(Circulation. 1996;94:667-672.)
© 1996 American Heart Association, Inc.
Articles |
Control Mechanisms for Physiological Hypertrophy of Pregnancy
the Department of Cardiology, Children's Hospital, and the Department of Pediatrics, Harvard Medical School, Boston, Mass.
Correspondence to Steven D. Colan, MD, Department of Cardiology, Children's Hospital, 300 Longwood Ave, Boston, MA 02115. E-mail colan@a1.tch.harvard.edu.
 |
Abstract |
|---|
 Top Abstract IntroductionMethodsResultsDiscussionReferences |
|---|
Background Pregnancy represents an excellent model of acute physiological hypertrophy and atrophy secondary to a transient hemodynamic load. This investigation examined the effects of pregnancy on ventricular mechanics using load-independent indexes of contractility to test the hypothesis that the cardiac trophic response functions as a servomechanism with wall stress as the feedback variable.
Methods and Results Serial studies were performed in 33 women at six time periods during and shortly after normal gestation. Changes in ventricular dimension, wall thickness, and left ventricular mass were parallel to changes in body size. Fractional shortening and velocity of shortening progressively diminished during pregnancy, with a nadir at the first postpartum examination, despite a progressive fall in afterload. Cardiac index rose rapidly in early gestation and remained elevated throughout pregnancy. Peak wall stress was elevated in early gestation coincident with the rapid rise in cardiac index due to elevated volume before compensatory rise in mass. With compensatory hypertrophy, peak wall stress normalized by midgestation. The change in left ventricular mass was closely related to peak wall stress but correlated poorly with mean, total, and end-systolic wall stress.
Conclusions Normal pregnancy is associated with a reversible fall in contractility. Systolic function is preserved throughout most of pregnancy by a fall in afterload but decreases near term and early postpartum because of decreased contractility and diminished preload. Left ventricular hypertrophy and atrophy are temporally related to changes in hemodynamic load. The response is consistent with a tightly coupled servomechanism transduced by peak wall stress with a 1- to 4-week compensatory response time.
Key Words: pregnancy • ventricles
|
Introduction |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Pregnancy is associated with dramatic alterations in hemodynamic load, but the associated changes in myocardial mechanics are not well defined. Previous noninvasive investigations have attempted to assess the response to the volume-overload state1 2 3 4 by use of ejection phase indexes of left ventricular performance such as percent FS, velocity of fiber shortening, and systolic time intervals. These indexes, however, are limited in their ability to assess myocardial properties by their dependence on loading conditions.5 6 7 8
The relation between VCFc and ESS has been shown to be an afterload-adjusted, preload-independent index of contractility.8 Noninvasive methods to quantify left ventricular systolic mechanical properties by use of this relation have been used to assess a variety of altered physiological states.9 10 11 12 Since pregnancy represents a hemodynamic state of altered preload (increased blood volume) and afterload (with interposition of the low-resistance placental circuit), use of a load-independent index such as the relation between ESS and VCFc is necessary to accurately assess the functional and contractile state of the left ventricle.
Pregnancy also represents an excellent model of acute physiological left ventricular hypertrophy and atrophy secondary to a transient, self-limited hemodynamic load. Load modulation of LVM is believed to occur by a servocontrolled mechanism with wall stress as the feedback variable.13 Using the volume overload imposed by pregnancy as the stimulus for cardiac hypertrophy, we wished to test this hypothesis by performing serial echo-Doppler examinations in women at multiple time periods during gestation and in the early postpartum period.
Thus, the purposes of this investigation were (1) to examine the effects of pregnancy on left ventricular mechanics by use of load-independent indexes of left ventricular contractility and (2) to test the hypothesis that the cardiac trophic response functions as a servomechanism with wall stress as the feedback variable.
|
Methods |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Subjects
Thirty-eight women over a 3-year period volunteered to participate in the study. All were free of known cardiovascular disease, none were taking cardioactive medicines, and all had normal intracardiac anatomy and wall motion by two-dimensional echocardiography. All subjects were white, and all had high-quality prenatal and postnatal health care. Because of our desire to quantify the normal response to pregnancy, women who experienced pregnancy-related problems such as hypertension or gestational diabetes were excluded from analysis. The study protocol was approved by the Brigham and Women's Human Research Committee, and after explanation of the study protocol, informed consent was obtained from each participant.
Data Acquisition
Height and weight were measured at the time of each echocardiographic evaluation, and body surface area was calculated according to the formula of Haycock et al.14 Simultaneous two-dimensionally directed M-mode echocardiograms, phonocardiograms, ECGs, indirect carotid pulse tracings, and blood pressure measurements were performed by previously described methods.11 15 Examinations were performed at 9 to 12, 18 to 20, 28 to 30, and 36 to 38 weeks of gestation and at 2 to 4 and 8 to 10 weeks postpartum. All echocardiographic examinations were performed by the same investigator (S.M.M.). Echocardiograms were performed with the patient in the left lateral decubitus position with either a Hewlett-Packard 1000 or 1500 or Acuson 128 XP ultrasound imaging system. High-speed (100-mm/s) hard-copy M-mode tracings were obtained of the left ventricular minor axis with either a 5.0- or 3.5-MHz transducer along with the phonocardiogram, ECG, and indirect carotid pulse tracing. The phonocardiogram was taken from the right upper sternal border. Systolic and diastolic blood pressures were measured with a Dinamap 845 automated vital signs monitor (Critikon, Inc).
Doppler echocardiography for determination of cardiac output, Z0, and impedance was also performed at the same time points. The blind 1.9-MHz continuous-wave transducer was placed in the suprasternal notch position and directed slightly leftward and anterior to record aortic flow velocities. The transducer position and orientation were adjusted until a maximum peak frequency shift and clean envelope were obtained. Aortic Doppler was recorded as a high-speed (100-mm/s) hard-copy tracing. The aortic valve orifice was measured from a parasternal long-axis transducer position. The diameter was measured in systole between the internal edges of the valve leaflets. The diameter was measured on three to five frames, and the results were averaged.
Data Analysis
M-Mode Analysis of Left Ventricular Dimensions, Thickness, Stress, and Mass
All computer measurements were performed by the same individual, eliminating issues of interobserver variability. The indirect carotid pulse tracing, the endocardial and epicardial borders of the left ventricular posterior wall, and the right and left ventricular borders of the interventricular septum were hand digitized on a microcomputer-based digitizing workstation with custom software. This system is programmed to adjust the tablet sampling rate to 200 Hz, which is adequate to obtain at least 50 nonaliased harmonics at heart rates <120 bpm. The carotid pulse tracing was corrected for time delay by alignment of the dicrotic notch with the first high-frequency component of the aortic component of the second heart sound. From the digitized data, the following instantaneous measurements were obtained by averaging three cardiac cycles: (1) left ventricular pressure during ejection calculated by assignment of diastolic pressure to the nadir and systolic pressure to the peak of the pulse trace and calculation of end-systolic pressure by linear interpolation to the height of the incisura (this method has been previously validated against an intra-arterial standard in our laboratory15 ); (2) left ventricular internal diameter; (3) left ventricular posterior wall thickness; and (4) left ventricular ESS in g/cm2, calculated throughout ejection according to ESS=[(P)(D)(1.35)]/[(4h)(1+h/D)], where P is the pressure in mm Hg, D is the short-axis dimension in centimeters, h is the posterior wall thickness in centimeters, and 1.35 is the conversion factor from mm Hg to g/cm2.16
From the continuous data, end-diastolic values for the left ventricular internal diameter and posterior wall thickness were taken at the time of maximum left ventricular dimension. End-systolic internal dimension and wall thickness, blood pressure, and ESS were measured synchronously with the first high-frequency component of the second heart sound (aortic valve closure). Blood pressure was taken as the average of four to six measurements. PSS was taken as the maximum value for ejection wall stress, mean systolic stress was calculated as the average stress during the ejection period, and total systolic stress was calculated as wall stress integrated over the ejection period.
Left ventricular FS was calculated as (EDD-ESD)/(EDD), where EDD is left ventricular end-diastolic diameter and ESD is end-systolic diameter. Left ventricular ejection time was measured from the pulse tracing and adjusted to a heart rate of 60 bpm by dividing by the square root of the RR interval on the ECG. The VCFc was calculated as FS divided by the rate-adjusted ejection time. LVM in grams was calculated by a modification of the method of Devereux and Reichek17 from M-mode measurements that assumes septal and posterior wall thickness to be equal: LVM=1.04[(D+2h)3-D3]-14 g, where D is the end-diastolic dimension and h is the posterior wall thickness.
Contractility and Preload Indexes
The relationship between VCFc and ESS has previously been shown to be an afterload-adjusted and preload-independent index of contractility.8 The position of the relation of ESS to VCFc for each patient at each time point was determined relative to the previously reported distribution of this index in normal control subjects8 and calculated as the SVI. The SVI is equal to the number of SDs from the population mean VCFc for the ESS. In contrast, the relationship between FS and ESS (SSI) is an after-load-adjusted index of contractility sensitive to changes in preload.8 10 11 The ESS-FS relation was correspondingly quantified as the SSI. The SSI is equal to the number of SDs from the population mean FS for the given ESS. The relative magnitude of VCFc compared with FS for any level of ESS is a measure of the preload status, reflecting the fact that FS is directly related to end-diastolic fiber length, whereas VCFc is independent of preload.5 8 10 11 18 Differences between the ESS-VCFc relation and the ESS-FS relation, therefore, reflect the functional consequences of altered preload, which was quantified as the functional preload index, FPI=SSI-SVI.
Doppler Measurements
Cardiac output was estimated by flow measurements of the ascending aorta using flow area times Doppler velocity as described by Goldberg et al.19 Because of the effect on cardiac output by the gravid uterus in the supine position,20 all measurements were performed with subjects in the left lateral decubitus position. Aortic input impedance was estimated by use of the calibrated carotid artery pressure as an estimate of central aortic pressure and Doppler-derived recording of aortic blood flow. This method has previously been shown to provide an excellent estimation of the invasively measured impedance harmonics.21 Phase-shift adjustment for spatial disparity between pulse and flow recordings was performed by alignment of aortic flow onset with the foot of the pressure wave. Pressure and flow waveforms were then transformed into the frequency domain by calculation of their complex Fourier series representation. The level at which the harmonics fell below the level of noise was estimated at 5 mL/s for flow and 1 mm Hg for pressure. Pressure and flow moduli were considered valid and were included in the calculation of impedance if both the pressure and flow components were greater than the system noise level. Aortic input impedance moduli were then obtained as the (complex magnitude of pressure) divided by the (complex magnitude of flow) for each valid modulus of pressure and flow. Z0 was calculated as the impedance modulus at 0 Hz, impedance at heart-rate frequency was taken as the first modulus, and Zc was calculated as the average of the valid impedance moduli beyond the first harmonic.
Statistics
All values are reported as mean±SD unless otherwise noted. The distribution within each group of variables was tested with the Shapiro-Wilk test for normality. If the distribution was normal (P>.05), then values obtained during different time periods were compared by ANOVA. If the distribution was abnormal by the Shapiro-Wilk test, then the groups were compared by Kruskal-Wallis one-way ANOVA. The relationship between LVM and the four indexes of stress (peak, mean, integrated, and end-systolic) was explored by linear regression analysis. All statistical analyses were performed with SPSS/PC+ from SPSS Inc. A value of P<.05 was considered statistically significant for all analyses.
|
Results |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
Of the original 38 women, 33 completed the study. Five were excluded after the study was initiated: preterm labor and subsequent terbutaline administration eliminated two participants, development of ventricular tachycardia and procainamide therapy excluded another, and the other two subjects elected not to complete the study. The subjects included in the analysis therefore had a normal, full-term pregnancy without significant complications. Maternal age was 30.8±3.7 years at the time of the first examination (9 to 12 weeks of gestation) and 31.4±3.8 at the time of delivery. Of the 33 women, this was the first pregnancy in 21, the second pregnancy in 6 (2 of whom had had spontaneous abortion during their first pregnancy), and the third pregnancy for the other 6 (2 of whom had had spontaneous abortion during both of their previous pregnancies). The gestational age at delivery ranged from 38 to 44 weeks (only 1 pregnancy was carried beyond 42 weeks), with a mean of 40.4 weeks. A total of 144 studies were obtained, with three to six examinations (mean, 4.4) in each subject.
Ventricular Dimensions and Wall Thickness
Hemodynamic and echocardiographic data for the gestational and postpartum periods are summarized in the Table
. Body surface area increased with weight gain during pregnancy and decreased accordingly with weight loss in the postpartum period. Peak systolic and diastolic pressures did not change (Fig 1). End-systolic pressure decreased in midgestation and neared baseline at term. Changes in dimension, wall thickness, and LVM were parallel to the change in weight and body surface area. LVM (in grams) increased by 16% from study 1 (139±32) to study 4 (161±35) and returned to initial levels (139±32) by 8 to 10 weeks postpartum. When adjusted for alterations in body mass, the change in LVM index was not statistically significant.
|
|
Wall Stress
ESS decreased 15% toward term, since the fall in end-systolic pressure exceeded the rise in end-systolic dimension (12% versus 6%). Peak wall stress (g/cm2) was highest in early pregnancy (154±38), was normal at studies 3 and 4 (138±38), fell to subnormal levels at the first postpartum study (127±35), and returned to normal by the last study (142±35). The increase in PSS in early gestation was due to an increase in dimension before a compensatory gain in wall thickness and was coincident with the rapid rise in CI. The postpartum fall in peak wall stress was due to more rapid reduction in dimension than thickness, corresponding to the fall in CI. The change in LVM closely followed the elevation or reduction in peak wall stress but correlated poorly with mean, total, or end-systolic stress (Fig 2).
|
Systolic Function, Stress-Shortening, and Stress-Velocity Relations
Despite the decrease in afterload, both FS and VCFc progressively diminished during gestation, achieving a reduction of 9% and 7%, respectively, at term. By the first postpartum examination, FS had fallen 15% and VCFc 11% compared with the first gestational examination. Although the afterload-adjusted VCFc (stress-velocity index), a load-independent index of contractility, remained within the normal range, it fell significantly in a linear fashion throughout gestation, reaching a nadir at the first postpartum examination and returning to baseline by the second postpartum examination (Fig 3). Afterload-adjusted FS (stress-shortening index), which is dependent on both contractility and preload,7 8 fell even further postpartum, consistent with the combined effects of reduced contractility and the postpartum fall in preload. The periods of altered preload corresponded to the periods during which CI changed most rapidly.
|
Cardiac Output, Z0, and Impedance
The change in stroke volume was proportional to the change in body mass. CI was elevated throughout pregnancy, rising most rapidly in early pregnancy and falling shortly postpartum, with associated fall and rise in arterial impedance and Z0. The rise in CI was secondary to the rise in heart rate, since Doppler stroke index fell progressively (Fig 4), corresponding to the observed fall in FS at constant indexed end-diastolic volume. Z0, impedance at heart rate, and Zc were lower throughout gestation than at postpartum. The reduction was proportional, with no significant change in the Zc/Z0 ratio.
|
|
Discussion |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
This study of pregnant women demonstrates relative preservation of systolic ventricular function throughout most of pregnancy by a fall in afterload, yet a decrease in function is apparent near term and early postpartum, caused by decreased preload and diminished contractility. Furthermore, the cardiac trophic response, determined by PSS, keeps pace with alterations in hemodynamic load, maintaining normal mass and wall stress throughout gestation and the postpartum period.
FS and velocity of shortening (both load-dependent indexes) decreased progressively throughout pregnancy, whereas load-independent indexes of contractility remained in the normal range throughout pregnancy. However, the load-independent index of contractility (SVI), while remaining in the normal range, fell progressively throughout gestation, reaching a nadir by the first postpartum examination. Since contractility was measured by load-independent indexes, this observation suggests that some undetermined aspect of pregnancy, possibly hormonal,22 may be responsible for alterations in intrinsic myocardial properties independent of the associated hemodynamic changes related to the well-recognized preload and afterload shifts.
In the only other study using load-independent indexes of ventricular function during pregnancy, Lang et al,23 in an investigation of preeclampsia, found VCFc values similar to ours during quiet labor and in the early postpartum period in 10 control pregnant women. Although early gestational values were not obtained, their findings demonstrate a decrease in VCFc from the end of gestation (quiet labor) to the early postpartum period, similar to our data.
Our data confirm observations by others1 2 24 25 that cardiac output increases up to 40% of nonpregnancy values by the early part of the second trimester. Others have reported the maximum gains in cardiac output occurring in late gestation.3 26 After delivery, there is an early and drastic reduction in output followed by a return toward normal cardiac output. The aortic impedance analysis provides some insight into the mechanism of the fall in resistance. Vasodilation leads to a fall in Z0, impedance at heart rate frequency, and Zc. However, the fall in Zc is less pronounced than the fall in Z0, resulting in a rise in the Zc/Z0 ratio. This ratio expresses the relationship between the opposition to pulsatile flow and the opposition to steady flow. For example, Langille and Adamson27 found that the baseline Zc/Z0 ratio of 
20% rose to nearly 30% during nitroprusside infusion and fell to about 10% during norepinephrine infusion in neonatal sheep. The usual value for this ratio in adults has been reported to be about 10%,28 not significantly different from the postpregnancy value of 12% that we found. The reductions in Zc and Z0 during pregnancy were sufficiently parallel that there was no significant change in Zc/Z0. This finding suggests that the fall in vascular resistance can be explained by the interposition of the low-resistance placental circuit without reflex or hormonally mediated systemic vasodilation.
The cardiovascular changes during pregnancy represent one of the forms of physiological hypertrophy and resemble those found with exercise training, with the exception of the observed fall in contractility. Physiological hypertrophy results in marked alterations in left ventricular loading conditions with secondary changes in systolic performance. Long-distance runners are faced with sustained elevation of preload due to increased venous return, leading to the addition of sarcomeres in series.29 Ventricular wall thickness increases proportionally to the increase in ventricular dimension. The pregnant woman experiences a sustained hemodynamic state similar to that of the trained long-distance runner. Distance-trained athletes have been found to have normal afterload but reduced preload at rest, manifested as reduced FS with normal afterload and contractile state.10 Our pregnant subjects underwent dramatic change in preload early postpartum; FS was reduced and afterload was normal, but contractility was diminished. Left ventricular mechanics of the pregnant woman and the trained distance runner differed primarily in the reduced contractility observed in late gestation and the early postpartum period. This diminished contractility in the setting of a "normal" physiological state warrants further investigation, particularly with regard to potential implications concerning peripartum cardiomyopathy.
In contrast to systolic function (which is determined primarily by ESS)8 9 10 and myocardial oxygen require-ments (which appear to be determined by total systolic stress),30 31 the myocardial trophic response appears to be governed by PSS.9 Our findings are consistent with the increase and decrease in LVM closely after the rise and fall of PSS. The elevation of PSS in early pregnancy is coincident with the rapid rise in CI and is closely followed by the increase in LVM. The normalization of PSS in late gestation is coincident with the plateau in LVM. The early postpartum fall in PSS corresponds to the rapid fall in CI as the left ventricle is "unloaded." Regression of myocardial hypertrophy closely follows this fall in PSS. This pattern of altered PSS preceding the rise or fall in LVM was not seen with other stress indexes, supporting the hypothesis that peak force requirements are the major control mechanism for physiological hypertrophy.
Limitations
This study, although defining the normal range of left ventricular function and contractility in pregnant women, involved white, healthy pregnant women with high-quality prenatal and postnatal care. This group may not be representative of the population at large. Furthermore, preconception values for all cardiovascular parameters were not obtained. It would be optimal to have preconception values to compare with the postpartum values to ascertain true return of variables to baseline. However, the primary conclusions of the study (the temporal relationship between change in hemodynamic load and hypertrophy and the reversible fall in contractility) are based on the observations made within the study period and do not rely on any assumptions concerning preconception conditions.
Conclusions
Myocardial remodeling is rapid during pregnancy as left ventricular hypertrophy and atrophy keep pace with changes in hemodynamic load, maintaining normal mass and wall stress. The timing of this physiological hypertrophic response appears to be transduced by peak wall stress with a 0- to 4-week compensatory response time.
Normal pregnancy is associated with a reversible fall in contractility. Systolic function is preserved throughout most of pregnancy by a fall in afterload but decreases near term and early postpartum as a result of decreased contractility and diminished preload. We speculate that the mechanism(s) responsible for this fall in contractility, which is most extreme in the early postpartum period, may have a relationship to the clinically important fall in contractility that manifests as postpartum cardiomyopathy.
|
Selected Abbreviations and Acronyms |
|---|
|
Received August 8, 1995; revision received February 8, 1996; accepted February 16, 1996.
|
References |
|---|
|
TopAbstractIntroductionMethodsResultsDiscussionReferences |
|---|
1. Rubler S, Damani PM, Pinto ER. Cardiac size and performance during pregnancy estimated with echocardiography. Am J Cardiol. 1977;40:534-540.[Medline] [Order article via Infotrieve]
2.
Katz R, Karliner JS, Resnick R. Effects of a natural volume overload state (pregnancy) on left ventricular performance in normal human subjects. Circulation. 1978;58:434-441.
3. Mashini IS, Albazzaz SJ, Fadel HE, Abdulla AM, Hadi HA, Harp R, Devoe LD. Serial non-invasive evaluation of cardio-vascular hemodynamics during pregnancy. Am J Obstet Gynecol. 1987;156:1208-1213.[Medline] [Order article via Infotrieve]
4. Rubler S, Scheebaum R, Hammer N. Systolic time intervals in pregnancy and the post-partum period. Am Heart J. 1973;86:182-188.[Medline] [Order article via Infotrieve]
5.
Nixon JV, Murray RG, Leonard PD, Mitchell JH, Blomquist CG. Effects of large variations in preload on left ventricular performance characteristics in normal subjects. Circulation. 1982;65:698-703.
6. Weber KT, Janicki JS, Hefner LL. Left ventricular force-length relations of isovolumic and ejecting contractions. Am J Physiol. 1976;231:337-343.
7. Mahler F, Ross J, O'Rourke RA, Covell JW. Effects of changes in preload, afterload and inotropic state on ejection and isovolumic phase measures of contractility in the conscious dog. Am J Cardiol. 1975;35:626-634.[Medline] [Order article via Infotrieve]
8. Colan SD, Borow KM, Neumann A. Left ventricular end-systolic wall stress-velocity of fiber shortening relation: a load-independent index of myocardial contractility. J Am Coll Cardiol. 1984;4:715-724.[Abstract]
9.
Borow KM, Colan SD, Neumann A. Altered left ventricular mechanics in patients with valvular aortic stenosis and coarctation of the aorta: effects on systolic performance and late outcome. Circulation. 1985;72:515-522.
10. Colan SD, Sanders SP, Borow KM. Physiologic hypertrophy: effects on left ventricular systolic mechanics in athletes. J Am Coll Cardiol. 1987;9:776-783.[Abstract]
11. Colan SD, Sanders SP, Ingelfinger JR, Harmon W. Left ventricular mechanics and contractile state in children and young adults with end-stage renal disease: effect of dialysis and renal transplantation. J Am Coll Cardiol. 1987;10:1085-1094.[Abstract]
12. Graham TP, Franklin RCG, Wyse RKH, Gooch V, Deanfield JE. Left ventricular wall stress and contractile function in childhood: normal values and comparison of Fontan repair versus palliation only in patients with tricuspid atresia. Circulation. 1986;74(suppl I):I-61-I-69.
13. Cooper G, Kent RL, Mann DL. Load induction of cardiac hypertrophy. J Mol Cell Cardiol. 1989;21(suppl V):11-30.
14. Haycock GB, Schwartz GJ, Wisotsky DH. Geometric method for measuring body surface area: a height-weight formula validated in infants, children, and adults. J Pediatr. 1978;93:62-66.[Medline] [Order article via Infotrieve]
15. Colan SD, Borow KM, MacPherson D, Sanders SP. Use of the indirect axillary pulse tracing for noninvasive determination of ejection time, upstroke time, and left ventricular wall stress throughout ejection in infants and young children. Am J Cardiol. 1984;53:1154-1158.[Medline] [Order article via Infotrieve]
16. Grossman W, Jones D, McLaurin LP. Wall stress and patterns of hypertrophy in the human left ventricle. J Clin Invest. 1975;56:56-64.
17.
Devereux RB, Reichek N. Echocardiographic determination of left ventricular mass in man: anatomic validation of the method. Circulation. 1977;55:613-618.
18.
Quinones MA, Gaasch WH, Cole JS, Alexander JK. Echocardiographic determination of left ventricular stress-velocity relations in man: with reference to the effects of loading and contractility. Circulation. 1975;51:689-700.
19. Goldberg SJ, Allen HD, Marz GR, Donnerstein RL. Doppler Echocardiography. 2nd ed. Philadelphia, Pa: Lea & Febiger; 1988:153-186.
20. Lees MM, Taylor SH, Scott DB, Kerr MG. A study of cardiac output at rest throughout pregnancy. J Obstet Gynaecol Br Commonw. 1967;74:319-328.[Medline] [Order article via Infotrieve]
21. Kelly R, Fitchett D. Noninvasive determination of aortic input impedance and external left ventricular power output: a validation and repeatability study of an new technique. J Am Coll Cardiol. 1992;20:952-963.[Abstract]
22.
Longo LD. Maternal blood volume and cardiac output during pregnancy: a hypothesis of endocrinologic control. Am J Physiol. 1983;245:R720.
23. Lang RM, Pridjian G, Feldman T, Neumann A, Lindheimer M, Borow KM. Left ventricular mechanics in preeclampsia. Am Heart J. 1991;121:1768-1775.[Medline] [Order article via Infotrieve]
24. Laird-Meeter K, Van De Ley G, Bom T, Wladimiroff JW, Roelandt J. Cardiocirculatory adjustments during pregnancy: an echocardiographic study. Clin Cardiol. 1979;2:328-332.[Medline] [Order article via Infotrieve]
25.
Robson SC, Hunter S, Boys RJ, Dunlop W. Serial study of factors influencing changes in cardiac output during human pregnancy. Am J Physiol. 1989;256:H1060-H1065.
26. Vered Z, Poler SM, Gibson P, Wlody D, Perez JE. Non-invasive detection of the morphologic and hemodynamic changes during normal pregnancy. Clin Cardiol. 1991;14:327-334.[Medline] [Order article via Infotrieve]
27.
Langille BL, Adamson SL. Thoracic aortic pressure-flow relationships and vascular impedance in fetal sheep. Am J Physiol.. 1992;263:H824-H832.
28. Milnor WR. The normal hemodynamic state. In: Milnor WR, ed. Hemodynamics. 2nd ed. Baltimore, Md: Williams & Wilkins; 1982:135-156.
29. Grossman W. Cardiac hypertrophy: useful adaptation or pathologic process? Am J Med. 1980;69:576-584.[Medline] [Order article via Infotrieve]
30. Laskey WK, Reichek N, St John Sutton M, Untereker WJ, Hirshfeld JW. Matching of myocardial oxygen consumption to mechanical load in human left ventricular hypertrophy and dysfunction. J Am Coll Cardiol. 1984;3:291-300.[Abstract]
31. Weber KT, Janicki JS. Myocardial oxygen consumption: the role of wall force and shortening. Am J Physiol. 1977;233:H421-H477.
This article has been cited by other articles:
 |
|
 |
|
  R. RAMARAJ and V. L. SORRELL Peripartum cardiomyopathy: Causes, diagnosis, and treatment Cleveland Clinic Journal of Medicine, May 1, 2009; 76(5): 289 - 296. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Pagni, B. L. Ganzel, and T. Tabb Hemiarch aortic replacement for acute type A dissection in a Marfan patient with twin pregnancy Interactive CardioVascular and Thoracic Surgery, August 1, 2008; 7(4): 740 - 741. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. M. D. Gonzalez, J. C. Osorio, C. Manlhiot, D. Gruber, S. Homma, and S. Mital Hypertrophy signaling during peripartum cardiac remodeling Am J Physiol Heart Circ Physiol, November 1, 2007; 293(5): H3008 - H3013. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. E.A.K. Bamfo, N. A. Kametas, K. H. Nicolaides, and J. B. Chambers Maternal left ventricular diastolic and systolic long-axis function during normal pregnancy Eur J Echocardiogr, October 1, 2007; 8(5): 360 - 368. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 R. Seth, A. J. Moss, S. McNitt, W. Zareba, M. L. Andrews, M. Qi, J. L. Robinson, I. Goldenberg, M. J. Ackerman, J. Benhorin, et al. Long QT Syndrome and Pregnancy J. Am. Coll. Cardiol., March 13, 2007; 49(10): 1092 - 1098. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 V. Bassien-Capsa, J.-C. Fouron, B. Comte, and A. Chorvatova Structural, functional and metabolic remodeling of rat left ventricular myocytes in normal and in sodium-supplemented pregnancy Cardiovasc Res, February 1, 2006; 69(2): 423 - 431. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 P. Khairy, D. W. Ouyang, S. M. Fernandes, A. Lee-Parritz, K. E. Economy, and M. J. Landzberg Pregnancy Outcomes in Women With Congenital Heart Disease Circulation, January 31, 2006; 113(4): 517 - 524. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Guedes, L.-A. Mercier, L. Leduc, L. Berube, F. Marcotte, and A. Dore Impact of pregnancy on the systemic right ventricle after a Mustard operation for transposition of the great arteries J. Am. Coll. Cardiol., July 21, 2004; 44(2): 433 - 437. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Y. Xia, H. Y. Wen, M. E. Young, P. H. Guthrie, H. Taegtmeyer, and R. E. Kellems Mammalian Target of Rapamycin and Protein Kinase A Signaling Mediate the Cardiac Transcriptional Response to Glutamine J. Biol. Chem., April 4, 2003; 278(15): 13143 - 13150. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. A. Simmons, A. G. Gillin, and R. W. Jeremy Structural and functional changes in left ventricle during normotensive and preeclamptic pregnancy Am J Physiol Heart Circ Physiol, October 1, 2002; 283(4): H1627 - H1633. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Y. H. Wong, S. Kulandavelu, K. J. Whiteley, D. Qu, B. L. Langille, and S. L. Adamson Maternal cardiovascular changes during pregnancy and postpartum in mice Am J Physiol Heart Circ Physiol, March 1, 2002; 282(3): H918 - H925. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Valensise, G. P. Novelli, B. Vasapollo, G. Di Ruzza, M. E. Romanini, M. Marchei, G. Larciprete, D. Manfellotto, C. Romanini, and A. Galante Maternal Diastolic Dysfunction and Left Ventricular Geometry in Gestational Hypertension Hypertension, May 1, 2001; 37(5): 1209 - 1215. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S. Denslow Constraints on cardiac hypertrophy imposed by myocardial viscosity J Appl Physiol, September 1, 2000; 89(3): 1022 - 1032. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 G. D. Pearson, J.-C. Veille, S. Rahimtoola, J. Hsia, C. M. Oakley, J. D. Hosenpud, A. Ansari, and K. L. Baughman Peripartum Cardiomyopathy: National Heart, Lung, and Blood Institute and Office of Rare Diseases (National Institutes of Health) Workshop Recommendations and Review JAMA, March 1, 2000; 283(9): 1183 - 1188. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B.M Weiss and O.M Hess Pulmonary vascular disease and pregnancy: current controversies, management strategies, and perspectives Eur. Heart J., January 2, 2000; 21(2): 104 - 115. [PDF]
|
|
|
|
|
|
D. A. Edouard, B. M. Pannier, G. M. London, J. L. Cuche, and M. E. Safar Venous and arterial behavior during normal pregnancy Am J Physiol Heart Circ Physiol, May 1, 1998; 274(5): H1605 - H1612. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Poppas, S. G. Shroff, C. E. Korcarz, J. U. Hibbard, D. S. Berger, M. D. Lindheimer, and R. M. Lang Serial Assessment of the Cardiovascular System in Normal Pregnancy: Role of Arterial Compliance and Pulsatile Arterial Load Circulation, May 20, 1997; 95(10): 2407 - 2415. [Abstract] [Full Text]
|
|
| |||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||