time of recruitment, and then every 4 weeks until delivery. BP
series were eliminated from analysis when they showed an
irregular schedule during the days of sampling, an odd sampling with
spans of more than 3 hours without BP measurement, or a night resting
span shorter than 6 hours or longer than 12 hours. The total number of
BP series provided by the women under investigation fulfilling all
mentioned requirements set a priori was 759. During sampling, all
women were living on their usual diurnal waking (
7:30 AM
to 12 PM for most subjects) and nocturnal resting
routine, following everyday life conditions with minimal restrictions.
They were told to follow a similar schedule during the days of sampling
and to avoid the use of medication for the duration of the trial. The
clinical evaluation of the monitor according to the standards published
by the Association for Advancement of Medical
Instrumentation23 has been previously
established.18 24 The BP cuff was worn on the nondominant
arm. ABPM was performed in addition to the woman’s routine antenatal
care, and no person was hospitalized during monitoring. Cuff size was
determined by upper arm circumference at the time of each visit. ABPM
always started between 10 AM and 1 PM. During
monitoring, each subject maintained a diary regarding information about
their activity cycle, dietary consumption, physical activity, emotional
state, and other external or internal stimuli possibly affecting
BP.
The Colin instrument uses both an oscillometric and an auscultatory (Riva Rocci-Korotkoff) method to assess BP. Since the oscillometric approach is usually more sensitive, there were fewer missing values (due to arm movement or environmental noise) with the oscillometric than auscultatory measurements. Moreover, when relying on the oscillometric measurements, the exact positioning of the cuff over the brachial artery is not critical. Consequently, a patient can take the cuff off, for example, to take a shower, exercise, or recharge the battery, and then replace it. The ability of the oscillometric technique to take accurate measurements in noisy environments and in the presence of a significant degree of respiration artifact is a further advantage. Therefore, the results reported here focus on the oscillometric measurements.
Statistical Methods
Original oscillometric data from each BP series were first
synchronized according to the rest-activity cycle of each individual by
recomputing all times of sampling in hours from bedtime to avoid
differences among subjects in actual times of daily activity and to
express results in circadian time rather than in less meaningful clock
hours. After synchronization, BP values were edited according to
commonly used criteria for the removal of outliers and measurement
errors.8 25 The remaining data were analyzed by
the use of Chronolab,26 a software package for biological
signal processing by linear and nonlinear least-squares estimation
that, among others, includes the single and population-mean
cosinor methods.27 Circadian
parameters were subsequently compared between groups of
women (complicated and uncomplicated pregnancies) in each trimester of
pregnancy, with a parameter test developed for comparison
of rhythm characteristics obtained from population-mean cosinor
analysis (Bingham test27 ).
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Results |
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For the normotensive pregnant women, no difference was found between circadian BP characteristics obtained as a function of parity or age for any trimester of pregnancy. Data from the whole database were therefore pooled for subsequent analysis and only divided according to gestational age and pregnancy outcome. Circadian rhythm parameters obtained first by the single cosinor method for each individual BP profile were used to obtain group characteristics separately in each trimester of pregnancy (in keeping with the documented predictable variability of BP with gestational age12 13 ). The parameters of the circadian rhythm (obtained by population-mean cosinor) for SBP and DBP in each trimester of pregnancy for clinically healthy women as well as for pregnant women with a final diagnosis of gestational hypertension or preeclampsia are indicated in the tables at the bottom of Figs 1 through 3. Compared with uncomplicated pregnancies, a statistically significant elevation of the circadian rhythm-adjusted mean (MESOR, average value of the rhythmic function fitted to the data) of BP is found in pregnancies with gestational hypertension or preeclampsia in all trimesters (P<.001 for both SBP and DBP from the Bingham test27 ). There is also a statistically significant difference in the circadian amplitude (difference between the maximum and the MESOR of the fitted curve) of both SBP and DBP between uncomplicated and complicated pregnancies in all trimesters of gestation (P<.002 for both variables in all trimesters).
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P value from testing the zero amplitude assumption. AMP
indicates amplitude, difference between the maximum and the MESOR of
the fitted curve (in mm Hg); ACR, acrophase, lag from a defined
reference time point (here, bedtime) of the crest time in the cosine
curve fitted to the data (in angular degrees, with 360°=24 hours);
and C.I., 95% confidence intervals. The cosine curve
represented for each group corresponds to the best fitted
model obtained by population-mean cosinor (with corresponding
characteristics given in the table below each chronogram). The arrows
from the upper horizontal axis indicate the circadian acrophases for
each group.
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The elevation of SBP and DBP during the first trimester of pregnancy in subjects with a later diagnosis of gestational hypertension or preeclampsia compared with clinically healthy pregnant women is shown in Fig 1. This figure represents a circadian population chronogram (display of data as a function of time), with 2-hourly means and standard errors of data computed as follows: First, 2-hourly means are computed from each individual series, after stacking all data sampled during a 48-hour monitoring span in only one idealized 24-hour span (given the highly statistically significant rhythm with a period of 24 hours demonstrated in about 94% of all BP series studied). In a second step, the average of those individual means at each interval is computed averaging across the total number of series for any given population. The lower horizontal axis represents circadian time in hours after bedtime; the resting span is indicated by the dark bar in the lower horizontal axis. The cosine curve represented for each group corresponds to the best fitted model obtained by population-mean cosinor applied to all original BP values (not just to the 2-hourly means). The arrow from the upper horizontal axis indicates the circadian acrophase (lag from a defined reference time point of the crest time in the curve fitted to the data) for each group. The values of acrophase, in angular degrees, are computed taking bedtime as the circadian reference time point. Statistically significant differences between means for each group (detected by t test not adjusted for multiple testing) at any given interval are indicated by an asterisk above the lower horizontal axis. Differences in rhythm characteristics (as is the case here for the circadian MESOR and amplitude), as well as the general waveform of circadian variability in SBP and DBP, can be readily seen from this graphic representation. The characteristics of the circadian rhythm are represented in the tables below each chronogram. The tables also include information on the number of BP series analyzed for each group. The circadian rhythm characteristics given in the tables are provided only as a first approximation and for descriptive purposes, given the nonsinusoidal pattern of BP circadian variability as well as the different duration of the activity and resting spans.
Fig 2 represents the circadian chronograms of SBP (left) and DBP (right) of women sampled during the second trimester of pregnancy. The differences between normotensive subjects and women with gestational hypertension are highly statistically significant at all circadian times. The circadian MESOR of BP for normotensive pregnant women is statistically lower in the second as compared to the first trimester (P<.001 for both SBP and DBP). The decrease in BP cannot be demonstrated, however, for women with a final diagnosis of gestational hypertension or preeclampsia.
Fig 3, comparing SBP and DBP between healthy and complicated pregnancies sampled in the third trimester of gestation, is similar. Far away from the statistically significant difference in circadian MESOR between both groups documented by Bingham test, the 2-hourly means of SBP and DBP are statistically significantly higher in women with gestational hypertension or preeclampsia at all sampling times. Compared with the second trimester, BP slightly increases for normotensive pregnant women, reaching a circadian MESOR comparable to that computed in the first trimester for the same subjects (Fig 1). For women with complicated pregnancies, however, BP increases greatly from the second to the third trimester.
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Discussion |
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The advantages of using rhythm parameters (MESOR and amplitude) compared with usual statistics (mean and range) when describing the pattern of circadian BP variability have already been described.9 10 11 Since the data were obtained at an unequidistant sampling rate covering approximately two cycles (48 hours), the MESOR provides a better estimation of the true 24-hour mean than the average of all BP values (usually overestimating the true mean due to the denser sampling during activity). The MESOR and the mean are only mathematically equal when the data are obtained at an equidistant sampling rate covering an integer number of cycles, a situation far from real in most clinical applications. The double amplitude provides information about the extent of total predictable change in BP along the 24 hours. Since the amplitude but not the range is computed from the best fitted curve to original values, it contains information about BP variability coming from the whole data series. The range, on the contrary, only reflects the difference between the maximum and minimum single values. These extreme values are too frequently associated with measurement errors or samples influenced by external stimuli.10 11 The cosinor analysis, however, requires that the data obtained be reasonably well represented by a cosine curve. Therefore, nonsinusoidality limits the applicability of the method. In cases where more than one period is statistically significant over the span of time investigated or when the waveform is nonsinusoidal (as in the case of the circadian variability of BP), the use of a multiple component analysis is recommended.27 The method allows us to fit a model consisting of several cosine functions. The multiple linear least-squares procedure is, however, only applicable for the analysis of longitudinal time series. An equivalent to the population-mean cosinor method (for analysis of short, sparse, and nonequidistant hybrid time series, that is, a collection of time series sampled at different times from a group of subjects) with the fit of multiple components, allowing inference to the population, has just been recently described.28 With these limitations notwithstanding, results in Figs 1 through 3 may serve to illustrate the statistically significant differences in the circadian pattern of BP variability between healthy and complicated pregnant women in all trimesters of pregnancy. The parameters in the tables below the figures are provided as a first approximation until the time comes to properly describe the nonsinusoidal waveform of BP variability by the fit of multiple components.
Results from Fig 1 indicate a highly statistically significant difference in both SBP and DBP between complicated and uncomplicated pregnant women sampled during the first 14 weeks of gestation. The differences in BP are statistically significant at each and every one of the 2-hourly intervals in which the 24-hour span was divided for comparative analysis. The differences in BP are found several months before the actual clinical diagnosis of gestational hypertension is made (usually obtained well in advance of the third trimester of pregnancy). Moreover, the differences of about 11 mm Hg in the circadian MESOR of SBP and of about 6 mm Hg in DBP are found when both SBP and DBP for women with a later diagnosis of gestational hypertension or preeclampsia are well within the accepted normal physiologic range of BP variability.29 The circadian MESOR for the group of women with complicated pregnancies was 114.3/66.0 mm Hg for SBP/DBP; the 2-hourly means were always below 127/75 mm Hg for the same variables, far below the "normal" limit of 140/90 mm Hg. As in the first trimester, the highly statistically significant differences documented in the second trimester (Fig 2), exceeding 12 mm Hg in the circadian MESOR of SBP and 6 mm Hg in the circadian MESOR of DBP, are found with BP values well below 140/90 mm Hg, even for the hypertensive women. The documented differences in the circadian MESOR between healthy and complicated pregnant women sampled during the third trimester are of about 17 mm Hg for SBP and 9 mm Hg for DBP.
Figs 1 through 3 also show differences in circadian amplitude between healthy and complicated pregnancies in all trimesters of gestation. By the use of ABPM, several authors have found a reduced drop in BP at night in preeclamptic patients,30 31 whereas others report an inversion in the circadian pattern of BP associated with preeclampsia.14 22 32 However, Figs 1 and 2 indicate that, during the first and second trimesters of pregnancy, before the clinical diagnosis of disease for most women investigated, the circadian amplitude of BP is statistically higher in complicated pregnancies. An increase in circadian amplitude of BP before the actual onset of hypertension (elevation in circadian MESOR) was also noted in several previous studies.9 The circadian amplitude of BP is statistically higher in neonates with a family history of hypertension and cardiovascular disease as compared to those without such history.33 By 14 years of age, correlations are found between the circadian amplitude of DBP and target organ involvement, namely the thickness of the interventricular cardiac septum determined by M-mode echocardiography.34 Fig 3 indicates that in the third trimester of pregnancy, the difference in circadian amplitude of BP between the groups compared is still statistically significant. For the complicated-pregnancy women, the amplitude decreases significantly from the second to the third trimester. This is mainly due to the reduced drop in BP at night (and therefore reduced circadian amplitude) in the patients who developed preeclampsia. The differences in amplitude between healthy and complicated pregnancies in this last trimester stem from the lack of reduction in amplitude for the women who developed gestational hypertension but not preeclampsia. The difference in amplitude between these two groups of complicated pregnancies (gestational hypertension with or without proteinuria) is statistically significant in the third (P<.009 for both SBP and DBP) but not in the first or second trimesters (P>.121 in all cases). A decrease in circadian amplitude of BP could then provide useful information in the identification of those women with an elevated BP in pregnancy who could also develop proteinuria, an issue that needs further investigation in larger groups of women.
Despite the differences observed in Figs 1 through 3, diagnosis cannot rely on BP measurements obtained at any given individual circadian time. To illustrate this point, we focused the analysis of all BP values sampled between 10 AM and 1 PM, the usual timing of most scheduled visits of pregnant women to the obstetrician at Spanish hospitals, including our own setting. Fig 4 represents the frequency histograms of all values of SBP sampled between those hours in healthy (top) and complicated pregnancies (bottom) in each of the trimesters of pregnancy. The histograms indicate the high degree of overlap between the distributions of SBP values obtained for both groups of pregnant women. During the first trimester (Fig 4, left), there was a total overlap of 96.8% of all 1472 SBP values sampled between 10 AM and 1 PM (98.5% for mean arterial BP; 98.2 for DBP, not shown). Women who later developed clinically diagnosed gestational hypertension or preeclampsia had at those times SBP values as low as 80 mm Hg, with only 36 of a total of 408 SBP values actually exceeding 140 mm Hg. During the second trimester, BP actually decreases for healthy pregnant women but not for those who develop gestational hypertension.13 The degree of overlap in SBP is 97.3% (Fig 4, center); only 117 of the 1488 SBP values obtained from complicated pregnancies exceeded 140 mm Hg. Results were almost similar during the third trimester, when many pregnant women had already developed clinically diagnosed gestational hypertension or preeclampsia, characterized by a "clearly" elevated BP. The graph on the right of Fig 4, for the third trimester, indicates an overlap of 98.9% in SBP; only 287 of 1954 values sampled from pregnant women with gestational hypertension or preeclampsia exceeded 140 mm Hg.
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The Table gives sensitivity and specificity based on BP values exceeding 140 or 110 or 90 mm Hg for SBP, mean arterial BP, and DBP, respectively. Results indicate a very poor sensitivity, comparable to that reported previously from other studies based on conventional casual BP sampling.1 2 3 4 5 6 Specificity is very high based on the distributions represented in Fig 4 and the chronograms of Figs 1 through 3: a very small number of BP samples actually exceeds the limit of 140/90 mm Hg for SBP/DBP, even in the third trimester, after the clinical diagnosis of gestational hypertension or preeclampsia has been made. One needs to be aware that results in the Table are overestimating the value of casual sampling and do not reflect the actual sensitivity of clinical diagnosis of gestational hypertension. The diagnosis indeed needs stronger criteria than just having one single value of BP obtained by ambulatory monitoring between 10:00 and 13:00 hours above 140 or 90 mm Hg for SBP or DBP.
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This study represents an example of longitudinal monitoring in healthy and complicated pregnancies, keeping the everyday life conditions by the use of a fully ambulatory and noninvasive BP monitor. The results were based on 48-hour series rather than on the 24-hour profiles more currently obtained by ABPM.16 17 18 19 20 21 As a compromise with practicability, monitoring over 48 hours has been shown to present advantages.9 11 35 The individualized estimation of rhythm characteristics becomes more reliable; new end points are obtained, such as the circadian period, that cannot usually be estimated from 24-hour records. Moreover, there may be relatively large day-to-day changes in individual rhythm characteristics, due in part to differences in day-to-day schedules, that are at least partly accounted for by sampling over 2 or more days. Noninvasive ABPM combined with chronobiometric methods for analysis of sparse and nonequidistant time series offers new end points that allow an early assessment of the risk of gestational hypertension and preeclampsia.35
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Selected Abbreviations and Acronyms |
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Acknowledgments |
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This research was supported in part by grants from Dirección General de Investigación Científica y Técnica (DGICYT), Ministerio de Educación y Ciencia (PB92-1111 and PB93-0372); Consellería de Educación e Ordenación Universitaria, Xunta de Galicia (XUGA-322002B97, 32205B95, and 32201B95); and Vicerrectorado de Investigación, University of Vigo.
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Footnotes |
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Reprint requests to Prof Ramón C. Hermida, PhD, Director, Bioengineering and Chronobiology Labs, ETSI Telecomunicación, Campus Universitario, Vigo (Pontevedra) 36200, Spain.
Received March 15, 1997; first decision April 17, 1997; accepted April 29, 1997.
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References |
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  R. T. Mikolajczyk, J. Zhang, J. Ford, and J. Grewal Effects of Interpregnancy Interval on Blood Pressure in Consecutive Pregnancies Am. J. Epidemiol., August 15, 2008; 168(4): 422 - 426. [Abstract] [Full Text] [PDF]
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 P.R.R. Gangula, P. Lanlua, R.D. Bukoski, S.J. Wimalawansa, and C. Yallampalli Mesenteric Arterial Relaxation to Calcitonin Gene-Related Peptide Is Increased During Pregnancy and by Sex Steroid Hormones Biol Reprod, November 1, 2004; 71(5): 1739 - 1745. [Abstract] [Full Text] [PDF]
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 R. C. Hermida, D. E. Ayala, A. Mojon, J. R. Fernandez, I. Alonso, I. Silva, R. Ucieda, and M. Iglesias Blood Pressure Patterns in Normal Pregnancy, Gestational Hypertension, and Preeclampsia Hypertension, August 1, 2000; 36(2): 149 - 158. [Abstract] [Full Text] [PDF]
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R. C. Hermida, D. E. Ayala, J. R. Fernandez, A. Mojon, I. Alonso, I. Silva, R. Ucieda, J. Codesido, and M. Iglesias Administration Time-Dependent Effects of Aspirin in Women at Differing Risk for Preeclampsia Hypertension, October 1, 1999; 34(4): 1016 - 1023. [Abstract] [Full Text] [PDF]
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 M. Tozawa, K. Iseki, S. Yoshi, and K. Fukiyama Blood pressure variability as an adverse prognostic risk factor in end-stage renal disease Nephrol. Dial. Transplant., August 1, 1999; 14(8): 1976 - 1981. [Abstract] [Full Text] [PDF]
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R. C. Hermida, D. E. Ayala, A. Mojon, J. R. Fernandez, I. Silva, R. Ucieda, and M. Iglesias Blood Pressure Excess for the Early Identification of Gestational Hypertension and Preeclampsia Hypertension, January 1, 1998; 31(1): 83 - 89. [Abstract] [Full Text] [PDF]
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R. C. Hermida and D. E. Ayala Diagnosing Gestational Hypertension and Preeclampsia With the 24-Hour Mean of Blood Pressure Hypertension, December 1, 1997; 30(6): 1531 - 1537. [Abstract] [Full Text]
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