Objective
The objective of the study was to evaluate the longitudinal changes in maternal systolic and diastolic function in a series of women carrying an uncomplicated twin pregnancy.
Study Design
A series of women carrying a twin pregnancy underwent standard M-mode, 2-dimensional color Doppler, and tissue Doppler transthoracic echocardiography during the first (11–13 weeks), the second (20–23 weeks), the third (28–32 weeks) trimesters, and the postpartum (6 months after delivery).
Results
From January 2012 to September 2013, 30 women with an uncomplicated twin pregnancy were included in this prospective study. All the pregnancies were diamniotic including 24 dichorionic and 6 monochorionic sets. Overall, 60 live births were observed with a mean gestational age at delivery of 37 ± 1 weeks and a mean birthweight of 2532 ± 313 g. During pregnancy a significant worsening of left ventricle systolic function expressed by ejection fraction, fractional shortening and S1 longitudinal contractility decrease was observed. These findings also persisted at postpartum assessment. Regarding diastolic function, our data showed a significant progressive reduction of pulsed Doppler E-wave velocity and an increase of A-wave from the first to the third trimester. Similar changes were documented for tissue Doppler E1 and A1 peak velocities assessed at the level of the mitral and tricuspid annulus. After delivery diastolic findings returned to values comparable with those obtained in the first trimester.
Conclusion
In uncomplicated twin gestations, significant changes in maternal systolic and diastolic function occur from the first to the third trimester. Moreover, although diastolic parameters normalize after pregnancy, a relative systolic dysfunction seems to persist after delivery.
Maternal cardiac function assessment in pregnancy has recently gained much interest because abnormal findings at echocardiography have been associated with a higher risk of obstetric complications including hypertensive disorders and placental insufficiency. Most of the studies have been carried out among singleton gestations, whereas a paucity of data is available on maternal hemodynamics in twins.
On the other hand, considering the greater increase in circulating volume that is expected in twin gestation, a detailed assessment of maternal cardiac changes throughout the pregnancy might offer a better insight to the process of cardiac adaptation to the multifetal pregnancy.
In a large cross-sectional study, Kametas et al documented a significantly higher maternal CO among twin vs singleton gestations.
More recently in a group of women with uncomplicated twin gestations submitted to serial echocardiography from 20 to 34 weeks, our group had noted a progressive increase of CO and a fall of total vascular resistances. Furthermore, compared with uneventful pregnancies, in those twin gestations complicated by preeclampsia or placental insufficiency, either CO or total peripheral vascular resistance (TVR) did not show significant changes from the second to the third trimester.
Data regarding maternal cardiac function since the first trimester and diastolic changes are lacking, with the only available studies including small numbers of patients.
The aim of this study was to assess by serial echocardiograms maternal cardiac function among uncomplicated twin gestations since the first trimester and to compare these sonographic findings with those obtained after pregnancy.
Materials and Methods
We conducted a prospective longitudinal study that included patients with a viable twin pregnancy who attended the Department of Obstetrics of Bologna University Hospital at 11–13 weeks of gestation for the first-trimester screening of aneuploidies.
A priori exclusion criteria were personal history of cardiovascular disease or chronic hypertension, systemic maternal disorders, smoking, or drug consumption. Patients were also excluded if at the time of ultrasound an increased nuchal translucency or a major structural anomaly was noted in 1 or both fetuses. At ultrasound performed at 11–13 weeks, the chorionicity and amnionicity were established.
Patients were defined as having a complicated pregnancy and retrospectively removed from the study group if any of the following occurred after recruitment: miscarriage or intrauterine fetal death, congenital anomaly or disease diagnosed at birth, spontaneous or indicated delivery less than 34 weeks; small-for-gestational-age birthweight of 1 or both twins (below the third centile), occurrence of maternal gestational hypertension (systolic blood pressure of ≥140 mm Hg and/or diastolic blood pressure of ≥90 mm Hg on at least 2 occasions in women known to be normotensive before pregnancy and before 20 weeks of gestation), or preeclampsia (gestational hypertension plus proteinuria of ≥300 mg per 24 hours).
All women included in the study underwent a complete cardiological evaluation including both a clinical and a transthoracic echocardiographic study at 11–13 weeks, 20–23 weeks, 28–32 weeks, and 6 months after delivery.
The cardiological evaluation was performed by D.d.E. and M.R. and included the collection of medical and family history; body measurement assessment; blood pressure profile; and complete M-mode, 2-dimensional, and color Doppler echocardiography, comprehensive of tissue Doppler (TD) evaluation.
Blood pressure was measured 3 times at 5 minute intervals, in patients lying in the left lateral position, with an appropriate size sphygmomanometer, after 10 minutes of rest. If the diastolic blood pressure detected exceeded 90 mm Hg or the systolic blood pressure exceeded 140 mm Hg, the measurement was then repeated after 30 minutes following an examination.
In all subjects a standard M-mode, 2-dimensional, color Doppler, and TD echocardiography was performed by the same experienced operator, using a suitable commercially available instrumentation (SONOS 5500; Royal Philips, Breitner Center, Amsterdam, The Netherlands) according to international guidelines for echocardiography of the American College of Cardiology Foundation/American Heart Association. The echocardiographic tracings were recorded simultaneously during the examination.
Methods of maternal cardiac assessment have been thoroughly described in a previous study published by our group. The parameters used to assess systolic function were left ventricular (LV) end-diastolic volume; LV end-systolic volume; LV ejection fraction calculated with the Teichholz’s formula derived from LV M-mode dimensions; LV fractional shortening, also calculated using LV M-mode measurements; CO (liters per minute) calculated with the formula CO = SV * HR (where HR is the heart rate and SV is the stroke volume); and the TVR calculated with the formula TVR = (mean arterial pressure/CO) * 80 (dynes/sec –1 per centimeter –5 ).
As for diastolic function, E-wave peak velocity, A-wave peak velocity, E/A ratio, and isovolumetric relaxation time were measured. We also assessed pulsed TD, including the systolic anterograde myocardial velocity (S 1 ) and the 2 retrograde diastolic myocardial velocities: protodiastolic (E 1 ) and atrial (A 1 ), all measured in centimeters per second. The TD sampling has been done on the mitral annulus, in both septal and left ventricle’s side, and on the tricuspid annulus.
All tracings were recorded at the held-end expiration with the patient in the left lateral decubitus position and after 20 minutes of rest, measured on 3 separate beats and then averaged to reduce the variability in calculation. All the echocardiography examinations were performed by the same expert operator. The within-study variability of our individual measurements around the mean averaged ±3%.
The obstetric management of the women enrolled was independent of echocardiographic findings and conducted by physicians not involved in the study. The data relating to the clinical history of pregnancy and to the childbirth were collected by means of medical records or telephone interviews for patients who were not delivered at our hospital.
Ethics
The study protocol conforms to the ethical guidelines of the World Medical Association (WMA) Declaration of Helsinki–Ethical Principles for Medical Research Involving Human Subjects adopted by the 18th WMA General Assembly (Helsinki, Finland, June 1964) and amended by the 59th WMA General Assembly (Seoul, South Korea, October 2008). A consent form signed at recruitment was obtained from each eligible patient.
Statistical analysis
Numerical data are reported as mean ± SD. Data obtained were processed statistically using SPSS software (version 19.0 for Windows; SPSS Inc, Chicago, IL). Variables were compared using the Friedman or ANOVA test as appropriate. All multiple comparisons were planned a priori, and therefore, no statistical corrections needed to be made. A value of P < .05 was considered statistically significant and all tests were 2 sided.
Results
During the study period, 38 twin pregnancies were considered eligible for the study and prospectively enrolled. Of these, 8 cases were subsequently excluded because of miscarriage less than 24 weeks (n = 2), delivery prior to 34 weeks (n = 1), preeclampsia after 34 weeks (n = 2), small-for-gestational-age birthweight of a twin (n = 2), or single intrauterine fetal death (n = 1). Thus, the study group analyzed consisted of 30 uncomplicated twin gestations that completed the 4 steps of echocardiographic assessment.
Demographic and pregnancy details of the study population are presented in Table 1 . Among the study group, all pregnancies were diamniotic, and the vast majority of them were dichorionic (24, or 80%).
| Characteristics | Uncomplicated (n = 30) | Complicated (n = 8) |
|---|---|---|
| Maternal age, y | 36.5 ± 4.8 | 36.3 ± 4.5 |
| Maternal ethnicity, % | ||
| White | 29 (96.7%) | 7 (87.5%) |
| Afro-Caribbean | 1 (3.3%) | 1 (12.5%) |
| Parity | ||
| 0 | 25 (83.3%) | 7 (87.5%) |
| 1 | 4 (13.3%) | 1 (12.5%) |
| 2 | 1 (3.3%) | 0 |
| Gestational age at delivery, wks | 37 ± 1 | 35 ± 3 |
| Birthweight, g | 2535 ± 313 | 2155 ± 638 |
| Chorionicity | ||
| Monochorionic | 6 (20%) | 1 (12.5%) |
| Dichorionic | 24 (80%) | 7 (87.5%) |
| Conception | ||
| Spontaneous | 20 (66.7%) | 5 (62.5%) |
| Medically assisted procreation | 10 (33.3%) | 3 (37.5%) |
The mean gestational age at delivery was 37 ± 1 weeks and the mean weight of the infants at birth was 2532 ± 313 g.
A summary of the maternal cardiac findings obtained at the 4 scheduled examinations are presented in Tables 2 and 3 . In the study population, significantly lower diastolic blood pressure and mean blood pressure in the second trimester in comparison with the values observed both in the first trimester or in the third trimester and postpartum were documented.
| Variable | First trimester | Second trimester | Third trimester | PP | 1 vs 2 | 2 vs 3 | 1 vs 3 | 1 vs PP | 2 vs PP | 3 vs PP | P value |
|---|---|---|---|---|---|---|---|---|---|---|---|
| BMI, kg/m 2 | 22.79 ± 3.52 | 24.90 ± 3.40 | 25.97 ± 2.79 | 22.24 ± 3.12 | .005 | .163 | .001 | .549 | .004 | .001 | < .001 |
| BSA, m 2 | 1.70 ± 0.15 | 1.77 ± 0.15 | 1.81 ± 0.15 | 1.69 ± 0.16 | .021 | .326 | .007 | .685 | .073 | .012 | .017 |
| SBP, mm Hg | 111.00 ± 8.44 | 105.45 ± 9.17 | 109.00 ± 12.54 | 110.48 ± 10.23 | .014 | .264 | .385 | .802 | .079 | .654 | .381 |
| DBP, mm Hg | 65.07 ± 7.69 | 58.59 ± 8.90 | 65.72 ± 10.56 | 66.66 ± 6.36 | .003 | .006 | .765 | .380 | .001 | .726 | .009 |
| MBP, mm Hg | 80.37 ± 7.56 | 74.21 ± 8.50 | 80.15 ± 10.51 | 81.26 ± 6.96 | .003 | .022 | .876 | .601 | .003 | .674 | .047 |
| HR, bpm | 82.35 ± 9.89 | 83.72 ± 13.18 | 80.87 ± 20.06 | 69.13 ± 9.83 | .563 | .617 | .830 | < .001 | < .001 | .010 | < .001 |
| CO, L/min | 5.50 ± 1.11 | 6.31 ± 1.16 | 6.29 ± 0.92 | 4.49 ± 0.71 | .010 | .847 | .002 | < .001 | < .001 | < .001 | < .001 |
| TVR, dynes/s –1 per centimeter –5 | 1219.39 ± 293.66 | 978.30 ± 243.49 | 1038.17 ± 199.10 | 1483.55 ± 277.25 | .001 | .443 | .002 | .001 | < .001 | < .001 | < .001 |
| EF, % | 72.81 ± 4.50 | 69.89 ± 5.96 | 69.43 ± 6.35 | 67.62 ± 5.08 | .006 | .733 | .008 | < .001 | .116 | .231 | < .001 |
| FS, % | 41.91 ± 3.85 | 39.67 ± 4.92 | 39.39 ± 3.73 | 37.64 ± 3.92 | .010 | .815 | .025 | < .001 | .083 | .176 | < .001 |
| LVMI 2 , g/m 2 | 69.88 ± 17.62 | 78.61 ± 19.93 | 79.03 ± 23.29 | 72.42 ± 20.67 | .152 | .964 | .263 | .644 | .255 | .291 | .129 |
| RWT | 0.36 ± 0.04 | 0.35 ± 0.03 | 0.38 ± 0.05 | 0.35 ± 0.04 | .933 | .080 | .152 | .857 | .825 | .065 | .102 |
| Variable | First trimester | Second trimester | Thirrd trimester | PP | 1 vs 2 | 2 vs 3 | 1 vs 3 | 1 vs PP | 2 vs PP | 3 vs PP | P value |
|---|---|---|---|---|---|---|---|---|---|---|---|
| MV max vel E, cm/s | 82.38 ± 13.14 | 78.57 ± 16.48 | 69.96 ± 17.27 | 82.20 ± 16.46 | .258 | .102 | .005 | .230 | .688 | .192 | .041 |
| MV max vel A, cm/s | 58.86 ± 11.03 | 63.67 ± 13.05 | 65.70 ± 11.53 | 53.34 ± 11.09 | .150 | .519 | .038 | .022 | .004 | .001 | .013 |
| MV E/A | 1.42 ± 0.27 | 1.29 ± 0.35 | 1.09 ± 0.22 | 1.46 ± 0.27 | .042 | .028 | < .001 | .697 | .061 | < .001 | < .001 |
| LV IVRT, s | 0.0879 ± 0.0083 | 0.0868 ± 0.0086 | 0.0871 ± 0.0098 | 0.093 ± 0.0082 | .648 | .873 | .698 | .007 | .003 | .024 | .018 |
| MV DtE, s | 0.20 ± 0.03 | 0.19 ± 0.04 | 0.18 ± 0.04 | 0.20 ± 0.04 | .670 | .187 | .071 | .344 | .260 | .026 | .413 |
Regarding the geometric pattern of left ventricle, the various indices of left ventricular mass showed no significant differences throughout the pregnancy. In particular, the left ventricular mass indexed to body surface area (LVMI2), showed a nonsignificant increase from the first to the third trimester returning comparable with early pregnancy soon after delivery.
Regarding the classical parameters of LV systolic function, a significant rise of cardiac output from the first to the second trimester (5.50 ± 1.11 vs 6.31 ± 1.16 L/min; P = .010) was noted, whereas these values remained stable in the third trimester and underwent an even deeper reduction after delivery (6.29 ± 0.92 vs 4.49 ± 0.71 L/min; P < .001). Total vascular resistance, instead, had an opposite trend with a significant fall from the first to the second trimester (1219.39 ± 293.66 vs 978.30 ± 243.49 dynes/s –1 per centimeter –5 ; P = .001), a subsequent plateau toward the late gestation and a more pronounced increase after delivery.
Interestingly both ejection fraction (EF) and fractional shortening (FS) showed a significant progressive decrease from the first to the second trimester and thereafter stabilized on values that also remained low at the postpartum assessment (72.81% ± 4.50% vs 69.89% ± 5.96%, P < .001, and 41.91% ± 3.85% vs 39.67% ± 4.92%, P < .001, respectively, for EF and FS from the first to the second trimester).
Still regarding the systolic function, at tissue Doppler the S1 wave measured at the septal mitral annulus, which can be considered an indicator of longitudinal contractility, had slightly significantly higher values during pregnancy than after delivery (first trimester vs postpartum, P < .001; second trimester vs postpartum, P = .025; third trimester vs postpartum, P = .002). A similar although not significant trend was observed for the lateral mitral annulus S1 wave.
A summary of diastolic function findings is presented in Table 4 . Regarding LV diastolic function, our data showed a significant progressive reduction of pulsed Doppler E-wave velocity and an increase of A-wave from the first to the third trimester. Both these parameters returned at values similar to those of the first trimester in the postpartum period.
| Variable | First trimester | Second trimester | Third trimester | PP | 1 vs 2 | 2 vs 3 | 1 vs 3 | 1 vs PP | 2 vs PP | 3 vs PP | P value |
|---|---|---|---|---|---|---|---|---|---|---|---|
| Septal mitral annulus | |||||||||||
| S1, cm/s | 8.90 ± 1.19 | 8.27 ± 1.64 | 9.13 ± 1.68 | 7.40 ± 1.05 | .186 | .184 | .546 | < .001 | .025 | .002 | < .001 |
| E1, cm/s | 11.53 ± 2.43 | 10.44 ± 2.52 | 8.57 ± 2.58 | 10.50 ± 1.98 | .046 | .035 | .001 | .096 | .990 | .008 | < .001 |
| A1, cm/s | 7.74 ± 1.81 | 8.72 ± 1.45 | 8.52 ± 1.92 | 6.46 ± 1.10 | .021 | .426 | .145 | .012 | < .001 | < .001 | < .001 |
| E1/A1 | 1.59 ± 0.59 | 1.23 ± 0.38 | 1.05 ± 0.39 | 1.66 ± 0.41 | .008 | .237 | .001 | .590 | .001 | < .001 | < .001 |
| Lateral mitral annulus | |||||||||||
| S1, cm/s | 11.77 ± 2.95 | 9.54 ± 3.27 | 10.32 ± 2.50 | 9.63 ± 1.35 | .030 | .091 | .164 | .006 | .456 | .006 | .249 |
| E1, cm/s | 17.65 ± 2.45 | 15.81 ± 2.70 | 12.57 ± 3.37 | 14.53 ± 2.83 | .021 | .006 | < .001 | .001 | .403 | .143 | < .001 |
| A1, cm/s | 8.73 ± 2.91 | 9.40 ± 2.14 | 8.17 ± 2.44 | 7.84 ± 1.88 | .389 | .120 | .338 | .201 | .012 | .090 | .122 |
| E1/A1 | 2.28 ± 0.94 | 1.77 ± 0.50 | 1.67 ± 0.64 | 1.96 ± 0.62 | .043 | .863 | .024 | .110 | .162 | .024 | .331 |
| E/E1 | 5.76 ± 1.08 | 6.01 ± 1.57 | 6.91 ± 1.98 | 6.21 ± 1.38 | .575 | .283 | .039 | .330 | .786 | .548 | .243 |
| Tricuspidal annulus | |||||||||||
| S1, cm/s | 13.84 ± 1.64 | 14.40 ± 1.47 | 15.42 ± 3.82 | 11.46 ± 1.93 | .105 | .116 | .128 | .037 | .001 | .002 | .034 |
| E1, cm/s | 15.68 ± 3.48 | 14.69 ± 3.61 | 11.89 ± 3.67 | 12.13 ± 2.99 | .971 | .390 | .204 | .038 | .043 | .369 | .566 |
| A1, cm/s | 14.50 ± 3.18 | 12.63 ± 2.62 | 12.91 ± 3.55 | 8.48 ± 2.45 | .860 | .973 | .980 | .009 | .002 | < .001 | .001 |
| E1/A1 | 1.23 ± 0.47 | 1.16 ± 0.30 | 0.91 ± 0.35 | 1.45 ± 0.23 | .513 | .724 | .235 | .291 | .063 | < .001 | .056 |
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