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Congenital heart disease
Original article
Cardiac adaption during pregnancy in women with congenital heart disease and healthy women
  1. Marlies A M Kampman1,2,
  2. Mattia A E Valente1,
  3. Joost P van Melle1,
  4. Ali Balci3,
  5. Jolien W Roos-Hesselink4,
  6. Barbara J M Mulder5,
  7. A P J van Dijk6,
  8. M A Oudijk7,
  9. M R M Jongbloed8,
  10. Dirk J van Veldhuisen1,
  11. Petronella G Pieper1
  12. on behalf of the ZAHARA II investigators
  1. 1Department of Cardiology, University Medical Center Groningen, University of Groningen, Groningen, The Netherlands
  2. 2The Netherlands Heart Institute (ICIN), Utrecht, The Netherlands
  3. 3Department of Cardiology, Isala Clinic, Zwolle, The Netherlands
  4. 4Department of Cardiology, Erasmus Medical Center, University of Rotterdam, Rotterdam, The Netherlands
  5. 5Department of Cardiology, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  6. 6Department of Cardiology, Radboud University Medical Center, University of Nijmegen, Nijmegen, The Netherlands
  7. 7Department of Obstetrics, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
  8. 8Department of Cardiology, University Medical Center Leiden, University of Leiden, Leiden, The Netherlands
  1. Correspondence to Dr Petronella G Pieper, Department of cardiology, University Medical Centre Groningen, Hanzeplein 1, Groningen 9700 RB, The Netherlands; p.g.pieper{at}umcg.nl

Abstract

Objective Pregnancy in women with congenital heart disease (CHD) is associated with deterioration in cardiac function. However, longitudinal data are scarce. This study describes serial changes in cardiac dimensions and function during pregnancy in women with CHD and compares these with healthy pregnant women (controls).

Methods Eight tertiary centres prospectively enrolled 125 pregnant women with CHD (pregnancy duration <20 weeks). Controls (N=49) were recruited from low-risk midwife practices. Standardised echocardiography at 20 and 32 weeks gestation and 1 year postpartum was performed.

Results Age and parity were comparable between both groups (p>0.1). Left ventricular ejection fraction (LVEF) <45% was present in 3.2% of women with CHD and 14.4% had tricuspid annular plane systolic excursion (TAPSE) <16 mm. Absolute values of ventricular function parameters and diameters were less favourable in women with CHD. No permanent changes occurred in right and left ventricular function parameters and dimensions in women with CHD. The patterns of change in cardiac function and dimensions were comparable between women with CHD and controls, except for LVEF (p=0.026). In women with right-sided CHD the pattern of TAPSE over time differed from controls (p=0.043) (no decrease in TAPSE postpregnancy in CHD). In women with left-sided CHD left ventricular end-diastolic diameter (LVEDD) tended to increase compared with controls (p=0.045).

Conclusions Absolute levels of ventricular function parameters and diameters differ between CHD and controls, but changes during and after pregnancy are generally comparable. However, different patterns over time seen for TAPSE and LVEDD in women with right-sided and left-sided CHD, respectively, compared with controls indicate the importance of echocardiographic follow-up during pregnancy in women with CHD.

https://doi.org/10.1136/heartjnl-2015-308946

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    Introduction

    Pregnancy in women with congenital heart disease (CHD) is associated with increased incidences of cardiovascular, obstetric and neonatal complications.1–5 Cardiac complications, such as arrhythmia and heart failure, are thought to be due to the haemodynamic changes of pregnancy. Depending on the specific underlying congenital defect, pregnancy can be associated with persisting structural cardiac remodelling and deterioration in function, such as dilatation of the subpulmonary ventricle after pregnancy, deterioration of valvular dysfunction and worsening ventricular function.6–10 It is thought that the deterioration starts during pregnancy in these patients. However, the observations in most of these studies were not based on longitudinal data. The majority of data on cardiovascular changes over time during pregnancy is based on studies in healthy women and only a few reports describe longitudinal cardiovascular changes in women with heart disease.11 ,12 Most of the available research focuses on left ventricular (LV) parameters.13 Data examining longitudinal changes in right ventricular (RV) function and dimension are scarce in healthy pregnant women and have never been reported in pregnant women with CHD.14 ,15

    Therefore, the objectives were to describe serial measurements in cardiac dimensions and systolic and diastolic function of the right and left ventricle during pregnancy in women with CHD and to compare the serial measurements in women with CHD with the changes seen in healthy pregnant women.

    Methods

    Study population

    The Zwangerschap bij Aangeboren HARtAfwijkingen II study (ZAHARA; pregnancy in CHD) is a national, prospective multicentre cohort study conducted between March 2008 and August 2011. All consecutive pregnant women with structural CHD, aged ≥18 years, pregnancy duration <20 weeks and presenting in one of the eight participating centres were eligible for enrolment. Healthy pregnant women (non-smokers, no medication use, aged ≥18 years) were recruited from low-risk midwife practices in Groningen and Rotterdam, the Netherlands. The study design and primary results have been published previously.16 ,17

    Only women from the ZAHARA II study with singleton pregnancies and complete echocardiographic follow-up (preconception (only applicable for women with CHD), 20 and 32 weeks gestation, 1 year postpartum) were included for the current study and only the first pregnancy during the study period was taken into account. Women with a systemic right ventricle or Fontan physiology were excluded, since various echocardiographic measurements are not validated for these types of CHDs.

    The Research Ethics Committee of all participating centres approved the study protocol and all participating women gave written informed consent. The ZAHARA II study was supported by a grant from the Netherlands Heart Foundation (2007B75).

    Baseline characteristics and echocardiography

    Baseline characteristics were collected using medical records during the first antepartum visit and included maternal age, underlying CHD, previous interventions, prior cardiac events, cardiac medication use, New York Heart Association (NYHA) functional class, echocardiography data, co-morbid conditions and obstetric history.

    Patients and healthy pregnant women visited the outpatient clinic at 20 and 32 weeks gestation and 1 year postpartum for clinical evaluation (including NYHA class assessment) and standardised echocardiography. All echocardiograms were evaluated offline by one of four experienced cardiologists at the University Medical Center Groningen, Groningen, the Netherlands.

    Transthoracic echocardiographic evaluation was performed according to current guidelines and recommendations, and adapted to the structural defect when necessary.18–21

    Left ventricular end-diastolic and end-systolic diameters (LVEDD, LVESD), as well as the left ventricular outflow tract (LVOT) diameter, were assessed on the parasternal long axis view. LVOT velocity time integral was derived from the apical five-chamber view. Cardiac output was calculated by multiplying LVOT area with the LVOT velocity time integral and heart rate. Left ventricular ejection fraction (LVEF) was determined using Simpson's biplane method using the apical four-chamber view and the apical two-chamber view where possible, otherwise Simpson's monoplane or the eyeballing method was used. Diastolic function was assessed by pulsed wave Doppler of the mitral inflow (E, A, E/A ratio) and colour tissue Doppler of the septal and lateral mitral annulus (E/E′).

    RV function was measured using the tricuspid annular plane systolic excursion (TAPSE) in the apical four-chamber view and the peak systolic colour tissue velocity Doppler of the RV lateral wall assessed at the tricuspid annulus (S′ RV). Maximal right ventricular end-diastolic diameter (RVEDD) was measured using the modified apical four-chamber view. LV systolic dysfunction was defined as an ejection fraction <45%. RV systolic dysfunction was defined as TAPSE <16 mm.

    Statistical analysis

    Continuous variables are presented as mean with SD or medians with IQRs as appropriate. Absolute numbers and percentages are displayed for categorical data.

    To investigate changes in the serial echocardiographic parameters over time in pregnant women with CHD and to compare the serial changes over time with healthy pregnant women, random slope, random intercept linear mixed-effects models were used, adjusted for age, race and parity. Variables were modelled continuously. These hierarchical regression models include fixed and random (subject-specific) effects, allowing for within subject correlation between repeated measurements. As the evolution of parameters during pregnancy might not be linear, patterns were investigated graphically, and polynomial transformations were considered where appropriate. Best fit transformations were selected via combined assessment of Akaike's information criterion (lower is better) for fixed effects and likelihood ratio tests of nested models for random effects. Second degree polynomial transformations for changes over time were selected for the final models. Interaction terms for group membership (pregnant women with CHD vs healthy pregnant women; pregnant women with right-sided CHD vs healthy pregnant women; pregnant women with left-sided CHD vs healthy pregnant women) were introduced as a fixed effect to check for differences in course over time. Based on anatomy and haemodynamics before correction, women with tetralogy of Fallot, atrial septal defects, partial atrioventricular septal defects, pulmonary atresia with intact ventricular septum, Ebstein's anomaly, abnormal pulmonary venous return, sinus venosus defects and pulmonary valve stenosis were classified as having right-sided CHD. Women with ventricular septal defects, aortic valve abnormalities, aortic coarctation, Marfan syndrome, Loeys–Dietz syndrome and with a cleft mitral valve were considered to have left-sided CHD. The patients with transposition of the great arteries with an arterial switch procedure and the patient with a corrected truncus arteriosus were considered non-classifiable in the aforementioned subgroups.

    All statistical analyses were performed using STATA software package (V.11, College Station, Texas, USA) and R: a language and environment for statistical computing (V.3.1.0, R Foundation for statistical computing, Vienna, Austria). A two-tailed p<0.05 was considered significant.

    Results

    During the study period, 213 women with CHD and 70 healthy women were included. Eighty-eight pregnancies in women with CHD were excluded because of a twin pregnancy (n=4), Fontan physiology or a systemic right ventricle (n=15), second pregnancy in the study period (n=9) or incomplete echocardiographic data (n=60), rendering 125 patients available for analysis. In one healthy woman a previously unknown atrial septal defect type II was found and 20 women did not have complete echocardiographic follow-up, resulting in 49 healthy pregnant women included in this analysis.

    Baseline characteristics and underlying congenital defects are displayed in table 1. Mean age was comparable between women with CHD (29.4±4.5 years) and healthy women (30.1±4.1 years). The majority of patients and healthy controls was nulliparous (62.4% vs 61.2%) and most of them were in NYHA functional class I (75.2% vs 98.0%). LV systolic dysfunction was seen in four (3.2%) women with CHD and 15 (12.0%) had RV systolic dysfunction.

    View this table:
    Table 1

    Maternal baseline characteristics (prior to pregnancy)

    Descriptive means over time of the ventricular function parameters and the ventricular dimensions of right and left ventricle are reported in table 2 (number of available measurements are reported in online supplementary table S1). Significant changes over time were seen for the systolic tissue velocity of the right (p=0.026) and left ventricle (0.019) and for RVEDD (0.024) with an augmentation and dilatation, respectively, during pregnancy with return to prepregnancy values postpartum.

    Supplementary table

    Available numbers of echocardiographic measurements on each parameter specified by time point and subgroup.

    View this table:
    Table 2

    Longitudinal echocardiographic parameters in pregnant women with CHD and healthy women

    Deterioration of RV function of ≥1 class (during pregnancy) occurred in 14/122 (11.5%) of the women with CHD. In 7/12 (58.3%) with RV function deterioration during pregnancy RV function recovered postpartum. RV function was defined as normal (TAPSE>16 mm), mildly impaired (TAPSE 13–15 mm), moderately impaired (TAPSE 10–12 mm) or severely impaired (TAPSE<10 mm).

    Deterioration of LV function during pregnancy of ≥1class occurred in 32/125 (25.6%) of the women with CHD. Recovery (LVEF postpartum≥LVEF prepregnancy) 1 year postpartum occurred in 14/32 (43.8%) of the women with deterioration during pregnancy. LV function was defined as normal (LVEF>55%), mildly impaired (LVEF 45%–54%), moderately impaired (LVEF 30%–44%) or severely impaired (LVEF<30%).

    Figure 1 compares the fitted patterns of the RV function parameters and RV dimension between women with CHD and healthy controls. Women with CHD have lower values of RV function parameters (TAPSE and systolic tissue velocity of the right ventricle) compared with healthy women. RVEDD was larger throughout pregnancy compared with healthy women. The changes observed in the entire cohort of women with CHD were comparable with the changes seen in healthy women; no statistically significant differences were found in the slope of any of the parameters, indicating similar patterns of change over time for both populations.

    Figure 1
    Figure 1

    Point estimates derived from the mixed models of right ventricular function parameters for women with congenital heart disease (CHD) (red), and healthy women (blue). (A) Tricuspid annular plane systolic excursion (TAPSE (mm) (n=116 vs 47)); (B) systolic tissue velocity of the right ventricle lateral wall (S′ RV (cm/s) (n=91 vs 39)) and right ventricular end-diastolic diameter (RVEDD (mm) (n=105 vs 41)) (C) Error bars represent 95% CI. p Value represents difference in the slope between women with CHD and healthy controls.

    In women with solely right-sided CHD, the slope of TAPSE over time was significantly different from that in healthy women (p=0.043), with TAPSE remaining unchanged in women with right-sided CHD (table 2).

    The fitted patterns of the LV function parameters and LV dimensions are shown in figure 2. Women with CHD have a worse LV systolic function during pregnancy compared with healthy pregnant women, as displayed by lower LVEF and systolic tissue velocity. LV dimensions are comparable between both groups. The slope of LVEF differed significantly between women with CHD and controls. No statistically significant differences were found in the slope of the other LV parameters between women with CHD and healthy controls, indicating similar patterns of change over time for both populations.

    Figure 2
    Figure 2

    Point estimates derived from the mixed models of left ventricular function parameters for women with congenital heart disease (CHD) (red) and healthy women (blue). (A) Left ventricular ejection fraction (LVEF (%) (n=116 vs 49)); (B) mean systolic tissue velocity of the septal and left ventricular lateral wall (S′ LV (cm/s)(n=87 vs 44)) and left ventricular end-diastolic (C (n=118 vs 49)) and end-systolic (D (n=118 vs 49)) diameter (mm). Error bars represent 95% CI. p Value represents difference in the slope between women with CHD and healthy controls.

    The slope of LVEDD in women with left-sided CHD over time was significantly different from that in healthy women (p=0.045) with LVEDD tending to increase over time in women with left-sided CHD (table 2).

    Discussion

    This is the first study that compares the serial changes in ventricular function parameters and ventricular dimensions during pregnancy in women with CHD with healthy pregnant women. In addition, this is the first study that describes the serial changes in RV parameters seen during and after pregnancy in women with CHD. For the serial changes in the heterogeneous population of women with CHD, significant changes over time were found for the systolic tissue velocity of the right and left ventricle and RVEDD. The serial changes in echocardiographic parameters during pregnancy in women with CHD were comparable with healthy pregnant women, except for LVEF, indicating similar patterns in both populations. However, the absolute levels of ventricular function and dimensions did clearly differ between women with CHD compared with healthy women. For women with right-sided CHD the pattern of TAPSE over time differed from the pattern seen in healthy women. Women with left-sided CHD had a different pattern of LVEDD over time compared with healthy pregnant women.

    Comparison of the results with other studies is difficult since data on cardiac adaption during pregnancy in women with CHD or heart disease in general are very rare. Cornette et al12 described a time effect during pregnancy towards a larger LVESD, lower fractional shortening and lower LVEF. In addition, they found a parabolic effect for E/E′, stroke volume and cardiac output. In this study, statistically significant changes over time were found for RVEDD and for systolic tissue velocity of the right and left ventricle with an augmentation of function parameters and small increase in RVEDD during pregnancy and values returning to baseline postpartum. These parameters were not evaluated before in women with CHD. The results on Doppler peak systolic velocity of the left ventricle differed from those described by Bamfo et al22 in healthy pregnant women. They did not find any change in LV systolic tissue velocity. Compared with healthy women, women with CHD show lower fitted values for LVEF and systolic tissue velocity of the left ventricle (figure 2). Vasapollo et al23 described significant lower LVEF and LV dimensions in healthy women with fetal growth restriction compared with healthy women with uncomplicated pregnancy outcome. The pattern observed in this study is comparable, with lower LVEF and LV dimensions during pregnancy in women with CHD compared with healthy women. Although no deterioration in systolic function or LV dimensions during pregnancy was found, these findings suggest that there might be an impaired potential in women with CHD to provide the required cardiac adaptions necessary to meet the increased metabolic demands of pregnancy, despite the augmentation in systolic tissue velocity observed. This may contribute to the higher obstetric and offspring complication rate in women with CHD, since cardiac dysfunction is related to impaired uteroplacental circulation and offspring complications.17 The smaller LV dimensions may additionally be explained by interaction between right and LV dimensions in women with enlarged right ventricles. The observed difference in pattern of LVEF over time between women with CHD and healthy controls does not indicate worsening of LVEF in women with CHD but seems to be due to an unexplained different pattern seen in healthy women compared with literature.24

    The observed difference in fitted values for LVEDD over time in women with left-sided CHD compared with healthy women may suggest that the volume load of pregnancy is not well tolerated in patients with these types of lesions; however, lesion-specific data are warranted.

    Data on RV function and dimensions during pregnancy are extremely scarce and have never been described in a longitudinal manner for women with CHD. Ducas described an enlargement of the RVEDD during pregnancy in healthy women, which is comparable with our results in women with CHD.15 Vogt et al14 were the first to report on systolic tissue velocities of the right ventricle (S′) during pregnancy in healthy women and did not find a significant change in systolic velocity comparing the first with the third trimester. Ducas et al15 described, in a study using MRI, no change in TAPSE and systolic myocardial velocity of the right ventricle lateral wall in healthy pregnant women during the third trimester compared with postpartum values (which were used as baseline measurement). The results of the current study on RV systolic function in women with CHD show an augmentation of RV systolic tissue velocity, but not of TAPSE. The absolute values in patients are considerably lower compared with the healthy women. TAPSE is related to impaired uteroplacental circulation and offspring complications.17 It might be that the absolute level of RV systolic function is not sufficient to meet the increased demands of pregnancy, leading to adverse obstetric and offspring outcome. The observation that the evolution of TAPSE in women with right-sided CHD is significantly different from the pattern seen in healthy women may also point into that direction. It might be that this subgroup has insufficient capacity to increase TAPSE, in order to accommodate cardiac output, which may contribute to the increased incidence rates of obstetric and offspring complications. Unfortunately, we did not have prepregnancy values in healthy women, but the observation that TAPSE decreased after pregnancy in healthy women likely implies a return to baseline after an increase in early pregnancy. Such increase and return to baseline were not observed in women with CHD with right-sided disease.

    It is known for specific congenital lesions, that is, systemic right ventricles and tetralogy of Fallot, that pregnancy can be associated with persistent deterioration in cardiac function6 ,8 and women with cardiovascular complications during pregnancy are at risk for persistent dilatation of the right ventricle.10 Close follow-up of high-risk patients is still warranted, since small changes in cardiac function in the individual patient might be clinically relevant, although no statistically significant deterioration was found in this study cohort.

    Strengths and limitations

    This is the first study that assessed the serial changes in ventricular function and dimensions during pregnancy in women with CHD and compared these with changes in healthy pregnant women. The comparison with healthy pregnant women is unique and makes the results more valuable. Unfortunately, no data on interobserver variability or intraclass correlation were available.

    Due to the study design echocardiographic data before pregnancy from patients were collected retrospectively and in healthy women preconception echocardiography was not preformed. This hampered the comparison of the serial changes in women with CHD and healthy controls, since preconception data were not included in this analysis. Several high-risk congenital lesions (Fontan physiology and systemic right ventricles) were excluded from analysis. These are the most vulnerable patient groups during pregnancy for cardiac complications and deterioration in cardiac function during and after pregnancy. Excluding these types of patients may underestimate the effects of pregnancy on maternal cardiac function.

    Conclusion

    This study showed that, though absolute values of ventricular function parameters and ventricular dimensions differ between women with CHD and healthy women, pregnancy generally does not lead to deterioration of cardiac function and dimensions in women with CHD. The patterns of change over time seen during pregnancy are comparable between women with CHD and healthy pregnant women. However, the slope of TAPSE over time in women with solely right-sided CHD remained fairly constant and differed significantly from healthy women where TAPSE decreased after pregnancy (which probably reflects a return to baseline after an increase early in pregnancy). In women with left-sided CHD, the slope indicated that LVEDD tended to increase over time, which was significantly different compared with healthy controls.

    These findings indicate that serial follow-up of cardiac function and dimensions during pregnancy in women with CHD is an important part of the management of pregnancy in women with CHD.

    Key messages

    What is already known on this subject?

    • Depending on the underlying congenital defect, pregnancy can be associated with persisting structural cardiac remodelling and deterioration in valvular dysfunction and worsening ventricular function. Only one study describes cardiac function during pregnancy in a longitudinal manner, which found permanent reduction in systolic and diastolic left ventricular (LV) function.

    What might this study add?

    • One hundred and twenty five pregnant women with congenital heart disease (CHD) were compared with 49 healthy pregnant controls. Significant changes over time occurred in systolic tissue velocity of the right (p=0.026) and left ventricle (0.019) and for right ventricular (RV) end-diastolic diameter (0.024): augmentation of systolic tissue velocities and dilatation of RV during pregnancy with return to prepregnancy values postpartum.

    • Women with right-sided CHD had a different pattern over time of tricuspid annular plane systolic excursion compared with healthy controls (p=0.043) (no decrease after pregnancy). Women with left-sided CHD had a different pattern of LV end-diastolic diameter (LVEDD) over time compared with healthy women (p=0.045), with tendency of LVEDD to increase over time.

    How might this impact on clinical practice?

    • These findings indicate that serial follow-up of cardiac function and dimensions during and after pregnancy in women with CHD is an important part of the management of women with CHD.

    Acknowledgments

    The authors thank Dr J P M Hamer for his contribution in evaluating the echocardiograms.

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    Footnotes

    • Contributors The authors MAMK, MAEV and PGP contributed to analysis and interpretation of data; BJMM, JWR-H, JPvM, AB, DJvV, APJvD, MAO, MRMJ and PGP contributed to data conception and design. Furthermore, all authors have drafted or revised the manuscript critically for important intellectual content, and all authors have read and approved the final manuscript.

    • Funding Netherlands Heart foundation (2007B75).

    • Competing interests None declared.

    • Ethics approval Research Ethics Committee of all participating centres approved the study protocol.

    • Provenance and peer review Not commissioned; externally peer reviewed.