The Journal of Maternal-Fetal & Neonatal Medicine

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Fetal tricuspid annulus plane systolic excursion (fTAPSE) at term – association with cerebroplacental ratio, birthweight and neonatal pH José Morales-Roselló, Asma Khalil & Alfredo Perales-Marín To cite this article: José Morales-Roselló, Asma Khalil & Alfredo Perales-Marín (2015): Fetal tricuspid annulus plane systolic excursion (fTAPSE) at term – association with cerebroplacental ratio, birthweight and neonatal pH, The Journal of Maternal-Fetal & Neonatal Medicine To link to this article: http://dx.doi.org/10.3109/14767058.2015.1057810

Accepted online: 02 Jul 2015.Published online: 27 Jul 2015.

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Date: 14 October 2015, At: 01:38

http://informahealthcare.com/jmf ISSN: 1476-7058 (print), 1476-4954 (electronic) J Matern Fetal Neonatal Med, Early Online: 1–6 ! 2015 Informa UK Ltd. DOI: 10.3109/14767058.2015.1057810

ORIGINAL ARTICLE

Fetal tricuspid annulus plane systolic excursion (fTAPSE) at term – association with cerebroplacental ratio, birthweight and neonatal pH Jose´ Morales-Rosello´1, Asma Khalil2, and Alfredo Perales-Marı´n1 Servicio de Obstetricia, Hospital Universitario y Polite´cnico La Fe, Valencia, Spain and 2Fetal Medicine Unit, St George Hospital, London, UK

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Abstract

Keywords

Objective: To study at term the association of the fetal tricuspid annulus plane systolic excursion (fTAPSE) with gestational age (GA), birthweight (BW), cerebroplacental ratio (CPR) and neonatal pH. Methods: fTAPSE was evaluated in 309 fetuses in relation with GA and BW. Standardized values for fetal size using the head circumference were also studied in relation with CPR multiples of the median (MoM) and BW centile, evaluating the existence of differences in smallfor-gestational-age (SGA) fetuses and in fetuses with low CPR. In addition, in a subgroup of 286 fetuses, standardized fTAPSE was evaluated according to neonatal venous and arterial pH. Results: fTAPSE correlated with BW but not with GA. In addition, although standardized values correlated with BW centile and CPR MoM, they did not differ either in SGA fetuses or in fetuses with abnormal CPR. Finally, no correlation was found between fTAPSE and neonatal pH. Conclusions: In the term fetus, fTAPSE changes with absolute fetal weight, reflecting the physiological variations occurring with fetal size. However, it is very scarcely influenced by fetal Doppler or BW centile and does not associate with neonatal pH. These data support the idea that the fetal heart is not a valuable target in the study of late-onset growth restriction.

Cerebroplacental ratio, failure to reach growth potential, fetal Doppler ultrasound, fetal growth restriction, fetal TAPSE, small-for-gestational-age History Received 30 April 2015 Revised 21 May 2015 Accepted 31 May 2015 Published online 27 July 2015

Introduction

Materials and methods

The tricuspid annulus plane systolic excursion (TAPSE) represents the longitudinal displacement of the tricuspid annulus towards the cardiac apex [1–4]. It was originally studied in adults for the assessment of ventricular function, and has also been applied in the evaluation of children and neonates where it increases in proportion to the body size [5,6]. Fetal TAPSE (fTAPSE) reflects the function of the fetal longitudinal myocardial fibers, which are more sensitive to hypoxia, in the dominant (right) chamber. It also varies with fetal size [7] and is therefore difficult to assess without making an adequate standardization. It has been evaluated prenatally in normal population [8] and in fetuses with earlyonset growth restriction [9,10] finding lower values in those with severe growth compromise. However, studies assessing its association with fetal size and Doppler at term are lacking. The main aim of this study was to assess the association of fTAPSE with birthweight (BW), cerebroplacental ratio (CPR) and neonatal pH at term.

This was a prospective study performed at the day assessment unit of a tertiary referral center between February 2014 and December 2014. It included 309 morphologically normal term singleton fetuses who had a routine ultrasound scan at term, according to our local protocol. Only pregnancies that delivered within 14 d of the date of the ultrasound assessment were included in the analysis, and only one (the last) examination per fetus was collected. Gestational age (GA) was determined according to the last menstrual period corrected with the crown-rump length in the first trimester. Ultrasound examinations were performed using Voluson E8/E6/730 ultrasound machines with 2–8 MHz convex probes during fetal quiescence, in the absence of fetal tachycardia, and keeping the insonation angle with the examined vessels and the longitudinal axis of the heart as small as possible. fTAPSE values were obtained using M-mode, measuring the total displacement of the external border of the valve annulus towards the apex (Figure 1) [8]. All examinations were performed by the first author (J. M. R.) with a good reproducibility (intra-class coefficient for intra-observer variation ¼ 0.92). Concerning Doppler measurements, the umbilical (UA) and middle cerebral artery (MCA) pulsatility index (PI) were recorded as described earlier [11,12] and CPR was

Address for correspondence: Dr Jose´ Morales-Rosello´, Servicio de Obstetricia, Hospital Universitario y Polite´cnico La Fe, Avenida Fernando Abril Martorell S/N, 46026, Valencia, Spain. E-mail: [email protected]

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Figure 1. Measurement of the fTAPSE. The total displacement of the external valve annulus was measured three times and the results were averaged before standardization.

calculated as the simple ratio between the MCA PI and the UA PI [13]. Finally, the UA cord pH measurements were obtained after birth using a radiometer ABL800-FLEX pH meter (Radiometer Medical ApS, Brønshøj, Denmark). fTAPSE values were tested later using the D’Agostino and Pearson omnibus normality test, which proved them to be normally distributed. As fTAPSE values had been earlier correlated with fetal size [8], they were subsequently adjusted according to the head circumference (HC), which is a reflection of brain size, considering that both fetal brain and heart are spared during intrauterine growth restriction. As CPR, UA PI and MCA PI values correlate with GA, they were also converted into multiples of median (MoM) correcting for GA [14]. In summary, all values were divided by the 50th centile (median), which was calculated according to the following equations: UA PI 50th centile ¼ 1:7993  0:02497  GA MCA PI 50th centile ¼ 3:266164164 þ 0:368135209  GA  0:006318278  GA ½2

Figure 2. Comparison groups according to the values of the CPR and BW centile. The 0.6765 threshold is based on our earlier publications [16,17], representing fetuses with failure to reach the growth potential. Percentile 10th represents the limit between SGA and non-SGA fetuses.

CPR 50th centile ¼ 1:3841 þ 0:22659  GA  0:003743  GA ½2 where GA was expressed in weeks with days in decimals. BW centiles were calculated adjusting for GA using the method described earlier by Yudkin [15]. The correlation of fTAPSE with BW and GA was evaluated using linear regression. Similarly, adjusted fTAPSE (using HC) was correlated with CPR MoM, BW centile, UA PI MoM and MCA PI MoM, obtaining in all cases the corresponding coefficients r2 and p-values.

The 10th centile defines the fetus small-for-gestational-age (SGA). In addition, the CPR MoM cut-off of 0.6765 was recently proposed as a measure to identify fetuses suffering from failure to reach the growth potential (FRGP) at term [16,17] (Figure 2). Accordingly, fTAPSE values were compared in different combinations between SGA and nonSGA, and between FRGP fetuses and non-FRGP fetuses. Finally, the correlation between fTAPSE and the acid–base status, represented by the arterial and venous UA cord pH,

Fetal TAPSE at term

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Table 1. Characteristics of the studied population. Group N Maternal age Week exam. Week labor Interval to labor (d) Birthweight (g) Cord pH (artery) Cord pH (vein)

Total

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2

3

4

309 32 (5.3) 39.5 (0.8) 40.3 (0.7) 5.9 (3.6) 3340 (413) 7.27 (0.07) 7.32 (0.06)

9 33.7 (4.9) 38.8 (1.2) 39.7 (0.9) 5.9 (4.7) 2626 (198) 7.26 (0.05) 7.29 (0.04)

18 32.7 (6) 39.7 (0.5) 40.4 (0.6) 4.5 (3.7) 3303 (269) 7.24 (0.08) 7.30 (0.09)

30 31.53 (5.8) 39.2 (0.7) 40.4 (0.7) 7.8 (3.7) 2723 (153) 7.26 (0.06) 7.32 (0.06)

252 32 (5.2) 39.5 (0.8) 40.4 (0.7) 5.8 (3.5) 3442 (355) 7.28 (0.06) 7.32 (0.06)

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For pH the total number was 286, and the number for groups 1–4 was 8, 17, 25 and 236.

was assessed in a subgroup of 286 fetuses using regression analysis. All patients gave verbal consent for the examination and this was approved by the local Institutional Review Board. GraphPad Prism version 5aÕ for Apple Macintosh (GraphPad SoftwareÕ Inc., San Diego, CA) and VassarStatsÕ (Richard Lowry, Vassar College, New York, NY) were used for data analyses. Statistical significance was established at p50.05.

Results The analysis included 309 pregnancies, of which 166 (53.7%) were male and 143 (46.3%) were female. The number of patients in groups 1–4 were 9, 18, 30, and 252. Table 1 summarizes some of the characteristics of the total population and the groups described in Figure 2. In general, the mean maternal age was 32.0 years (SD 5.3, range 15–44) and the mean BW was 3340 g (SD 413.2, range 2285–4765). The mean GA at ultrasound examination was 39.5 weeks (SD 0.80, range 37.00–41.00), and at delivery 40.3 weeks (SD 0.73, range 37.86–41.29). Finally, the mean interval between ultrasound and delivery was 5.9 days (SD 3.6, range 0–14). Figure 3(A) and (B) show the association of the fTAPSE with GA and BW. While no correlation was seen between fTAPSE and GA (R250.0001, p ¼ 0.8989), fTAPSE strongly correlated with BW (R2 ¼ 0.0756, p50.0001). Figure 4(A–D) shows the association of the adjusted fTAPSE (independent of fetal size) with BW centile, CPR MoM, UA PI MoM and MCA PI MoM. A significant correlation was seen with the first two parameters (R2 ¼ 0.0314, p ¼ 0.0018 and R2 ¼ 0.0142, p ¼ 0.0363). However, no correlation was observed for the UA PI and MCA PI, although it was in both cases close to significance (R2 ¼ 0.0098, p ¼ 0.0823 and R2 ¼ 0.0119, p ¼ 0.0554). Figure 5(A–D) shows the differences in adjusted fTAPSE according to the different combinations of the groups described in Figure 2. Figure 5(A) shows the difference between fetuses with normal and abnormal CPR, Figure 5(B) shows the difference between SGA and non-SGA fetuses, Figure 5(C) shows the difference between SGA fetuses with normal CPR and SGA fetuses with abnormal CPR (groups 1 versus 3) and Figure 5(D) shows the differences between SGA fetuses with abnormal CPR and non-SGA fetuses with normal CPR (groups 1 versus 4). No significant differences were seen for any of these groups (p ¼ 0.3157, p ¼ 0.6900, p ¼ 0.7719 and p ¼ 0.4334).

Figure 3. Scattergrams showing the associations of the fTAPSE with: (A) GA in weeks and (B) BW in grams. Only correlation with BW was significant (p50.0001).

Finally, Figure 6(A) and (B) show the correlation of adjusted fTAPSE with neonatal venous and arterial pH. No correlation was observed for either of them (R2 ¼ 0.0006, p ¼ 0.6774 and R2 ¼ 0.0036, p ¼ 0.3134).

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Figure 4. Scattergrams showing the association of the adjusted fTAPSE with: (A) BW centile, (B) CPR MoM, (C) UA PI MoM and (D) MCA PI MoM. Although only the first two parameters correlated with fTAPSE, the remaining presented a borderline significance. fTAPSE was adjusted using the HC (TAPSE/HC).

Discussion The majority of the literature related to fTAPSE has focuses on early-onset fetal growth restriction. This is therefore the first study investigating its associations with fetal growth and Doppler at term. According to our data, fTAPSE correlated with BW but not with GA, thus making difficult to ascertain whether the observed variation in small fetuses was partially due to the presence of minor cardiac dysfunction. In order to adjust fTAPSE for fetal size, previous studies used the heart longitudinal axis [9]. However, as this parameter might also vary by the same factors that influence the fTAPSE values,

we used an external measurement (HC), as a surrogate marker of fetal brain size, as both the fetal brain and heart are preserved in case of fetal undernourishment [18,19]. With this correction, and adjusting BW and CPR for GA by using BW centiles and CPR MoM, we aimed to evaluate accurately fTAPSE according to CPR and BW. Our results indicate that the adjusted fTAPSE is still influenced by fetal growth (BW). However, the influence of this phenomenon at term is likely to be too small to yield significant differences in SGA fetuses or in SGA with low CPR. Interestingly, this is not the case before term. In a recent work, early-onset growth-restricted fetuses were found to present lower fTAPSE values [9] and the authors

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Fetal TAPSE at term

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Figure 5. Box and whiskers comparison of adjusted fTAPSE in: (A) fetuses with failure to reach the growth potential (FRGP) versus fetuses without FRGP (no FRGP) using the CPR threshold of 0.6765 MoM (groups 1 + 2 versus 3 + 4), (B) fetuses with BW below the 10th centile (SGA) versus fetuses with BW over the 10th percentile (groups 1 + 3 versus 2 + 4), (C) SGA fetuses with normal CPR versus SGA fetuses with abnormal CPR (groups 1 versus 3) and (D) SGA fetuses with abnormal CPR versus non-SGA fetuses with normal CPR (groups 1 versus 4). No differences were seen in any these comparisons. fTAPSE was adjusted using the head HC (fTAPSE/HC).

concluded that fTAPSE was a useful tool in the evaluation of growth-restriction. Our data do not support a similar importance in the evaluation of the SGA term fetus, probably because late-onset fetal smallness represents a much milder condition causing an absent or minimal cardiac dysfunction. Adjusted fTAPSE was also associated with fetal CPR MoM. As with BW centile, this association was not enough to yield significant differences in fetuses with low CPR, even in fetuses that were also SGA, compared to those with normal CPR. Although this might be different in the early-onset growth restricted fetus with a more severe hemodynamic

disturbance, the scarcity of publications precludes drawing solid conclusions. Finally, adjusted fTAPSE was not associated with neonatal pH. However, as with CPR, there were no previous studies with which to compare our results. In summary, along with the ductus venosus Doppler [20] and myocardial performance index [21] fetal TAPSE seems to be affected only in advanced stages of fetal hemodynamic compromise such as that described in early-onset intrauterine growth restriction. Its minor importance at term suggests that the fetal heart is unlikely to be a target in the clinical evaluation of late-onset fetal growth restriction.

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13. 14.

15. Figure 6. Scattergrams showing the association of adjusted fTAPSE with arterial and venous pH. No correlation was seen for any of these parameters. fTAPSE was adjusted using the head circumference (HC) (TAPSE/HC).

Declaration of interest

16. 17. 18.

The authors declare no conflicts of interests.

References 1. Kaul S, Tei C, Hopkins JM, Shah PM. Assessment of right ventricular function using two-dimensional echocardiography. Am Heart J 1984;107:526–31. 2. Park JH, Kim JH, Lee JH, et al. Evaluation of right ventricular systolic function by the analysis of tricuspid annular motion in patients with acute pulmonary embolism. J Cardiovasc Ultrasound 2012;20:181–8. 3. Kjaergestational ageard J, Iversen KK, Akkan D, et al. Predictors of right ventricular function as measured by tricuspid annular

19.

20. 21.

plane systolic excursion in heart failure. Cardiovasc Ultrasound 2009;7:51. Caminiti G, Volterrani M, Murugesan J, et al. Tricuspid annular plane systolic excursion is related to performance at six minute walking test in patients with heart failure undergoing exercise training. Int J Cardiol 2013;169:91–2. Koestenberger M, Nagel B, Ravekes W, et al. Right ventricular performance in preterm and term neonates: reference values of the tricuspid annular peak systolic velocity measured by tissue Doppler imaging. Neonatology 2013;103:281–6. Koestenberger M, Ravekes W, Nagel B, et al. Reference values of the right ventricular outflow tract systolic excursion in 711 healthy children and calculation of z-score values. Eur Heart J Cardiovasc Imag 2014;15:980–6. Koestenberger M, Nagel B, Avian A, et al. Systolic right ventricular function in children and young adults with pulmonary artery hypertension secondary to congenital heart disease and tetralogy of Fallot: tricuspid annular plane systolic excursion (TAPSE) and magnetic resonance imaging data. Congenit Heart Dis 2012;27: 250–8. Messing B, Gilboa Y, Lipschuetz M, et al. Fetal tricuspid annular plane systolic excursion (f-TAPSE): evaluation of fetal right heart systolic function with conventional M-mode ultrasound and spatiotemporal image correlation (STIC) M-mode. Ultrasound Obstet Gynecol 2013;42:182–8. Cruz-Lemini M, Crispi F, Valenzuela-Alcaraz B, et al. Value of annular M-mode displacement vs tissue Doppler velocities to assess cardiac function in intrauterine growth restriction. Ultrasound Obstet Gynecol 2013;42:175–81. Cruz-Lemini M, Crispi F, Valenzuela-Alcaraz B, et al. A fetal cardiovascular score to predict infant hypertension and arterial remodeling in intrauterine growth restriction. Am J Obstet Gynecol 2014;210:552.e1–22. Acharya G, Wilsgestational ageard T, Berntsen GK, et al. Reference ranges for serial measurements of umbilical artery Doppler indices in the second half of pregnancy. Am J Obstet Gynecol 2005;192:937–44. Bahlmann F, Reinhard I, Krummenauer F, et al. Blood flow velocity waveforms of the fetal middle cerebral artery in a normal population: reference values from 18 weeks to 42 weeks of gestation. J Perinat Med 2002;30:490–501. Baschat AA, Gembruch U. The cerebro-placental Doppler ratio revisited. Ultrasound Obstet Gynecol 2003;21:124–7. Morales Rosello J, Hervas Marı´n D, Fillol Crespo M, Perales Marı´n A. Doppler changes in the vertebral, middle cerebral and umbilical arteries in fetuses delivered after 34 weeks: relationship to severity of growth restriction. Prenat Diagn 2012;32:960–7. Yudkin PL, Aboualfa M, Eyre JA, et al. New birth weight and head circumference centiles for gestational ages 24 to 42 weeks. Early Hum Dev 1987;15:45–52. Morales-Rosello´ J, Khalil A, Morlando M, et al. fetal doppler changes as a marker of failure to reach growth potential at term. Ultrasound Obstet Gynecol 2014;43:303–10. Morales-Rosello´ J, Khalil A, Morlando M, et al. Poor neonatal acidbase status in term fetuses with low cerebro-placental ratios. Ultrasound Obstet Gynecol 2015;45:156–61. Campbell S, Thoms A. Ultrasound measurement of the fetal head to abdomen circumference ratio in the assessment of growth retardation. Br J Obstet Gynaecol 1977;84:165–74. Gestational agele CR, O’Callaghan FJ, Bredow M, Martyn CN; Avon Longitudinal Study of Parents and Children Study Team. The influence of head growth in fetal life, infancy, and childhood on intelligence at the ages of 4 and 8 years. Pediatrics 2006;118: 1486–92. Baschat AA. Ductus venosus Doppler for fetal surveillance in highrisk pregnancies. Clin Obstet Gynecol 2010;53:858–68. Bhorat IE, Bagratee JS, Pillay M, Reddy T. Determination of the myocardial performance index in deteriorating grades of intrauterine growth restriction and its link to adverse outcomes. Prenat Diagn 2015;35:266–73.

Fetal tricuspid annulus plane systolic excursion (fTAPSE) at term - association with cerebroplacental ratio, birthweight and neonatal pH.

To study at term the association of the fetal tricuspid annulus plane systolic excursion (fTAPSE) with gestational age (GA), birthweight (BW), cerebro...
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