Estimated cardiac output and cardiovascular profile score in fetuses with high cardiac output lesions
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1 Ultrasound Obstet Gynecol 213; 41: Published online in Wiley Online Library (wileyonlinelibrary.com). DOI: 1.12/uog.1239 Estimated cardiac output and cardiovascular profile score in fetuses with high cardiac output lesions C. J. STATILE, J. F. CNOTA, S. GOMIEN, A. DIVANOVIC, T. CROMBLEHOLME and E. MICHELFELDER Cincinnati Children s Hospital Medical Center, Cincinnati, OH, USA KEYWORDS: cardiac output; cardiovascular profile score; chorioangioma; hydrops fetalis; sacrococcygeal teratoma ABSTRACT INTRODUCTION Objective High cardiac output lesions are associated with an increased risk of fetal death, largely as a result of cardiac failure and hydrops fetalis. The cardiovascular profile score () has been used to characterize cardiovascular wellbeing, and has been linked to fetal outcomes in other conditions. We aimed to test the hypothesis that elevated combined cardiac output (CCO) in fetuses with high output lesions may be associated with worsening cardiovascular status, as evidenced by a lower. Methods A retrospective review was performed of fetuses with high cardiac output lesions that underwent echocardiography between July 26 and November 21. Diagnoses included sacrococcygeal teratoma, placental chorioangioma and vein of Galen aneurysm. Fetal echocardiographic evaluation included assessment of, as well as Doppler/two-dimensional estimation of CCO, indexed to estimated fetal weight (CCOi). The relationship between CCO and was assessed. Results A total of 35 fetuses were studied: 27 had sacrococcygeal teratoma, seven had chorioangioma and one had vein of Galen aneurysm. There was a significant inverse relationship between mean logccoi and (r 2 =.48, P =.8). Of 31 patients with clinical outcome data, 1 experienced either in-utero demise or intervention; 8% of these fetuses had a of < 8. Conclusions There is an inverse relationship between CCO and in the fetus with high cardiac output lesions. As a measure of fetal cardiovascular wellbeing in this population, the may be a useful tool for stratifying risk and for selection for intervention in these fetuses. Copyright 213 ISUOG. Published by John Wiley & Sons, Ltd. Prenatal diagnosis of lesions such as sacrococcygeal teratomas, placental chorioangiomas and arteriovenous malformations has become more common; this trend has accompanied the development and clinical dissemination of fetal therapies to treat affected high-risk fetuses 1.One of the main risk factors for fetal and neonatal mortality in this population is the development of high output heart failure in utero, with resultant hydrops and fetal demise 2. As the heart tries to compensate for the increasing blood flow and cardiac output, cardiovascular changes can be seen in the fetus 3 5. Although cardiovascular changes in this population have been described in the literature, there are limited data objectively measuring them using the cardiovascular profile score () 6,7. The is a summary score of cardiac function and Doppler velocimetry that is designed to describe fetal cardiovascular wellbeing. The has been used to follow and predict cardiovascular wellbeing in a number of fetal conditions, including intrauterine growth restriction, twin twin transfusion syndrome and fetal congenital heart disease 8,9. The has also been linked to outcomes in these same patient populations 1,11. Calculating and following the in fetuses with high output lesions may prove useful in characterizing the degree of hemodynamic derangement in these patients, both in assessing fetal wellbeing and possibly in improving patient selection and the timing of fetal interventional procedures. The purpose of this study was to determine the relationship between and estimated combined cardiac output (CCO) in a cohort of fetuses with high cardiac output lesions. We hypothesized that higher CCO would be associated with progressive abnormalities in cardiovascular function, reflected by decreasing. Correspondence to: Dr C. Statile, Cincinnati Children s Hospital, The Heart Institute, 3333 Burnet Ave., MLC 23, Cincinnati, OH 45229, USA ( Christopher.statile@cchmc.org) Accepted: 19 September 212 Copyright 213 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER
2 vs cardiac output 55 METHODS This was a retrospective cohort study of patients with high cardiac output lesions referred to the Fetal Care Center at Cincinnati Children s Hospital Medical Center between 26 and 21. High output lesions included sacrococcygeal teratoma, placental chorioangioma and vein of Galen aneurysm. Fetuses with structurally abnormal hearts and abnormal fetal cardiac rhythm were excluded. Cases of twin-reversed arterial perfusion (TRAP) sequence were excluded from the analysis, as we have previously reported CCO and findings in this population 12. The most recent echocardiogram before delivery, demise or intervention was used for analysis. Echocardiograms were performed by a trained sonographer with expertise in fetal echocardiography. Each echocardiogram was performed in accordance with published standards 13. All examinations were performed using either an Acuson Sequoia C512 ultrasound system or an Acuson S2 ultrasound system (Siemens Medical Solutions USA, Inc., Malvern, PA, USA) with commercially available curvilinear transducers. The presence or absence of hydrops (effusion, ascites and/or skin edema) was noted. Pulsed-wave Doppler evaluation of flow patterns in the ductus venosus, umbilical vein and umbilical artery were recorded. The cardiothoracic ratio was measured as the ratio of the cardiac area/thoracic area measured in the four-chamber view of the fetal heart. Color-flow Doppler was utilized to assess the degree of atrioventricular valve regurgitation, which was qualitatively graded as absent, mild, moderate or severe based on jet width and length. Right ventricular (RV) and left ventricular (LV) shortening fraction was calculated using either M-mode or two-dimensional imaging. Transmitral and transtricuspid flow patterns were assessed for biphasic vs monophasic flow patterns by pulsed-wave Doppler. CCO was derived through pulsed-wave Doppler of the aortic and pulmonary valves, using the following equation: cross-sectional area of the semilunar valve (3.14 valve radius 2 ) velocity time integral heart rate. The CCO was then indexed to the estimated fetal weight, known as the combined cardiac index (CCOi), and compared with published normal values ( ml/min/kg) 14. The is a composite measure of overall cardiovascular wellbeing in the fetus. It consists of a 1-point scale (Table 1) that incorporates the presence or absence of fetal hydrops, abnormal venous and arterial Doppler findings, cardiomegaly, atrioventricular valve regurgitation and cardiac dysfunction; the score is 1 if there are no abnormal signs and there are 1-point to 2-point deductions from the total score depending on the extent of cardiovascular abnormalities noted for each category 6,7. The was calculated by evaluating each individual echocardiogram. Significant cardiovascular compromise was defined as a of < Clinical outcomes were defined as fetal intervention, fetal demise, live birth and overall perinatal mortality (22 weeks gestation up to 28 days of postnatal life) 13,14. Descriptive results are presented as mean ± SD or median and interquartile range (IQR), where appropriate. CCOi was log transformed to normalize the distribution. Comparison of CCOi across levels was performed using ANOVA. The relationship between CCOi and was assessed by linear regression. Statistical significance was assigned for P <.5. RESULTS Thirty-five fetuses were studied: one with vein of Galen aneurysm, seven with chorioangioma and 27 with sacrococcygeal teratoma. The mean ± SD gestational age at the time of echocardiography was 26.6 ± 5.4 weeks. Clinical findings for the study population are summarized in Table 2. The ranged from 2 to 1 (Figure 1). There were 22 fetuses without signs of significant cardiovascular distress, defined as a of 8. There were 13 fetuses with signs of cardiovascular compromise ( < 8) (Figure 2). The median CCOi was 525 (IQR, ) ml/min/kg with a range from 241 to 111 ml/min/kg. Mean logccoi differed across values (P <.1, ANOVA), demonstrating a significant inverse relationship on linear regression (r 2 =.48, P =.8) (Figure 1). Table 1 Summary of the five categories used to calculate cardiovascular profile score () Category Score (normal) Score 1 Score 2 Hydrops fetalis None Ascites or pleural effusion or Skin edema pericardial effusion Venous Doppler Normal Flow reversal in ductus venosus Umbilical venous pulsations tracing Heart size (heart.2 and < >.5 or <.2 area/chest area) Cardiac function Normal TV and MV, RV/LV shortening fraction >.28 and Holosystolic TR or RV/LV shortening fraction <.28 Holosystolic MR or dp/dt < 4 or monophasic filling biphasic diastolic ventricular filling Arterial Doppler Normal UA tracing UA D-wave reaches baseline UA diastolic flow reversal Score is 1 if there are no abnormal signs, and there are 1-point or 2-point deductions from total score depending on extent of cardiovascular abnormalities noted for each category 9. dp/dt, rate of rise of left ventricular pressure; LV, left ventricular; MR, mitral regurgitation; MV, mitral valve; RV, right ventricular; TR, tricuspid regurgitation; TV, tricuspid valve; UA, umbilical artery.
3 56 Statile et al. Table 2 Clinical findings and outcomes for individual study subjects Diagnosis CCOi (ml/min/kg) Fetal intervention Outcome Abnormal CCOi Chorio Yes Lost to follow-up after intervention Chorio 15 2 Yes LB, 34 weeks SCT Yes IUFD at 22 weeks with intervention VGA No LB, 37 weeks Chorio Yes LB, 35 weeks SCT Yes IUFD at 21 weeks with intervention SCT Yes IUFD at 22 weeks after intervention SCT No Spontaneous IUFD at 26.5 weeks SCT No Lost to follow-up Chorio Yes IUFD at 25 weeks after intervention SCT No Spontaneous IUFD at 2.5 weeks Chorio No Lost to follow-up SCT No LB, 29 weeks Normal CCOi SCT No EXIT to resection at 31 weeks SCT No TOP at 2 weeks SCT No Lost to follow-up SCT No LB, 36 weeks SCT No LB, 37 weeks Chorio 59 1 No LB, 39 weeks SCT 59 1 No LB, 38 weeks SCT 59 9 No LB, 34 weeks SCT 57 1 No LB, 36 weeks SCT No LB, 32 weeks SCT No LB, 36 weeks SCT No LB, 35 weeks SCT No LB, 37 weeks SCT No LB, 31 weeks SCT 43 1 No LB, 37 weeks SCT No LB, 37 weeks Chorio No LB, 38 weeks SCT 39 1 No LB, 37 weeks SCT No LB, 39 weeks SCT No IUFD at 32 weeks SCT 32 1 No LB, 37 weeks SCT No Lost to follow-up CCOi, indexed combined cardiac output; Chorio, placental chorioangioma;, cardiovascular profile score; EXIT, ex-utero intrapartum therapy; IUFD, intrauterine fetal death; LB, live birth; SCT, sacrococcygeal teratoma; TOP, termination of pregnancy; VGA, vein of Galen aneurysm. The relationship between and CCOi in individual fetuses is presented in Figure 2. Of the 22 fetuses without signs of cardiovascular compromise ( 8), there were two fetuses with a CCOi of > 625 ml/min/kg. In the group of 13 fetuses that showed signs of cardiovascular compromise ( < 8), 11/13 had a CCOi of > 625 ml/min/kg. The relationship between severity score (, 1 or 2) for the five individual categories comprising the and CCOi was also examined. The CCOi and severity score were significantly associated for the categories of cardiac function (P =.2) and heart size (P <.1) (Figure 3). There was no significant difference between CCOi and score (, 1 or 2) in the hydrops, venous Doppler or arterial Doppler categories. Clinical follow-up and outcome data (up to either fetal intervention or birth) were available in 31 of 35 subjects. The CCOi was 625 ml/kg/min in 11 of 31 subjects. In those 11 patients, nine (82%) went on to fetal surgical intervention or intrauterine death. The remaining two (18%) underwent amnioreduction and were watched expectantly. One was denied fetal intervention for maternal risk and the other declined intervention. Both died after birth in the perinatal period. Of the 2 fetuses with a CCOi of < 625 ml/kg/min and follow-up data, no patients had intervention. There was one intrauterine fetal death and one termination of pregnancy. In those cases with a CCOi of > 625 ml/kg/min, the was < 8in1(91%)of11patients,compared with only two (1%) of 2 in those with a normal CCOi. Ten (32%) of 31 subjects with relevant data available experienced either in-utero demise or intervention; the proportion of these fetuses with a of < 8 was significantly higher than in those who survived to birth without intervention (8% vs 16%, χ 2 = 13.7, P <.1). Data on overall perinatal mortality were available in 28 subjects. There were nine deaths between 22 weeks gestation and 28 days of postnatal life. The CCOi was> 625 ml/kg/min in eight (89%) of nine of these cases and the was < 8 in the same eight fetuses.
4 vs cardiac output 57 (a) 7. 1 CCOi (ml/kg/min) logccoi Cardiac function score n = 1 n = 1 n = 1 n = 2 n = 8 n = 2 n = 6 n = (b) 7. Figure 1 Plot of mean indexed combined cardiac output (CCOi) against cardiovascular profile score (), with error bars showing 95% CI. Open circles show single observations. The logccoi differed across values (P <.1, ANOVA), demonstrating a significant inverse relationship on linear regression (r 2 =.48, P =.82). logccoi CCOi Elevated CCOi 8 1 Figure 2 Scatterplot of indexed combined cardiac output (CCOi) against cardiovascular profile score () for individual fetuses (filled diamonds). Significant cardiovascular compromise was defined as < 8 (vertical line). Abnormal CCOi was defined as > 625 ml/min/kg 14 (horizontal line). DISCUSSION This study demonstrates that there is an inverse correlation between and CCOi in fetuses with high output lesions. These data confirm our hypothesis that progressive increases above normal CCOi would be associated with decrements in fetal cardiovascular wellbeing. Our findings are consistent with those of previous reports examining the relationship among, fetal cardiovascular status and outcomes in other fetal lesions. Hofstaetter et al. 9 described the use of in over 1 hydropic fetuses and found a median of 6 for all hydropic fetuses with in-utero demise, and a median of 7 for those that survived to term. Within this cohort Heart size score Figure 3 Box plots of log-transformed combined cardiac output (logccoi) against severity score (, 1 or 2, where zero is normal and 1 and 2 represent progressive abnormalities) for cardiac function (a) and heart size (b) categories of cardiovascular profile score (). Boxes and internal lines represent 25 th 75 th percentiles and median, diamonds show mean, whiskers show range excluding outliers and small circles represent outliers. There is a significant increase in CCOi with larger heart size (P <.1) and worsening cardiac function (P =.2). there was only one patient with a high output lesion (sacrococcygeal teratoma). Similarly, was used, by Makikallio et al., to characterize cardiovascular health in fetuses with intrauterine growth restriction 1. Those fetuses that either died or were born before 28 weeks gestation had a median of 6. In comparison, those fetuses that survived beyond 35 weeks gestation had a median of 9. Low has also been correlated to poor outcomes in congenital heart disease 15 and in recipient twins in twin twin transfusion syndrome 11. Our group has previously used to characterize the pump twin in TRAP sequence, and found that pump twin was significantly associated with elevations in CCO 12. Furthermore, this study demonstrated that the improved in four of six patients treated with radiofrequency ablation, suggesting that the may be a useful tool for serial evaluation of cardiovascular status before and after fetal therapeutic procedures. The or its relation to CCO has not, to date, been reported in a large cohort of patients with high output lesions. 2
5 58 Statile et al. The current study demonstrates that the in fetuses with high output lesions tends to decrease as CCOi increases. Our data suggest that a of 8is associated with excellent fetal survival in fetuses with high output lesions. Survival to birth for fetuses with a of < 8, regardless of intervention, was low, suggesting that a low is associated with poorer survival. However, it is difficult to assess the relationship between and natural history in this group given our institutional practice, as elevations in CCO are incorporated into the overall decision to intervene in many of these lesions. Heart size and cardiac function were the only two parts of the that were associated with significant differences in CCO, with the lower scores having a higher CCO. Interestingly, there was no significant difference in CCO across hydropic scores. This suggests that heart size and functional assessment may be better predictors of CCO than is the presence of hydrops. These results suggest that monitoring of CCO and may be useful in serial assessment and in selection for fetal therapy in these high-risk lesions. CCO is a measurement that may be difficult to replicate in institutions that do not perform it regularly, making a more reliable and easier-to-obtain measure. The may also be more practical in clinical settings where fetal cardiovascular health is followed by obstetric ultrasound. Although fetal intervention, particularly open fetal surgery, is traditionally reserved for patients with hydrops, cardiovascular status may become a means of identifying fetuses at risk for hydrops and in-utero death for potential treatment, which may, in turn, improve overall outcomes in this population. This may be particularly relevant, for example, in cases where less-invasive, fetoscopic therapies are available (e.g. TRAP sequence) and in devascularization of placental chorioangioma. While this is a large cohort of patients for these particular diagnoses, the data are still limited by a relatively small cohort size. Clinical follow-up was also limited in patients with a normal fetal CCO. The interpretation of clinical outcomes must be made with the understanding that treatment decisions for fetal interventions were determined, in part, by the results of the fetal echocardiogram. Therefore, it is not possible to assess the relationship between and the natural history of these high output fetal lesions. In conclusion, the current study demonstrates that in fetuses with high cardiac output lesions, progressive elevations in CCO are associated with decrements in fetal cardiovascular health, reflected by a decreasing. Amongst fetuses with a of 8, survival was excellent without intervention. Monitoring CCO and in these fetuses may be a clinically useful means of assessing fetal wellbeing, and perhaps a tool for improving patient selection for fetal interventional procedures in the future. REFERENCES 1. Ruano R, Duarte S, Zugaib M. Percutaneous laser ablation of sacrococcygeal teratoma in a hydropic fetus with severe heart failure too late for a surgical procedure? Fetal Diagn Ther 29; 25: Russell RT, Carlin A, Ashworth M, Welch CR. Diffuse placental chorioangiomatosis and fetal hydrops. Fetal Diagn Ther 27; 22: Wilson RD, Hedrick H, Flake AW, Johnson MP, Bebbington MW, Mann S, Rychik J, Liechty K, Adzick NS. Sacrococcygeal teratomas: prenatal surveillance, growth and pregnancy outcome. Fetal Diagn Ther 29; 25: Zanardini C, Papageorghiou A, Bhide A, Thilaganathan B. Giant placental chorioangioma: natural history and pregnancy outcome. Ultrasound Obstet Gynecol 21; 35: Henrich W, Fuchs I, Buhrer C, van Landeghem FK, Albig M, Stoever B, Dudenhausen JW. 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