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ORIGINAL RESEARCH |
From the MRC/UKZN Pregnancy Hypertension Research Unit and Department of Obstetrics and Department of Gynaecology and Cardiology, Nelson R. Mandela School of Medicine, University of KwaZulu-Natal, Durban, South Africa.
Address reprint requests to: J. Moodley, Department of Obstetrics and Gynaecology, Nelson R. Mandela School of Medicine, Private Bag 7, Congella, 4013, South Africa; e-mail: gynae{at}nu.ac.za.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: One hundred sixty echocardiographic studies were performed in 35 healthy pregnant women for longitudinal evaluation from early second trimester until term and 6–12 weeks postpartum.
RESULTS: Cardiac output increased significantly at the early to mid third trimester and was maintained until term. It increased predominantly in the latter half of pregnancy, and peak cardiac output of 46–51% occurred from a 15% increase in heart rate and 24% increase in stroke volume. Maternal cardiac output measured in the early third trimester showed a good correlation with maternal body surface area (r = 0.72; P < .001) and fetal birth weight (r = 0.52; P = .008). Left ventricular systolic function was preserved until term.
CONCLUSION: Maternal cardiac output peaks in the early to mid third trimester and is maintained until term. Significant correlations were observed among maternal cardiac output, maternal body surface area, and fetal birth weight.
LEVEL OF EVIDENCE: II-2
Van Oppen et al1 also performed a meta-analysis of 6 longitudinal studies that had 2 or more cardiac output measurements during pregnancy. The authors found widely divergent changes in cardiac output between the second and third trimesters, with 2 studies showing an increase, 2 with no change, and 2 with a decrease. Both van Oppen et al3 and Duvekot and Peeters4 cited patient factors rather than technique as being responsible for the apparent divergent trends of cardiac output in the third trimester.
Although Thornburg et al5 in their review reported that cardiac output peaks in the mid third trimester by approximately 50%, the peaking of cardiac output has been reported to occur at gestations varying from 24 weeks to term. In addition, the relative contributions to cardiac output made by increases in heart rate and stroke volume have not been well addressed. Furthermore, most studies of maternal hemodynamics in normal pregnancy have reported measurement of cardiac output rather than a stature-corrected measure of cardiac index. This study evaluates echocardiographic maternal central hemodynamics, cardiac structure and function, and maternal stature in healthy pregnant women.
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MATERIALS AND METHODS |
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At enrollment, the attending obstetrician performed an obstetric assessment together with clinical assessment of gestational age. Obstetric ultrasound examination was performed to obtain accurate fetal gestation, to exclude fetal abnormalities, and to confirm a singleton pregnancy.
All participants had a clinical examination by 1 of the authors (D.K.D.) to rule out preexisting heart disease. Enrolled women rested in the left lateral position with assistance of a foam wedge for 10 minutes. Echocardiographic studies were performed thereafter (by D.K.D.) using the Ultramark 9-HDI imaging system with a 2.5 MHz transducer (Scientific Medical Systems, Inc., New York, NY). Two-dimensional echocardiography facilitated accurate M-mode recordings and color flow mapping facilitated Doppler measurements according to standard criteria.6 Ten normotensive participants at 32–36 weeks of gestation had repeat echocardiographic studies 2 hours apart to evaluate reproducibility; the mean percentage error for cardiac output was measured at 2.0%.
In brief, the procedure was carried out as follows: an initial 2-dimensional study in the standard parasternal long axis and short axis planes followed by the apical 4-chamber plane view was performed to evaluate cardiac structure and obtain a visual assessment of left ventricle (LV) contractile function. Two-dimensional-imaging–directed M-mode studies were then performed at the level of aorta, left atrium, and left ventricle at mid position between the tips of the mitral valve and papillary muscle. Frozen M-mode images on screen were used to measure chamber size and ventricular wall thickness. Pulsed Doppler flow across the mitral valve was recorded just beyond the tips of the mitral valve leaflets to obtain the LV diastolic filling pattern.
Heart rate and blood pressure (BP) were measured during the echocardiographic study by an automated BP measuring device (Critikon [SA], GE Medical Systems, Melville, NY) at 3-minute intervals. Blood pressure was measured in the dependent (left) arm. The average of 5–7 measurements obtained was accepted as representative heart rate and blood pressure measurements at echocardiography. Mean blood pressure was computed using the standard formula of mean BP (mm Hg) = diastolic BP + 1/3 (systolic BP – diastolic BP). These values were used with echocardiographic-Doppler–derived stroke volume to obtain cardiac output, and systemic vascular resistance (SVR) was computed using the following formula:
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| (1) |
Cardiac output derived from LV Doppler was obtained by the standard accepted method as described by Ihlen et al.7 Three estimates of the aortic annulus diameter were made in the parasternal long axis plane, and the average was accepted as the representative cross-sectional area at the aortic annulus. The velocity time integral Doppler measurement was performed in the apical—5—chamber view at the level of the aortic valve using pulsed Doppler. The best profile of 3 measurements was selected and measured; the maximal velocity time integral value was accepted. Calculation of LV stroke volume was done using the following formula:
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| (2) |
where VTI(m) = velocity time integral at the level of aorta in meters.
The product of stroke volume and mean heart rate (average of 5–7 measures) at echocardiography produced a measure of cardiac output. Cardiac output was corrected for stature by the standard DuBois and DuBois formula8 that used weight and height to derive body surface area to obtain cardiac index (L · min–1 · m–2). Systemic vascular resistance was computed from cardiac output, and mean arterial blood pressure was obtained from the average of 5–7 measurements at echocardiography; systemic vascular resistance index was derived by correction for body surface area.
The LV contractility (systolic function) was measured from M-mode recordings of the LV in the short axis view at a level just beyond the tips of the mitral valve leaflets. On-screen measurements of the LV M-mode tracing were used to measure LV cavity dimensions in systole and diastole, from which indices of LV contractile function (fractional shortening, ejection fraction, velocity of circumferential fiber shortening, and LV end systolic wall stress) were computed. At least 2 M-mode tracings of the LV were performed to ensure that cavity dimensions were within 2 mm and that of ventricular wall thickness to be within 1 mm of each other. A third trace was performed if the first 2 M-mode traces did not provide satisfactory measurements, and representative values were obtained by consensus with a cardiology colleague.
The LV ejection time, measured from the aortic velocity time integral profile, was used to correct fractional shortening to obtain the velocity of circumferential fiber shortening, an index of LV contractile function.
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| (3) |
where LVID(d) is the left ventricle internal dimension in diastole and LVID(s) is the left ventricle internal dimension in systole.
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| (4) |
where LVV(d) is the left ventricle volume in diastole, LVV(s) is the left ventricle volume in systole, and where LV volumes are calculated by the Teichholz formula:
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| (5) |
where D is the LV minor axis dimension (in centimeters) in diastole. The LV septum and posterior wall thickness together with LV cavity size in diastole were used to compute LV mass (in grams) according to the formula of Devereux.6 The LV mass was corrected for maternal size by dividing LV mass by body surface area (in square meters) to obtain the LV mass index (in grams per square meter). The LV mass was also corrected for height to obtain LV mass/height (in grams per meter). The LV mass was derived using measurements of LV septum, posterior wall thickness, and LV internal diameter. The formulae used to compute LV mass and LV mass index are listed below.
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| (6) |
where LVID(d) is the left ventricle internal dimension (in centimeters) in diastole, LV septum(d) is left ventricle septal thickness (in centimeters) in diastole, and LV pw (d) is left ventricle posterior wall thickness (in centimeters) in diastole.
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| (7) |
Left atrial size was assessed from the 2-dimensional-view–directed M-mode measurements to obtain left atrial and aortic root diameters from which a measure of the left atrial to aortic size ratio was computed.
The LV diastolic filling velocities across the mitral valve were obtained using pulsed Doppler in the apical 4-chamber view; recordings were made at a position just distal to the mitral valve leaflets. The results were recorded as early filling velocity (in meters per second), late filling velocity, and the early/late diastolic filling ratio was computed.
All statistical comparisons were performed using the SPSS 11.0 statistical package (SPSS Inc., Chicago, IL). The primary comparative analyses of cardiovascular hemodynamic and structural variables were made using paired-sample t tests. Where appropriate, comparisons of average values between periods were made either by independent samples t tests or 1-way analysis of variance, and significance was set at P < .05. Cross tabulation (
2 test) was used for evaluation of noncontinuous variables. Bivariate correlation and linear regression analyses were used to estimate relationships among measured cardiovascular variables.
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RESULTS |
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Table 2 details the hemodynamic changes in cardiac output and systemic vascular resistance with corresponding changes in heart rate, stroke volume, and mean blood pressure. Cardiac output increased predominantly in the latter half of pregnancy and continued to increase and peak at term. However, statistically significant increases (P < .05) were seen at the early third, late second, and mid second trimester periods. Using postpartum value as baseline, a 46% increase in cardiac output was present. This maximal cardiac output occurred as a result of a 15% increase in heart rate and a 24% increase in stroke volume. This 24% increase in stroke volume was derived at Doppler echocardiography by a 9% increase in velocity time integral at the aortic annulus and a 15% increase in aortic annulus cross-sectional area.
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Heart rate showed a statistically nonsignificant decrease at the late third trimester compared with the mid third trimester. Although stroke volume increased until term, statistically significant increases were noted only at the late third and late second trimester periods. A statistically significant maximal decrease in systemic vascular resistance was observed at the early third trimester, and mean blood pressure by comparison showed a statistically significant increase after the early third trimester.
Table 3 shows the stroke volume and cardiac output in a subgroup of women (n = 10) who had echocardiographic studies at all periods from the mid second trimester and were compared with the full group. The stroke volume and cardiac output between these groups were similar, without any statistically significant differences. Paired t tests showed similar trends and P values at the various periods in the subgroup and full group and thus validated conclusions drawn from the full study group members, who had missing visits. The P values for cardiac output increases in the mid and late third trimester in the subgroup (P = .083 and P = .156, respectively) indicate that cardiac output probably peaks at a period between the early and mid third trimester and is maintained until term. A significant increase in stroke volume at term was also noted for both the subgroup and full group.
Table 4 details changes in cardiac output and cardiac index together with weight and computed body surface area. It is noted that both cardiac output and cardiac index show similar statistical increases at the indicated periods. Table 5 estimates relationships among cardiac output, cardiac index, and maternal stature variables in the early and mid third trimester and fetal birth weight. Significant correlations were noted between cardiac output and fetal birth weight and maternal stature variables as indicated. Linear regression analysis showed that in the early and mid third trimesters, weight best predicted maternal cardiac output (r2 = 0.56 and 0.50, respectively).
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Table 6 shows changes in cardiac structure and function variables of left atrial size together with left atrial to aorta size ratio, LV early/atrial diastolic filling ratio, LV mass, LV mass index, and LV systolic function reflected by fractional shortening percentage. Both left atrial size and left atrial/aorta size ratio showed a significant increase at term, followed by a significant reduction in size postpartum. The LV diastolic filling of early/atrial filling ratio showed a nonsignificant decrease in the third trimester.
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Table 6 also shows significant increases in LV mass and LV mass index that are maximal at term. The mean LV mass index remained well below the arbitrary cutoff level of 110 g/m2 to diagnose LV hypertrophy. The study also showed good correlation of LV mass with stature-corrected indices of LV mass index (r = 0.93), LV mass/height (r = 0.99), and LV mass/height1.7 (r = 0.99). A lower LV mass index at 14–19 weeks of gestation compared with postpartum value (6–12 weeks) is noted and probably reflects that LV mass measured 6–12 weeks postpartum had not returned to normal prepregnant values; this limits an accurate assessment of the extent of LV mass increase in our study.
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DISCUSSION |
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The literature has conflicting data on cardiac output changes during pregnancy, particularly in the third trimester.3,4,9–11 Although the meta-analysis of cross-sectional studies by van Oppen et al1 showed a trend to a lower cardiac output in the third trimester compared with the second, the authors observed large ranges in cardiac output among the different studies that did not allow for any firm conclusions. In evaluating 6 longitudinal studies, van Oppen et al1 found that cardiac output between the second and third trimesters plateaued, decreased, or increased. Of these, the 4 studies with comparable techniques still showed striking differences in the course of cardiac output in the third trimester, with Duvekot et al12 showing a decrease of 11.5%, no change by Robson et al,13 and increases of 9.3% by Mabie et al14 and 16.4% by Thomsen et al.15
Although design differences and measurement techniques among studies can explain some of the reported differences in maternal hemodynamics in normal pregnancy, most researchers concur that patient factors rather than measurement error are largely responsible for discrepancies in reported studies. The longitudinal study by Robson et al13 of 13 patients, cited as the only true longitudinal study in the van Oppen meta-analysis,1 surprisingly showed a significant increase in cardiac output of 75% of peak value by 12 weeks of gestation that was followed by a very gradual rise to peak cardiac output occurring at 24–36 weeks and cardiac output being maintained thereafter until term. It is to be noted that after 16 weeks of gestation, the Robson study data did not show any statistically significant increase in cardiac output at any of the defined 4-week periods.
Our study shows a similar increase in mean cardiac output until term as described by Mabie et al14 in their longitudinal study of 18 normotensive women. However, although the Mabie study showed a peak cardiac output at term, none of the increases in the comparative periods (4 weeks) were significant. In addition, a similar wide variation in measured cardiac output at the mid and late third trimester was also noted. Our study, by contrast, shows a statistically significant increase in cardiac output in the early third trimester over the late second trimester, data that clearly indicate that cardiac output at the very least peaks in the early to mid third trimester. The increase in cardiac output thereafter in the mid and late third trimester in our study, although not statistically significant, does indicate that at the very least, cardiac output in the mid and late third trimester is maintained.
The ability of our study to show a statistically significant increase in cardiac output at the early to mid third trimester compared with the Robson and Mabie studies described above probably reflects differences in observed cardiac output increase in the first half of pregnancy. We did not directly measure cardiac output in early pregnancy, but using postpartum values as baseline, our data show that 40% of peak cardiac output occurred at 24 weeks compared with the Robson and Mabie studies described above, where more than 75% of peak cardiac output occurred by 24 weeks. These differences of a "predominantly early" versus a " predominantly late" increase in cardiac output in normal pregnancy are not easily explained. Although maternal body surface area and cardiac output increase expressed as a percentage in our study are similar to the study by Mabie et al,14 the peak cardiac index of 4.8 ± 0.8 L · min–1 · m–2 in the Mabie study is higher than 4.0 ± 0.8 L · min–1 · m–2 in our study. In addition, the mean birth weight in our study was 2.9 ± 0.6 kg compared with 3.4 ± 0.6 kg in the Mabie study. Despite comment in the Mabie study of having cardiac output measurements that are higher than most reported studies, the above observations provide supportive evidence for a positive association between maternal cardiac output and fetal birth weight. In addition, they generate hypotheses, especially for comparative studies in different population groups where apparent normal maternal health and accepted normal fetal birth weights may not be so and simultaneous uteroplacental evaluation may provide a more precise research definition of normal healthy pregnancy.
Most of the heart rate increase in our study (60%) probably occurred in the first trimester and that of stroke volume in the third trimester, because changes in heart rate in the second and third trimester were not significant. It therefore appears that the mild increase in cardiac output in early pregnancy is largely accounted for by an increase in heart rate, and the progressive increase in cardiac output thereafter in the latter half of pregnancy is due to an increase in stroke volume. The apparent bimodal peaking of stroke volume occurring initially in the second trimester probably occurs as a result of changes in heart rate described above. These observations are supported by the hypothesis of Carbillon et al16 that adaptation of vascular tone in early pregnancy precedes and probably triggers blood volume and cardiac output increase.
Noting a satisfactory association between maternal cardiac output and maternal body size in our study, some of the variations in cardiac output in normotensive pregnant women can be explained by differences in maternal stature and its surrogate marker of fetal birth weight. Despite earlier reports of a poor correlation between maternal cardiac output and body surface area by van Oppen et al17, our study, together with reported cardiovascular studies outside pregnancy in children and obese adult participants by de Simone et al,18 indicate that variables such as cardiac output need correction for participants’ body stature for appropriate comparison between groups. The need for correction of cardiovascular variables for maternal size is highlighted in some early studies. Rosso et al19 found that underweight mothers had lower birth weight babies compared with normal weight mothers, which corresponded with lower maternal plasma volume and cardiac output. Similarly, Carpenter et al20 found differences in maximal oxygen uptake when evaluating effects of maternal weight on exercise during pregnancy, differences that were not present when oxygen uptake measurements were corrected for maternal weight.
The poor correlation between cardiac output and body surface area in the van Oppen et al17 study are not easily explained; possible reasons include a bias from including more women (n = 78) who had cardiac output measured by thoracic electrical bioimpedance technique than the 10 women from a cohort in a subfertility clinic whose cardiac output was measured by the Doppler technique (in whom 3 of the 5 antenatal evaluations were in the first trimester). Both the Doppler and bioimpedance groups in the van Oppen study had cardiac output increases of 88% and 92% of peak values by the fifth and eighth weeks of gestation, respectively, observations that do not make physiologic sense. Duvekot et al12 suggested that this increase of cardiac output in the early and mid first trimester is probably mediated by an endocrine stimulus and hence, not surprisingly, poorly related to maternal body surface area at this stage. It is also to be noted that the correlation of maternal cardiac output with maternal stature variables reported in our study were made, albeit more appropriately, only in the third trimester. Finally, despite criticism, the use of body surface area computed by using the formula described by DuBois and DuBois8 to standardize maternal cardiovascular variables seems justified, because Wang et al21 in their study evaluating predictors of body surface area that included 60 women at gestation between 34–40 weeks concluded that several body surface area formulas, including the DuBois formulas, adequately predict measured body surface area over a wide range of patient populations.
Differences in LV systolic function among studies can explain some of the observed variation in measured cardiac output and hence heart rate and stroke volume. Normal pregnancy is associated with a significant drop in blood pressure and systemic vascular resistance index, a reflection of the reduced cardiovascular afterload and fall in uterine vascular resistance. Physiologically, an increase in preload and reduced afterload is often accompanied by an increase in left ventricular systolic function. Our study demonstrates that LV fractional shortening during pregnancy is preserved, findings that are similar to data of Robson et al13 and Mabie et al.14 However, these observations are at variance with studies by Mone et al,10 who showed a transient fall in LV fractional shortening during the third trimester, and that of Schannwell et al,22 who also showed a reduction in left ventricular systolic function values of fractional shortening and velocity of circumferential fiber shortening that had a nadir at the first postpartum visit. These differences are not easily explained; the very plausible postulate both by Mone et al10 and Schannwell et al22 is that a reduced preload in the latter part of the third trimester contributes to a reversible fall in LV systolic function.
The study by Poppas et al23 is of particular interest, in that they report a steady increase in cardiac output until term but without any change in LV contractility, measured both by the load-dependent index of fractional shortening and also by load-independent indices of LV velocity of circumferential fiber shortening and LV systolic wall stress. As indicated, a limitation of LV fractional shortening and echocardiography-derived ejection fraction is that they are sensitive to loading conditions, particularly preload and, to a lesser extent, afterload. Noting this limitation, future studies evaluating maternal LV contractility should focus more on the less load-dependent indices such as LV velocity of circumferential shortening and LV systolic wall stress. Group ethnic profile as a factor associated with LV contractility is also noted, because all participants in our study were Black Africans. Desai et al24 had previously reported a very high prevalence of peripartum cardiomyopathy in the same population group. Such differences in LV systolic function, although clinically small and transient, may explain some of the divergent trends in cardiac output in the third trimester.
In addressing a possible effect of parity on cardiac output changes in pregnancy, Clapp et al25 in their M-mode echocardiographic study suggested that cardiovascular adaptation is enhanced by a subsequent pregnancy. In the study by van Oppen et al3 that evaluated cardiac output in the third trimester by thoracic electric bioimpedance, the authors found a significant difference in mean cardiac output between nulliparous and multiparous women. The number of participants in our study did not allow for any confident conclusions on differences in hemodynamics between primiparous and multiparous normotensive pregnant women. Despite limitations of measuring cardiac output in pregnancy by M-mode echocardiographic and thoracic electrical bioimpedance techniques, the above observations suggest that some of the reported differences in reported cardiac output among studies may be related to parity differences of study participants.
The variability of echocardiographic-Doppler–determined stroke volume and hence cardiac output depends largely on measurement of aortic annulus diameter and the computed aortic annulus cross-sectional area. Data on appropriate and accurate aortic annulus measurements are conflicting.5,7,14 In our study, using a single operator, obtaining 3 measurements, and using the average as representative measurement, the aortic annular measurement accounted for only 1.8% of the variation in measured cardiac output. Robson et al26 have reported within-subject, intraobserver, and temporal variation for Doppler-derived cardiac output in pregnancy at less than 5%. Although a smaller number of subjects having echocardiographic evaluation in the late third trimester did not significantly affect comparative observations, it probably limited a more precise and confident measure of changes between mid and latter portions of the third trimester where expected absolute changes are smaller. However, a limitation in our study is that reproducibility was tested only at 32–26 weeks of gestation; this could potentially be different at other gestational periods.
Our study shows a significant increase in LV mass and LV mass index of 26% and 18%, respectively, using 6–12 weeks postpartum as baseline, observations that are similar to data of Mabie et al.14 However, reported increases in LV mass in pregnancy have been variable, being 10% in a study of 14 healthy pregnant women by Poppas et al,23 16% in a study of 33 normotensive women by Mone et al,10 and a 34% increase in left ventricular mass index by Schannwell et al.21 These variations in percentage increase in LV mass probably reflect differences in the precise timing of postpartum measurements, because Mone et al10 have indicated that when evaluating LV structural changes, there is a lag period of 1–4 weeks to develop a compensatory increase in LV mass to offset an increase in LV wall stress.
This study also shows that in healthy pregnant women, there is an excellent correlation between LV mass and its stature-corrected variables of LV mass index, LV mass/height, or LV mass/height.1.7 An echocardiographic diagnosis of LV hypertrophy (LV mass index 
110 g/m2) was noted in only 1 of 35 normotensive women at term. The data of this study thus supports the fact that although LV mass increases significantly in normotensive pregnancy, levels that define the presence of echocardiographic LV hypertrophy do not occur in most women.
Our study shows significant increases in LV mass in the mid and late third trimester that correspond to small but statistically significant increases in mean blood pressure, a significant increase in left atrial size at term, and a nonsignificant decrease in LV diastolic filling value reflected by reduced LV early/atrial filling ratio. These observations may be of relevance, because we27 have reported abnormalities in LV diastolic filling in pregnant women who presented with hypertensive crises complicated by pulmonary edema. Because it is also accepted that LV diastolic dysfunction often precedes systolic dysfunction, differences in the degree of LV hypertrophy and diastolic filling could explain some of the reported small differences in LV contractility and cardiac output in the third trimester in normotensive pregnant women.
In conclusion, our study shows a significant increase in cardiac output at the early third trimester that is maintained until term. Cardiac output increased predominantly in the latter half of pregnancy. We also show a significant correlation between cardiac output and maternal stature and its surrogate marker of fetal birth weight. Comparative analysis of our data with that of Mabie et al14 further supports this association of maternal cardiac output, stature, and fetal birth weight.
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Footnotes |
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10.1097/01.AOG.0000128170.15161.1d
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REFERENCES |
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