Abstract
Background: During a healthy pregnancy women experience cardiovascular and hemodynamic changes and normal ranges of left ventricular (LV) function on two-dimensional speckle tracking echocardiography (STE) are not well defined. The aim of this study was to describe the cardiovascular changes that occur during the second and third trimesters of a healthy pregnancy using STE. Methods: Pregnant subjects were enrolled retrospectively if they underwent a transthoracic echocardiography (TTE) between 2011-2014. Subjects with abnormal TTE findings, hypertension, diabetes, preeclampsia, prior cardiac surgery, poor imaging quality or in the 1st trimester were excluded. A total of 74 pregnant subjects were categorized into the 2nd or 3rd trimesters. Twenty-one healthy age-matched females were selected as a control group. Results: The heart undergoes extensive remodeling during pregnancy with increased LV septal thickness, posterior wall thickness, cavity size and mass (p=0.045, p=0.002, p<0.001, p=0.018, respectively). However, myocardial mechanical function measured by: global longitudinal strain, radial strain, circumferential strain, systolic and diastolic global longitudinal strain rate (GLSR), global radial strain rate (GRSR) and global circumferential strain rate, remains preserved. Only time to peak strain rate corrected for heart rate for diastolic GRSR and diastolic GLSR were significantly increased in the third trimester (p=0.016 for both). Conclusion: Despite extensive heart remodeling, many STE derived parameters of LV function in healthy pregnant women remain unchanged and valid for women in the 2nd and 3rd trimester. Future studies investigating early detection of pregnancy related heart disease can refer to these parameters as reference ranges.
Keywords: Two-dimensional speckle tracking echocardiography, strain, pregnancy
Introduction
The cardiovascular system of women during pregnancy undergoes a unique set of physiological changes. There is a decrease in systemic vascular resistance leading to a decrease in left ventricular (LV) hemodynamic afterload, and an increase in blood volume leading to an increase in venous preload [1,2]. These hemodynamic changes are accompanied by cardiac remodeling including: an increase in LV wall thickness, an increase in LV cavity size and an increase in LV mass [3,4]. However, LV systolic and diastolic strain function remains poorly characterized during a normal pregnancy [3]. Two-dimensional speckle tracking echocardiography (STE) allows for indepth quantification of global and regional LV mechanical function and reference values for healthy non-pregnant individuals have been reported [5-8]. Yet for women during a healthy pregnancy, previous studies have reported conflicting unchanged or decreased systolic strain function [9,10]. Establishing reference values for systolic and diastolic strain function during a healthy pregnancy is critical for the evaluation of pregnancy-related heart disease. Therefore this study was undertaken to explore the strain function of the LV in healthy pregnant women and define normal references values for the second and third trimesters.
Methods
Study design and patient population
In this retrospective cohort study pregnant subjects who were referred for transthoracic echocardiography (TTE) were identified using Montefiore Medical Center’s echocardiography database between April 2011 and May 2014. Healthy pregnancy was defined as pregnant women without pre-eclampsia, seizure disorder, hypertension, non-gestational diabetes and renal disease. Subjects with suboptimal imaging quality for STE, a history of hypertension, non-gestational diabetes, sickle cell disease, pre-eclampsia, in first trimester or have abnormal findings on TTE were excluded. Abnormal TTE was defined as: 1) dilation of at least one of the 4 cardiac chambers beyond normal reference dimension [11] 2) LV ejection fraction (LVEF) <55% or right ventricular dilation or hypokenesis, 3) moderate or worse valvular disease, 4) presence of a pathological (more than small amount) pericardial effusion, 5) corrected or uncorrected cyanotic or non-cyanotic congential heart disease, 6) presence of diastolic dysfunction. First, second and third trimester were defined as 1-12 weeks, 13-26 weeks and 27-42 weeks, respectively. Twenty-one age-matched, non-pregnant female subjects without history of hypertension, diabetes, hyperlipidemia, smoking or other comorbidities were selected as a healthy control population. All medical information was retrospectively obtained through electronic medical record system. The Montefiore Medical Center and Albert Einstein College of Medicine Institutional Review Board approved the study.
Transthoracic echocardiography
All subjects underwent standard TTE (Philips IE33, Philips Medical, Andover, MA). All images were recorded according to the American Society of Echocardiography guidelines [12]. Parasternal long axis, short axis and 2, 3 and 4-chamber apical views were recorded with the patient at left lateral position. LV systolic and diastolic diameter, inter-ventricular septal thickness and posterior wall thickness were measured at the parasternal long axis view. Doppler images were used to measure mitral inflow deceleration time (DT) and E/A at appropriate views. Tissue Doppler imaging was used to measure E/e’. LV mass was calculated using the Devereux formula [13]. Relative wall thickness (RWT) was calculated as 2 x (LV posterior wall thickness/LV end-diastolic diameter). It was considered increased when it was RWT >0.42 [11]. Pulmonary artery pressure was obtained by adding the central venous pressure to 4 x (maximum velocity of tricuspid regurgitation)2 [14]. Augmentation index was calculated as stroke volume index/pulse pressure [15]. All images were digitally stored to Xcelera R3.1L1 workstations (Philips, Andover, MA) and all measurements were performed by physician echocardiographers.
Speckle tracking echocardiography
Offline analysis was performed with Syngo Velocity Vector Imaging software version 3.5 (Siemens Healthcare, Erlangen, Germany). Strain analysis for pregnant and non-pregnant subjects was performed by two blinded observers. The endocardium of the LV was manually traced at the end-diastolic phase using simultaneous electrocardiography monitoring. Tracing of the epicardium was automatically performed by the software and was manually corrected when appropriate to maximize tracking accuracy. STE was deemed sufficient when all 6 segments were considered to be adequate in apical and parasternal views.
Global radial strain (GRS) and strain rate (GRSR), global circumferential strain (GCS) and strain rate (GCSR) were calculated from the six segments of the parasternal short axis view at the papillary muscle level. Global longitudinal strain (GLS) and strain rate (GLSR) were calculated from the 18 segments of the 2, 3 and 4- chamber apical views. Time to peak (TTP) values were recorded for each strain measurement. STE analysis was performed with imaging stored in digital imaging and communications in medicine (DICOM) format at 30 frames/sec.
Statistical analysis
All continuous variables are reported as mean ± standard deviation. All categorical variables are reported as a number (percentage). Comparison of categorical variables was performed using the Chi-squared and if significant difference was detected, then the two-tailed Fischer exact test was used in post-hoc analysis. All continuous variables were confirmed to be normally distributed using the Shapiro-Wilk test. Comparison of continuous variables was performed using the ANOVA test; and if significant difference was detected, then a two-tailed Tukey test was used in post-hoc analysis. A p-value <0.05 was considered significant. Intraclass correlation coefficients (ICC) were calculated to assess intra-observer and inter-observer variability of the strain measurements GLS, GLSR, GCS, GCSR, GRS and GRSR by performing duplicate strain analysis on ten randomly selected patients. Statistical analysis was performed using SPSS Ver. 19 (IBM, Chicago, IL).
Results
Patient characteristics
222 pregnant subjects who were referred for TTE were identified during the study period. Of this population, 115 patients were excluded for abnormal TTE results, 10 for suboptimal STE imaging, 4 for hypertension, 1 for type 1 diabetes, 1 for sickle cell disease, 2 for pre-eclampsia, 6 for being in the first trimester and 9 for missing relevant clinical information, therefore leaving 74 normal pregnant patients for analysis. Twenty-one non-pregnant women without comorbidities were selected as an age-matched control group from the same time period.
The 74 pregnant subjects had a mean age of 29±6 years, a mean body mass index (BMI) of 30±6.9 kg/m2, a mean body surface area (BSA) of 1.82±0.18 m2 and were in a mean gestational week of 26 weeks. Thirty-seven patients were in the second trimester and 37 pateints were in the third trimester. There were no statistical differences between pregnant and control groups regarding age, BSA, BMI, heart rate (HR) or pulse pressure (Table 1). Pregnant subjects did have a significantly lower mean diastolic blood pressure compared to controls (p=0.03).
Table 1.
Population demographics and comorbidities
| Variables | A) Female controls | B) Second trimester | C) Third trimester | p value |
|---|---|---|---|---|
| Demographics | ||||
| N | 21 | 37 | 37 | |
| Age (years) | 30±6 | 29±6 | 29±6 | 0.556 |
| Gestational week (week) | - | 21±6 | 33±4 | |
| BSA (m2) | 1.76±0.17 | 1.80±0.20 | 1.84±0.16 | 0.162 |
| BMI (kg/m2) | 27±6 | 29±7 | 31±7 | 0.152 |
| Mean daytime SBP (mmHg) | 115±11 | 108±11 | 110±15 | 0.150 |
| Mean daytime DBP (mmHg) | 72±10bb,cc | 64±9aa | 64±9aa | 0.003 |
| Mean daytime PP (mmHg) | 44±9 | 44±8 | 48±9 | 0.107 |
| Twin pregnancy | - | 4 (11) | 2(5) | 0.674 |
| C-section | - | 8 (22) | 13 (35) | <0.001 |
| Comorbidities, n (%) | ||||
| Hyperlipidemia | 0 | 2 (5) | 1 (3) | 0.522 |
| Gestational diabetes mellitus | 0 | 0 | 2 (4) | 0.562 |
|
| ||||
| BSA: Body surface area, BMI: Body mass index, SBP: Systolic blood pressure, DBP: Diastolic blood pressure, PP: Pulse pressure. | ||||
|
| ||||
| Key | p<0.05 | p≤0.01 | p≤0.001 | |
|
| ||||
| a- vs Controls | a | aa | aaa | |
| b- vs 2nd Trimester | b | bb | bbb | |
| c- vs 3rd Trimester | c | cc | ccc | |
Cardiac remodeling
Pregnant subjects were found to have significantly increased interventricular septal thickness (p=0.002), significantly increased posterior wall thickness (p<0.001), significantly increased LV mass index (p=0.018) and significantly increased left atrial volume (p=0.006) as compared to non-pregnant controls (Table 2). No significant difference was detected in dimensional measurements between the second and third trimester patient groups.
Table 2.
Echocardiographic measurements
| Variables | A) Female controls | B) Second trimester | C) Third trimester | p value |
|---|---|---|---|---|
| Dimensions | ||||
| Interventricular septum (cm) | 0.77±0.12c | 0.81±0.10 | 0.84±0.11a | 0.045 |
| Posterior wall thickness (cm) | 0.75±0.14c | 0.82±0.10 | 0.86±0.10a | 0.002 |
| LV Dimension, diastole (cm) | 4.5±0.3 | 4.8±0.4 | 4.7±0.4 | 0.05 |
| LV Dimension, systole (cm) | 2.8±0.3bbb,c | 3.2±0.3aaa | 3.0±0.4a | <0.001 |
| DT (sec) | 0.20±0.03 | 0.20±0.04 | 0.21±0.04 | 0.706 |
| LV Mass index (g/m2) | 63±12b,c | 71±9a | 72±14a | 0.018 |
| Relative wall thickness | 0.34±0.07 | 0.35±0.07 | 0.37±0.05 | 0.145 |
| LVEF (%) | 62±3 | 62±4 | 63±4 | 0.302 |
| Volumes | ||||
| LA Volume (ml) | 36±7bb,c | 44±14aa | 44±13a | 0.006 |
| LAVI (LAV/BSA, ml/m2) | 20±4bb,c | 25±6aa | 24±7a | 0.010 |
| Doppler | ||||
| RSVP (mmHg) | 28±5 | 30±5 | 30±5 | 0.573 |
| E/A | 1.7±0.5 | 1.7±0.5 | 1.5±0.4 | 0.706 |
| E/e’ | 5.4±1.4 | 5.6±1.4 | 6.1±2.3 | 0.323 |
| Arterial impedance | ||||
| SVR (dynes·sec·cm-5) | 1690±520bbb,ccc | 1294±303aaa | 1152±351aaa | P<0.001 |
| AI (%) | 54±24 | 55±15 | 47±19 | 0.176 |
|
| ||||
| LV: Left ventricular, DT: deceleration time, LVEF: Left ventricle ejection fraction, LA: Left atrium, RVSP: Right ventricular systolic pressure, LAVI: Left atrium volume index, SVR: Systemic vascular resistence, AI: Augmentation index. | ||||
|
| ||||
| Key | p<0.05 | p≤0.01 | p≤0.001 | |
|
| ||||
| a- vs Controls | a | aa | aaa | |
| b- vs 2nd Trimester | b | bb | bbb | |
| c- vs 3rd Trimester | c | cc | ccc | |
Systolic and diastolic mechanical function on strain analysis
Table 3 summarizes the results of STE-derived values for systolic and diastolic mechanical function. Overall, pregnant women in both trimesters had preserved cardiac function similar to non-pregnant healthy controls. GRS, GCS, GLS, systolic and early diastolic GRSR, GCSR and GLSR were unchanged from the control group. Early diastolic GLSR time to peak (TTP) corrected for HR (GLSR TTP/HR) was found to be increased in pregnant women in the third trimester compared to controls or the second trimester patients (0.56±0.08 vs 0.61±0.07, respectively, p=0.016). Diastolic GRSR TTP corrected for HR (GRSR TTP/HR) was also significantly increased in the third trimester compared to controls (0.54±0.09 vs 0.62±0.10, respectively, p=0.016).
Table 3.
Comparison of strain based on trimester
| Variable | A) Female Controls | B) Second Trimester | C) Third Trimester | p value | |
|---|---|---|---|---|---|
| Longitudinal Strain | |||||
| Basal Strain (%) | -18.4±3.4 | -18.3±3.6 | -18.2±4.8 | 0.983 | |
| Medial Strain (%) | -18.7±3.7 | -18.4±3.7 | -18.0±3.7 | 0.756 | |
| Apical Strain (%) | -24.0±4.2 | -23.1±4.8 | -23.6±42 | 0.750 | |
| GLS (%) | -20.3±3.4 | -19.9±3.2 | -19.9±3.4 | 0.884 | |
| GLS TTP/HR | 0.35±0.05 | 0.35±0.5 | 0.37±0.04 | 0.489 | |
| GLSR- systolic (1/s) | -1.31±0.24 | -1.25±0.21 | -1.31±0.24 | 0.512 | |
| GLSR TTP/HR- systolic | 0.23±0.04 | 0.22±0.04 | 0.24±0.12 | 0.619 | |
| GLSR- diastolic (1/s) | 1.48±034 | 1.46±0.29 | 1.49±0.30 | 0.941 | |
| GLSR TTP/HR- diastolic | 0.56±0.08 | 0.56±0.08c | 0.61±0.07b | 0.016 | |
| Circumferential Strain | |||||
| GCS (%) | -28.5±6.6 | -25.3±5.2 | -25.7±4.3 | 0.070 | |
| GCS TTP/HR | 0.40±0.07 | 0.41±0.06 | 0.41±0.07 | 0.746 | |
| GCSR- systolic (1/s) | -2.00±0.46 | -1.76±0.41 | -1.88±0.41 | 0.114 | |
| GCSR TTP/HR- systolic | 0.22±0.04 | 0.23±0.04 | 0.23±0.04 | 0.773 | |
| GCSR- diastolic (1/s) | 2.18±0.63 | 1.93±0.53 | 1.98±0.54 | 0.234 | |
| GCSR TTP/HR- diastolic | 0.55±0.09 | 0.56±0.08 | 0.59±0.08 | 0.157 | |
| Radial Strain | |||||
| GRS (%) | 28.7±11.7 | 25.8±7.6 | 26.4±8.5 | 0.492 | |
| GRS TTP/HR | 0.39±0.08 | 0.40±0.06 | 0.41±0.07 | 0.620 | |
| GRSR- systolic (1/s) | 1.45±0.44 | 1.35±0.51 | 1.35±0.41 | 0.631 | |
| GRSR TTP/HR- systolic | 0.19±0.05 | 0.20±0.06 | 0.18±0.06 | 0.460 | |
| GRSR- diastolic (1/s) | -1.53±0.56 | -1.46±0.45 | -1.48±0.63 | 0.876 | |
| GRSR TTP/HR- diastolic | 0.54±0.09c | 0.58±0.09 | 0.62±0.10a | 0.016 | |
|
| |||||
| GLS: Global longitudinal strain, GLSR: Global longitudinal strain rate, TTP: Time to peak, HR: Heart rate, GCS: Global circumferential strain, GCSR: Global circumferential strain rate, GRS: Global radial strain, GRSR: Global radial strain rate. | |||||
|
| |||||
| Key | p<0.05 | p≤0.01 | p≤0.001 | ||
|
| |||||
| a- vs Controls | a | aa | aaa | ||
| b- vs 2nd Trimester | b | bb | bbb | ||
| c- vs 3rd Trimester | c | cc | ccc | ||
Inter-observer analysis
Inter and intra-observer analysis evaluated byICC generally showed good correlation (Table 4). Systolic GRSR TTP/HR for both inter and intra ICC showed fair correlation (ICC<0.7 for all). Diastolic GCSR intra-observer correlation and systolic GRSR TTP/HR inter-observer correlation showed poor agreement (ICC=0.690 and ICC=0.423, respectively).
Table 4.
Intraclass correlation coefficients
| Variables | Intra-observer ICC | Inter-observer ICC |
|---|---|---|
| GLS (%) | 0.948 | 0.819 |
| GLS TTP/HR | 0.665 | 0.665 |
| GLSR- systolic (1/s) | 0.849 | 0.857 |
| GLSR TTP/HR- systolic | 0.849 | 0.857 |
| GLSR- diastolic (1/s) | 0.706 | 0.828 |
| GLSR TTP/HR- diastolic | 0.969 | 0.950 |
| GRS (%) | 0.801 | 0.807 |
| GRS TTP/HR | 0.842 | 0.892 |
| GRSR- systolic (1/s) | 0.885 | 0.372 |
| GRSR TTP/HR- systolic | 0.518 | 0.390 |
| GRSR- diastolic (1/s) | 0.908 | 0.792 |
| GRSR TTP/HR- diastolic | 0.822 | 0.907 |
| GCS (%) | 0.958 | 0.743 |
| GCS TTP/HR | 0.899 | 0.873 |
| GCSR- systolic (1/s) | 0.965 | 0.381 |
| GRSR TTP/HR- systolic | 0.715 | 0.423 |
| GCSR- diastolic (1/s) | 0.690 | 0.830 |
| GCSR TTP/HR- diastolic | 0.912 | 0.952 |
Discussion
In this study, we made three important clinical observations: first, the heart undergoes extensive remodeling during the second and third trimester of pregnancy. Second, despite this remodeling, cardiac systolic and diastolic mechanical function remains preserved. Third, an increase in GLSR and GRSR TTP/HR was detected and may reflect an adaptation mechanism not yet reported. Previous studies have mainly focused on systolic strain, our study has extended our knowledge to diastolic strain properties of myocardial adaptation in healthy pregnant subjects. Furthermore, we categorized the subjects based on real-world gestational week many previous studies did not do, making our results more applicable to daily practice.
Remodeling and mechanical function during healthy pregnancy
We detected remodeling of the left ventricle, expressed as an increase in septal and wall thickness, cavity size and mass, which was consistent with previous reports (3, 4). It is thought that this remodeling is due to the increase in preload received by the heart from the increase in blood volume that occurs with pregnancy [1,2]. Regarding the STE derived parameters, past studies have shown a decrease in systolic-GLS and systolic-GLSR in the third trimester [9,10]. However, the present study did not detect this change. This discrepancy is possibly a result of different inclusion criteria. We included patients in the second and third trimesters, while the aforementioned study included patients only in weeks 32-36 of pregnancy. On post-hoc analysis of the present study we compared strain variables between patients in 32-42 weeks of pregnancy to non-pregnant controls. Only GLSR TTP/HR-diastolic and GRSR TTP/HR-diastolic were found to be significantly prolonged. Jianwen et al. demonstrated that early mitral diastolic velocity/strain rate ratio during the isovolumetric relaxation period is strongly dependent on left ventricular relaxation and can be used to assess diastolic function [16]. Kolias et al. recently reported that patients with diastolic dysfunction had significantly lower longitudinal and circumferential diastolic strain rate [17]. In addition, they found that global longitudinal strain was a sensitive parameter that was able to distinguish patients with diastolic function [17]. In our study, pregnant subjects did not have significantly decreased diastolic GLSR or GCSR and therefore were considered to not to have diastolic dysfunction based on STE analysis. This is consistent with TTE data that there was no difference in E/A and E/e’ between study subjects and healthy controls. Prolongation of early diastolic GLSR and GRSR TTP/HR is considered to reflect increased left ventricle filling time and may simply reflect the increase in preload that occurs in healthy pregnancy. Diastolic function during pregnancy has been reported in the past with mixed results [10,18,19].
Utility of speckle-tracking echocardiography in pregnancy
There are several opportunities where STE could be utilized in evaluating cardiac conditions during pregnancy. Peripartum cardiomyopathy is a rare but potentially devastating non-ischemic cardiomyopathy of unknown etiology. It mainly occurs in the last month of pregnancy to within six months postpartum [20]. Preeclampsia is characterized by increased blood pressure after 20 weeks of gestation and its pathophysiology is considered mainly as endothelium dysfunction [21]. Shahul et al. reported a decrease in GLS, GCS and GRS in women with pre-eclampsia compared with normal healthy women [22]. The role of STE in these pathologic cardiovascular conditions is expected to be further investigated in the future once reliable reference ranges have been established.
Limitations
There are several limitations in our study that need to be mentioned. First, this is a retrospective study that enrolled pregnant subjects who were referred for TTE for clinical indications and therefore does not totally represent healthy pregnant women. However, we have excluded subjects with abnormal findings on TTE with strict protocol and subjects with other comorbidities that would influence the STE derived values. Second, first trimester pregnant data were excluded because of a small sample size and were not explored in our study. However, the most profound cardiovascular changes during pregnancy occur during the second and third trimester and little change is seen in the first trimester. Third, the TTE data in each trimester was not serially obtained from the same subjects that may limit the power of this study. Some STE parameters had sub-optimal ICCs values in inter-observer analysis and so those parameters should be interpreted with caution.
Conclusion
Our study showed that despite extensive left ventricular remodeling, mechanical strain function remained unchanged in women in the second and third trimester of a healthy pregnancy. Therefore it is valid to use the same normal STE parameters defined in non-pregnant women when studying pregnant women. Future studies using strain parameters to evaluate heart disease in pregnant women can now be performed and are warranted.
Acknowledgements
Our authors would like to thank echocardiography technicians for obtaining images.
Disclosure of conflict of interest
None of the authors have any conflicts of interest or received compensation for their work on this manuscript.
References
- 1.Duvekot JJ, Cheriex EC, Pieters FA, Menheere PP, Peeters LH. Early pregnancy changes in hemodynamics and volume homeostasis are consecutive adjustments triggered by a primary fall in systemic vascular tone. Am J Obstet Gynecol. 1993;169:1382–1392. doi: 10.1016/0002-9378(93)90405-8. [DOI] [PubMed] [Google Scholar]
- 2.Duvekot JJ, Peeters LL. Maternal cardiovascular hemodynamic adaptation to pregnancy. Obstet Gynecol Surv. 1994;49:S1–14. doi: 10.1097/00006254-199412011-00001. [DOI] [PubMed] [Google Scholar]
- 3.Kametas NA, McAuliffe F, Cook B, Nicolaides KH, Chambers J. Maternal left ventricular transverse and long-axis systolic function during pregnancy. Ultrasound Obstet Gynecol. 2001;18:467–474. doi: 10.1046/j.0960-7692.2001.00574.x. [DOI] [PubMed] [Google Scholar]
- 4.Laird-Meeter K, van de Ley G, Bom TH, Wladimiroff JW, Roelandt J. Cardiocirculatory adjustments during pregnancy -- an echocardiographic study. Clin Cardiol. 1979;2:328–332. doi: 10.1002/clc.4960020503. [DOI] [PubMed] [Google Scholar]
- 5.Dalen H, Thorstensen A, Aase SA, Ingul CB, Torp H, Vatten LJ, Stoylen A. Segmental and global longitudinal strain and strain rate based on echocardiography of 1266 healthy individuals: the HUNT study in Norway. Eur J Echocardiogr. 2010;11:176–183. doi: 10.1093/ejechocard/jep194. [DOI] [PubMed] [Google Scholar]
- 6.Kocabay G, Muraru D, Peluso D, Cucchini U, Mihaila S, Padayattil-Jose S, Gentian D, Iliceto S, Vinereanu D, Badano LP. Normal left ventricular mechanics by two-dimensional speckle-tracking echocardiography. Reference values in healthy adults. Rev Esp Cardiol (Engl Ed) 2014;67:651–658. doi: 10.1016/j.rec.2013.12.009. [DOI] [PubMed] [Google Scholar]
- 7.Marwick TH, Leano RL, Brown J, Sun JP, Hoffmann R, Lysyansky P, Becker M, Thomas JD. Myocardial strain measurement with 2-dimensional speckle-tracking echocardiography: definition of normal range. JACC Cardiovasc Imaging. 2009;2:80–84. doi: 10.1016/j.jcmg.2007.12.007. [DOI] [PubMed] [Google Scholar]
- 8.Reckefuss N, Butz T, Horstkotte D, Faber L. Evaluation of longitudinal and radial left ventricular function by two-dimensional speckle-tracking echocardiography in a large cohort of normal probands. Int J Cardiovasc Imaging. 2011;27:515–526. doi: 10.1007/s10554-010-9716-y. [DOI] [PubMed] [Google Scholar]
- 9.Papadopoulou E, Kaladaridou A, Agrios J, Matthaiou J, Pamboukas C, Toumanidis S. Factors Influencing the twisting and untwisting properties of the left ventricle during normal pregnancy. Echocardiography. 2014;31:155–163. doi: 10.1111/echo.12345. [DOI] [PubMed] [Google Scholar]
- 10.Savu O, Jurcut R, Giusca S, van Mieghem T, Gussi I, Popescu BA, Ginghina C, Rademakers F, Deprest J, Voigt JU. Morphological and functional adaptation of the maternal heart during pregnancy. Circ Cardiovasc Imaging. 2012;5:289–297. doi: 10.1161/CIRCIMAGING.111.970012. [DOI] [PubMed] [Google Scholar]
- 11.Lang RM, Badano LP, Mor-Avi V, Afilalo J, Armstrong A, Ernande L, Flachskampf FA, Foster E, Goldstein SA, Kuznetsova T, Lancellotti P, Muraru D, Picard MH, Rietzschel ER, Rudski L, Spencer KT, Tsang W, Voigt JU. Recommendations for cardiac chamber quantification by echocardiography in adults: an update from the American Society of Echocardiography and the European Association of Cardiovascular Imaging. Eur Heart J Cardiovasc Imaging. 2015;16:233–270. doi: 10.1093/ehjci/jev014. [DOI] [PubMed] [Google Scholar]
- 12.Picard MH, Adams D, Bierig SM, Dent JM, Douglas PS, Gillam LD, Keller AM, Malenka DJ, Masoudi FA, McCulloch M, Pellikka PA, Peters PJ, Stainback RF, Strachan GM, Zoghbi WA American Society of Echocardiography. American Society of Echocardiography recommendations for quality echocardiography laboratory operations. J Am Soc Echocardiogr. 2011;24:1–10. doi: 10.1016/j.echo.2010.11.006. [DOI] [PubMed] [Google Scholar]
- 13.Devereux RB, Alonso DR, Lutas EM, Gottlieb GJ, Campo E, Sachs I, Reichek N. Echocardiographic assessment of left ventricular hypertrophy: comparison to necropsy findings. Am J Cardiol. 1986;57:450–458. doi: 10.1016/0002-9149(86)90771-x. [DOI] [PubMed] [Google Scholar]
- 14.Yock PG, Popp RL. Noninvasive estimation of right ventricular systolic pressure by Doppler ultrasound in patients with tricuspid regurgitation. Circulation. 1984;70:657–662. doi: 10.1161/01.cir.70.4.657. [DOI] [PubMed] [Google Scholar]
- 15.Palmieri V, Bella JN, Roman MJ, Gerdts E, Papademetriou V, Wachtell K, Nieminen MS, Dahlof B, Devereux RB. Pulse pressure/stroke index and left ventricular geometry and function: the LIFE Study. J Hypertens. 2003;21:781–787. doi: 10.1097/00004872-200304000-00022. [DOI] [PubMed] [Google Scholar]
- 16.Wang J, Khoury DS, Thohan V, Torre-Amione G, Nagueh SF. Global diastolic strain rate for the assessment of left ventricular relaxation and filling pressures. Circulation. 2007;115:1376–1383. doi: 10.1161/CIRCULATIONAHA.106.662882. [DOI] [PubMed] [Google Scholar]
- 17.Kolias TJ, Hagan PG, Chetcuti SJ, Eberhart DL, Kline NM, Lucas SD, Hamilton JD. New universal strain software accurately assesses cardiac systolic and diastolic function using speckle tracking echocardiography. Echocardiography. 2014;31:947–955. doi: 10.1111/echo.12512. [DOI] [PubMed] [Google Scholar]
- 18.Fok WY, Chan LY, Wong JT, Yu CM, Lau TK. Left ventricular diastolic function during normal pregnancy: assessment by spectral tissue Doppler imaging. Ultrasound Obstet Gynecol. 2006;28:789–793. doi: 10.1002/uog.3849. [DOI] [PubMed] [Google Scholar]
- 19.Mesa A, Jessurun C, Hernandez A, Adam K, Brown D, Vaughn WK, Wilansky S. Left ventricular diastolic function in normal human pregnancy. Circulation. 1999;99:511–517. doi: 10.1161/01.cir.99.4.511. [DOI] [PubMed] [Google Scholar]
- 20.Pyatt JR, Dubey G. Peripartum cardiomyopathy: current understanding, com prehensive management review and new developments. Postgrad Med J. 2011;87:34–39. doi: 10.1136/pgmj.2009.096594. [DOI] [PubMed] [Google Scholar]
- 21.Osol G, Bernstein I. Preeclampsia and maternal cardiovascular disease: consequence or predisposition? J Vasc Res. 2014;51:290–304. doi: 10.1159/000367627. [DOI] [PubMed] [Google Scholar]
- 22.Shahul S, Rhee J, Hacker MR, Gulati G, Mitchell JD, Hess P, Mahmood F, Arany Z, Rana S, Talmor D. Subclinical left ventricular dysfunction in preeclamptic women with preserved left ventricular ejection fraction: a 2D speckle-tracking imaging study. Circ Cardiovasc Imaging. 2012;5:734–739. doi: 10.1161/CIRCIMAGING.112.973818. [DOI] [PMC free article] [PubMed] [Google Scholar]