Automated quantitative evaluation of fetal atrioventricular annular plane systolic excursion

L Herling, J Johnson, K Ferm-Widlund, A Zamprakou, M Westgren, G Acharya, L Herling, J Johnson, K Ferm-Widlund, A Zamprakou, M Westgren, G Acharya

Abstract

Objectives: The primary aim of this study was to evaluate the feasibility of automated measurement of fetal atrioventricular (AV) plane displacement (AVPD) over several cardiac cycles using myocardial velocity traces obtained by color tissue Doppler imaging (cTDI). The secondary objectives were to establish reference ranges for AVPD during the second half of normal pregnancy, to assess fetal AVPD in prolonged pregnancy in relation to adverse perinatal outcome and to evaluate AVPD in fetuses with a suspicion of intrauterine growth restriction (IUGR).

Methods: The population used to develop the reference ranges consisted of women with an uncomplicated singleton pregnancy at 18-42 weeks of gestation (n = 201). The prolonged-pregnancy group comprised women with an uncomplicated singleton pregnancy at ≥ 41 + 0 weeks of gestation (n = 107). The third study cohort comprised women with a singleton pregnancy and suspicion of IUGR, defined as an estimated fetal weight < 2.5th centile or an estimated fetal weight < 10th centile and umbilical artery pulsatility index > 97.5th centile (n = 35). Cineloops of the four-chamber view of the fetal heart were recorded using cTDI. Regions of interest were placed at the AV plane in the left and right ventricular walls and the interventricular septum, and myocardial velocity traces were integrated and analyzed using an automated algorithm developed in-house to obtain mitral (MAPSE), tricuspid (TAPSE) and septal (SAPSE) annular plane systolic excursion. Gestational-age specific reference ranges were constructed and normalized for cardiac size. The correlation between AVPD measurements obtained using cTDI and those obtained by anatomic M-mode were evaluated, and agreement between these two methods was assessed using Bland-Altman analysis. The mean Z-scores of fetal AVPD in the cohort of prolonged pregnancies were compared between cases with normal and those with adverse outcome using Mann-Whitney U-test. The mean Z-scores of fetal AVPD in IUGR fetuses were compared with those in the normal reference population using Mann-Whitney U-test. Inter- and intraobserver variability for acquisition of cTDI recordings and offline analysis was assessed by calculating coefficients of variation (CV) using the root mean square method.

Results: Fetal MAPSE, SAPSE and TAPSE increased with gestational age but did not change significantly when normalized for cardiac size. The fitted mean was highest for TAPSE throughout the second half of gestation, followed by SAPSE and MAPSE. There was a significant correlation between MAPSE (r = 0.64; P < 0.001), SAPSE (r = 0.72; P < 0.001) and TAPSE (r = 0.84; P < 0.001) measurements obtained by M-mode and those obtained by cTDI. The geometric means of ratios between AVPD measured by cTDI and by M-mode were 1.38 (95% limits of agreement (LoA), 0.84-2.25) for MAPSE, 1.00 (95% LoA, 0.72-1.40) for SAPSE and 1.20 (95% LoA, 0.92-1.57) for TAPSE. In the prolonged-pregnancy group, the mean ± SD Z-scores for MAPSE (0.14 ± 0.97), SAPSE (0.09 ± 1.02) and TAPSE (0.15 ± 0.90) did not show any significant difference compared to the reference ranges. Twenty-one of the 107 (19.6%) prolonged pregnancies had adverse perinatal outcome. The AVPD Z-scores were not significantly different between pregnancies with normal and those with adverse outcome in the prolonged-pregnancy cohort. The mean ± SD Z-scores for SAPSE (-0.62 ± 1.07; P = 0.006) and TAPSE (-0.60 ± 0.89; P = 0.002) were significantly lower in the IUGR group compared to those in the normal reference population, but the differences were not significant when the values were corrected for cardiac size. The interobserver CVs for the automated measurement of MAPSE, SAPSE and TAPSE were 28.1%, 17.7% and 15.3%, respectively, and the respective intraobserver CVs were 33.5%, 15.0% and 17.9%.

Conclusions: This study showed that fetal AVPD can be measured automatically by integrating cTDI velocities over several cardiac cycles. Automated analysis of AVPD could potentially help gather larger datasets to facilitate use of machine-learning models to study fetal cardiac function. The gestational-age associated increase in AVPD is most likely a result of increasing cardiac size, as the AVPD normalized for cardiac size did not change significantly between 18 and 42 weeks. A decrease was seen in TAPSE and SAPSE in IUGR fetuses, but not after correction for cardiac size. © 2021 The Authors. Ultrasound in Obstetrics & Gynecology published by John Wiley & Sons Ltd on behalf of International Society of Ultrasound in Obstetrics and Gynecology.

Keywords: M-mode; annular plane systolic excursion; atrioventricular plane displacement; automated analysis; fetal cardiac function; fetal echocardiography; tissue Doppler imaging.

© 2021 The Authors. Ultrasound in Obstetrics & Gynecology published by John Wiley & Sons Ltd on behalf of International Society of Ultrasound in Obstetrics and Gynecology.

References

REFERENCES

    1. Carlsson M, Ugander M, Mosen H, Buhre T, Arheden H. Atrioventricular plane displacement is the major contributor to left ventricular pumping in healthy adults, athletes, and patients with dilated cardiomyopathy. Am J Physiol Heart Circ Physiol 2007; 292: H1452-1459.
    1. Lundback S. Cardiac pumping and function of the ventricular septum. Acta Physiol Scand Suppl 1986; 550: 1-101.
    1. Acharya G. Measurement of atrioventricular annular plane displacement has been revived: will it prove to be useful in assessing fetal cardiac function? Ultrasound Obstet Gynecol 2013; 42: 125-129.
    1. Carlsson M, Ugander M, Heiberg E, Arheden H. The quantitative relationship between longitudinal and radial function in left, right, and total heart pumping in humans. Am J Physiol Heart Circ Physiol 2007; 293: H636-644.
    1. Asgeirsson D, Hedstrom E, Jogi J, Pahlm U, Steding-Ehrenborg K, Engblom H, Arheden H, Carlsson M. Longitudinal shortening remains the principal component of left ventricular pumping in patients with chronic myocardial infarction even when the absolute atrioventricular plane displacement is decreased. BMC Cardiovasc Disord 2017; 17: 208.
    1. Pahlm U, Seemann F, Engblom H, Gyllenhammar T, Halvorsen S, Hansen HS, Erlinge D, Atar D, Heiberg E, Arheden H, Carlsson M. Longitudinal left ventricular function is globally depressed within a week of STEMI. Clin Physiol Funct Imaging 2018. DOI: 10.1111/cpf.12521.
    1. Henein MY, Priestley K, Davarashvili T, Buller N, Gibson DG. Early changes in left ventricular subendocardial function after successful coronary angioplasty. Br Heart J 1993; 69: 501-506.
    1. Jones CJ, Raposo L, Gibson DG. Functional importance of the long axis dynamics of the human left ventricle. Br Heart J 1990; 63: 215-220.
    1. Carvalho JS, O'Sullivan C, Shinebourne EA, Henein MY. Right and left ventricular long-axis function in the fetus using angular M-mode. Ultrasound Obstet Gynecol 2001; 18: 619-622.
    1. Wandt B, Bojo L, Wranne B. Influence of body size and age on mitral ring motion. Clin Physiol 1997; 17: 635-646.
    1. Cruz-Lemini M, Crispi F, Valenzuela-Alcaraz B, Figueras F, Sitges M, Gomez O, Bijnens B, Gratacos E. Value of annular M-mode displacement vs tissue Doppler velocities to assess cardiac function in intrauterine growth restriction. Ultrasound Obstet Gynecol 2013; 42: 175-181.
    1. Gardiner HM, Pasquini L, Wolfenden J, Barlow A, Li W, Kulinskaya E, Henein M. Myocardial tissue Doppler and long axis function in the fetal heart. Int J Cardiol 2006; 113: 39-47.
    1. Herling L, Johnson J, Ferm-Widlund K, Lindgren P, Acharya G, Westgren M. Automated analysis of color tissue Doppler velocity recordings of the fetal myocardium using a new algorithm. Cardiovasc Ultrasound 2015; 13: 39.
    1. Herling L, Johnson J, Ferm-Widlund K, Bergholm F, Elmstedt N, Lindgren P, Sonesson SE, Acharya G, Westgren M. Automated analysis of fetal cardiac function using color tissue Doppler imaging in second half of normal pregnancy. Ultrasound Obstet Gynecol 2019; 53: 348-357.
    1. Saltvedt S, Almstrom H, Kublickas M, Reilly M, Valentin L, Grunewald C. Ultrasound dating at 12-14 or 15-20 weeks of gestation? A prospective cross-validation of established dating formulae in a population of in-vitro fertilized pregnancies randomized to early or late dating scan. Ultrasound Obstet Gynecol 2004; 24: 42-50.
    1. Herling L, Johnson J, Ferm-Widlund K, Bergholm F, Lindgren P, Sonesson SE, Acharya G, Westgren M. Automated analysis of fetal cardiac function using color tissue Doppler imaging. Ultrasound Obstet Gynecol 2018; 52: 599-608.
    1. Marsal K, Persson PH, Larsen T, Lilja H, Selbing A, Sultan B. Intrauterine growth curves based on ultrasonically estimated foetal weights. Acta Paediatr 1996; 85: 843-848.
    1. Arstrom K, Eliasson A, Hareide JH, Marsal K. Fetal blood velocity waveforms in normal pregnancies. A longitudinal study. Acta Obstet Gynecol Scand 1989; 68: 171-178.
    1. Bergholm F. En algoritm för att finna maxima och minima i “periodisk” kolvliknande rörelse. KTH Technology and Health: Stockholm, Sweden, 2016.
    1. Garcia-Otero L, Gomez O, Rodriguez-Lopez M, Torres X, Soveral I, Sepulveda-Martinez A, Guirado L, Valenzuela-Alcaraz B, Lopez M, Martinez JM, Gratacos E, Crispi F. Nomograms of Fetal Cardiac Dimensions at 18-41 Weeks of Gestation. Fetal Diagn Ther 2020; 47: 387-398.
    1. Lee-Tannock A, Hay K, Gooi A, Kumar S. Longitudinal Reference Ranges for Tricuspid Annular Plane Systolic Excursion and Mitral Annular Plane Systolic Excursion in Normally Grown Fetuses. J Ultrasound Med 2020; 39: 929-937.
    1. Peixoto AB, Bravo-Valenzuela NJ, Martins WP, Tonni G, Mattar R, Moron AF, Pares DB, Araujo Júnior E. Reference ranges for the fetal mitral, tricuspid, and interventricular septum annular plane systolic excursions (mitral annular plane systolic excursion, tricuspid annular plane systolic excursion, and septum annular plane systolic excursion) between 20 and 36 + 6 weeks of gestation. J Perinat Med 2020; 48: 601-608.
    1. Royston P, Wright EM. How to construct ‘normal ranges’ for fetal variables. Ultrasound Obstet Gynecol 1998; 11: 30-38.
    1. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986; 1: 307-310.
    1. Bland JM, Altman DG. Measuring agreement in method comparison studies. Stat Methods Med Res 1999; 8: 135-160.
    1. Acharya G, Sitras V, Erkinaro T, Makikallio K, Kavasmaa T, Pakkila M, Huhta JC, Rasanen J. Experimental validation of uterine artery volume blood flow measurement by Doppler ultrasonography in pregnant sheep. Ultrasound Obstet Gynecol 2007; 29: 401-406.
    1. Hyslop NP, White WH. Estimating precision using duplicate measurements. J Air Waste Manag Assoc 2009; 59: 1032-1039.
    1. Mao YK, Zhao BW, Wang B. Z-Score Reference Ranges for Angular M-Mode Displacement at 22-40 Weeks' Gestation. Fetal Diagn Ther 2017; 41: 115-126.
    1. Batterham A, Shave R, Oxborough D, Whyte G, George K. Longitudinal plane colour tissue-Doppler myocardial velocities and their association with left ventricular length, volume, and mass in humans. Eur J Echocardiogr 2008; 9: 542-546.
    1. Patey O, Carvalho JS, Thilaganathan B. Perinatal changes in cardiac geometry and function in growth-restricted fetuses at term. Ultrasound Obstet Gynecol 2019; 53: 655-662.
    1. Kiserud T, Ebbing C, Kessler J, Rasmussen S. Fetal cardiac output, distribution to the placenta and impact of placental compromise. Ultrasound Obstet Gynecol 2006; 28: 126-136.
    1. Hobbins JC, Gumina DL, Zaretsky MV, Driver C, Wilcox A, DeVore GR. Size and shape of the four-chamber view of the fetal heart in fetuses with an estimated fetal weight less than the tenth centile. Am J Obstet Gynecol 2019; 221: 495.e1-9.

Source: PubMed

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