ORIGINAL RESEARCH ARTICLE

https://doi.org/10.5005/jp-journals-10009-1951
Donald School Journal of Ultrasound in Obstetrics and Gynecology
Volume 16 | Issue 4 | Year 2022

Fetal Cardiac Structures, Shape, and Aortic Tortuosity at 15–17 + 6 Weeks of Gestation: HDlive Flow Study

Toshiyuki Hata¹, Aya Koyanagi², Tomomi Kawahara³, Miyu Konishi⁴, Saori Bouno⁵, Tomomi Yamanishi⁶, Yasunari Miyagi⁷, Takahito Miyake⁸

¹Department of Obstetrics and Gynecology, Miyake Clinic, Minami-ku, Okayama, Japan; Department of Perinatology and Gynecology, Kagawa University Graduate School of Medicine, Miki, Kagawa, Japan

^2–6Department of Obstetrics and Gynecology, Miyake Clinic, Minami-ku, Okayama, Japan

⁷Department of Gynecology, Miyake Ofuku Clinic, Minami-ku, Okayama, Japan

⁸Department of Obstetrics and Gynecology, Miyake Clinic, Minami-ku, Okayama, Japan; Department of Perinatology and Gynecology, Kagawa University Graduate School of Medicine, Miki, Kagawa, Japan; Department of Gynecology, Miyake Ofuku Clinic, Minami-ku, Okayama, Japan

Corresponding Author: Toshiyuki Hata, Department of Obstetrics and Gynecology, Miyake Clinic, Minami-ku, Okayama, Japan; Department of Perinatology and Gynecology, Kagawa University Graduate School of Medicine, Miki, Kagawa, Japan, Phone: +81087812174, e-mail: hata.toshiyuki@kagawa-u.ac.jp, toshi28@med.kagawa-u.ac.jp

Received on: 19 October 2022; Accepted on: 28 October 2022; Published on: 26 December 2022

ABSTRACT

Objective: To examine fetal cardiac structures at 15–17 + 6 weeks of gestation using HDlive Flow with spatio-temporal image correlation (STIC). Assessments of the fetal cardiac shape and tortuosity of the descending aorta (DAo) were also conducted.

Methods: Transabdominal HDlive Flow with STIC was performed on 101 normal fetuses at 15–17 + 6 weeks of gestation to evaluate the feasibility of the spatial three-vessel and panoramic views (PaVs). Target structures were examined in both views. The following ratings were used: “good” when all structures were identified, “fair” when only one structure was missing, and “poor” when two or more structures were missing. The fetal cardiac circumference (FCC) was obtained with ellipse measurements in the spatial four-chamber view. The spatial global sphericity index (GSI) to assess the fetal cardiac shape and the aortic tortuosity index (ATI) to evaluate fetal aortic tortuosity were also calculated.

Results: The rates of “good,” “fair,” and “poor” were 81.8, 16.2, and 2%, respectively, in the spatial three-vessel view (3VV) and 27.3, 64.6, and 8.1%, respectively, in the PaV. FCC was 3.59 (mean) ± 1.16 mm [standard deviation (SD)]. Spatial GSI was 1.15 (mean) ± 0.34 (SD). Posterior ATI was 0.97 (mean) ± 0.07 (SD). Lateral ATI was 0.988 (mean) ± 0.458 (SD).

Conclusion: HDlive Flow with STIC has the potential as a useful diagnostic modality to assess fetal cardiac structures and aortic tortuosity in the early stages of the second trimester. Furthermore, spatial GSI and ATI may be applied to evaluations of the fetal cardiac shape and aortic tortuosity.

How to cite this article: Hata T, Koyanagi A, Kawahara T, et al. Fetal Cardiac Structures, Shape, and Aortic Tortuosity at 15–17 + 6 Weeks of Gestation: HDlive Flow Study. Donald School J Ultrasound Obstet Gynecol 2022;16(4):272-277.

Source of support: Nil

Conflict of interest: None

Keywords: Aortic tortuosity index, Early second trimester, Fetal aortic tortuosity, Fetal heart shape, HDlive Flow with spatio-temporal image correlation, Spatial global sphericity index

INTRODUCTION

Previous studies proposed the application of five fetal cardiac views (the frontal, spatial three-vessel, panoramic, posterior, and right lateral views) using HDlive Flow with STIC to assessments of normal and abnormal fetal cardiac structures.¹^-³ However, success rates differed among these cardiac views between 12–14 + 6 and 18–21 + 6 weeks of gestation, but not between 18–21 + 6 and 28–31 + 6 weeks of gestation.²^,³

Hata et al.³ reported various cardiac shapes and aortic tortuosity at 12–14 + 6 weeks of gestation; however, their judgments were subjective. Therefore, fetal cardiac structures at 15–17 + 6 weeks of gestation were examined in the present study using HDlive Flow with STIC. Evaluations of the fetal cardiac shape and tortuosity of the DAo were also performed using the spatial GSI and ATI.

MATERIALS AND METHODS

To assess the feasibility of the spatial three-vessel and PaVs, 101 normal fetuses at a gestational age (GA) of 15–17 + 6 weeks were subjected to HDlive Flow with STIC between January and September 2021. Target structures were examined in both views (Table 1 and Figs 1 and 2). We previously described these cardiac views in detail.²^-⁴ Participants comprised healthy nonsmokers with singleton pregnancies. The following pregnancies with a high maternal or fetal risk were excluded: hypertensive disorders of pregnancy, gestational diabetes mellitus, thyroid disease, fetal growth restriction, polyhydramnios, oligohydramnios, and chromosomal abnormalities. Two-dimensional (2D) sonography was performed to calculate GAs based on crown-rump length measurements in the first trimester.⁵ All fetuses grew normally, and no fetal abnormalities were detected in ultrasound examinations. There were also no congenital anomalies or genetic disorders.

**Table 1:** Target structures with each cardiac view
Cardiac view	Target structure
Spatial 3VV	Ao	LV	PA	RV	SVC
Panoramic view	AoA	DA	DAo	IVC	LA	LV	PA	RV

3VV, Three-vessel view; Ao, Aorta; AoA, Aortic arch; DA, Ductus arteriosus; DAo, Descending aorta; IVC, Inferior vena cava; LA, Left atrium; LV, Left ventricle; PA, Pulmonary artery; RA, Right atrium; RV, Right ventricle; SVC, Superior vena cava

Fig. 1: Spatial 3VV of a normal fetal heart using HDlive Flow at 16 weeks and 3 days of gestation. Ao, Aorta; LV, Left ventricle; PA, Pulmonary artery; RV, Right ventricle; SVC, Superior vena cava

Fig. 2: Panoramic view (PaV) of a normal fetal heart using HDlive Flow at 15 weeks of gestation. AoA, Aortic arch; DA, Ductus arteriosus; DAo, Descending aorta; DV, Ductus venosus; HV, Hepatic vein; IVC, Inferior vena cava; LA, Left atrium; LV, Left ventricle; PA, Pulmonary artery; RV, Right ventricle; SVC, Superior vena cava; UV, Umbilical vein

Two-dimensional sonographic anomaly scans were performed in the mid-second (18–21 + 6 weeks) and early third (28–31 + 6 weeks) trimesters according to the guidelines of the International Society of Obstetrics and Gynecology in order to exclude the presence of fetal abnormalities. Japanese growth charts were used to measure fetal growth.⁶ Each singleton pregnancy was assessed once. All fetuses grew normally, and HDlive Flow with STIC did not detect any fetal abnormalities at 15–17 + 6, 18–21 + 6, or 28–31 + 6 weeks of gestation.

All examinations were performed using a curved array transabdominal transducer (GE eM6C G2, 2–7 MHz) with Voluson E10 BT20 (GE Healthcare, Zipf, Austria). The Ethics Committee of Miyake Clinic, Okayama, Japan approved the protocols used in the present study. All participants provided their written informed consent after obtaining a full explanation of the aims of this study.

An experienced examiner (TH) performed 2D sonographic examinations and STIC volume data acquisition at 15–17 + 6 weeks of gestation. Volume datasets on the fetal heart were acquired during an automated transverse or sagittal sweep of the anterior chest wall with STIC. Maximal sensitivity was achieved using a pulse repetition frequency of 1.3 kHz and a wall motion filter of “mid 2.” The following constant default instrument settings (corresponding to the Doppler power setting of the manufacturer) were used in each examination: dynamic, balance, 225; smooth, 3/4; ensemble, 8; line density, 7; power Doppler map, 1; artifact suppression, on; power Doppler line filter, 3; quality, normal. Volume acquisition by the curved array transabdominal transducer was conducted at an acquisition angle of 20 or 25° and was completed within 10 seconds. Recordings with a transabdominal probe were performed between one and three times. Due to fetal movement, volume acquisition was repeated to ensure that satisfactory data had been obtained. Each participant underwent 2D sonography to monitor the fetus prior to HDlive Flow with STIC. HDlive Flow of the fetal heart was then performed and displayed. Volume datasets for each participant were examined with the selection of optimal images for more detailed analyses. The following ratings were used: “good” when all structures were identified, “fair” when only one structure was missing, and “poor” when two or more structures were missing. Since we previously achieved good intra and interobserver agreements on the scores for each cardiac view,²^,³ success rates were evaluated by one examiner (AK) only in the present study.

In the spatial four-chamber view, an ellipse was adjusted along with the margin of HDlive Flow silhouette mode of the fetal heart in diastole (the automated ellipse method) (Fig. 3). The FCC, the longest length of the basal-apical length (D1), and the widest transverse length orthogonal to D1 (D2) were automatically measured according to machine settings. Spatial GSI was calculated as D1/D2.

Fig. 3: The spatial GSI in the spatial four-chamber view at 17 weeks and 4 days of gestation. D1, Basal-apical length; D2, The widest transverse length orthogonal to D1. Ao, Aorta; LA, Left atrium; LV, Left ventricle; PA, Pulmonary artery; RA, Right atrium; RV, Right ventricle

Aortic tortuosity was evaluated with ATI. ATI was defined as the kinking angle of the aortic tortuosity lesion divided by 180 (Figs 4 and 5). Lateral and posterior ATIs were assessed.

Fig. 4: Posterior fetal aortic tortuosity at 17 weeks and 2 days of gestation. The posterior ATI (1 Å) is measured. DAo, Descending aorta; LA, Left atrium; LV, Left ventricle

Fig. 5: Lateral fetal aortic tortuosity at 16 weeks and 2 days of gestation. The lateral ATI (1 Å) is measured. AoA, Aortic arch; DAo, Descending aorta; HV, Hepatic vein; IVC, Inferior vena cava; LA, Left atrium; LV, Left ventricle; PA, Pulmonary artery; RV, Right ventricle

The rates of “good,” “fair,” and “poor” in each cardiac view were compared among 12–14 + 6,³ 15–17 + 6, and 18–21 + 6² weeks of gestation using the Chi-square test with a 3 × 3 contingency table. Intra (AK) and interobserver (AK and TH) agreements for FCC, spatial GSI, and lateral and posterior ATIs were conducted on 30 fetuses. Intra and interclass correlation coefficients were used to measure the reliability of ratings,⁷ were defined as a correlation between any two measurements from the same FCC, spatial GSI, and lateral and posterior ATIs, and ranged between zero and one, with zero indicating maximum reliability. Intra and interobserver variabilities in 30 samples were assessed by AK and by AK and TY, respectively, using a previously reported method.⁸ In this analysis, differences between measurements (the y-axis) were plotted against the mean (the x-axis) on a graph. The 95% limits of individual agreements between two measurements were calculated as the mean difference between two measurements ±2.0 SD. The difference between the mean difference and zero was examined using a two-sample t-test. Statistical analyses were performed using the statistical software Mathematica 13.0.0.0 (Wolfram Research, Champaign, Illinois, United States of America), and the significance of differences was set at p < 0.05.

RESULTS

The present study enrolled 101 fetuses at 15–17 + 6 weeks of gestation. Two fetuses lacking data on maternal and perinatal outcomes or perinatal management and delivery in other hospitals were excluded. Therefore, 99 fetuses at 15–17 + 6 weeks were analyzed. The clinical characteristics of participants are shown in Table 2. Data acquisition and analyses were completed within 30 minutes.

**Table 2:** Clinical characteristics of subjects
Subjects	n	Maternal age (yo) Median (range)	Para median (range)	Examination week (weeks) mean (SD)	Birth age (weeks) mean (SD)	Birth weight (gm) mean (SD)	Sex (male/female)	Apgar score		UApH mean (SD)	Neonatal abnormality (%)
Subjects	n	Maternal age (yo) Median (range)	Para median (range)	Examination week (weeks) mean (SD)	Birth age (weeks) mean (SD)	Birth weight (gm) mean (SD)	Sex (male/female)	1-minute median (range)	5-minute median (range)	UApH mean (SD)	Neonatal abnormality (%)
15–17-week-old fetuses	99	32 (20–41)	1 (0–3)	16.6 (0.7)	39.2 (1.3)	3003.1 (371.1)	47/52	9 (6–9)	10 (7–10)	7.315 (0.066)	0

yo, Years old; SD, Standard deviation; UApH, Umbilical artery blood pH

The rates of “good,” “fair,” and “poor” were 81.8, 16.2, and 2%, respectively, in the spatial 3VV and 27.3, 64.6, and 8.1%, respectively, in the PaV (Table 3). Significant differences were observed in the success rates of the spatial 3VV among 12–14 + 6, 15–17 + 6, and 18–21 + 6 weeks (p = 0.0000614) (Table 3 and Fig. 6) but not in those of the PaV (Table 3 and Fig. 7).

**Table 3:** Detection rates with each cardiac view at different gestational weeks
Cardiac view	GA (weeks)	Study	n	Detection rate (%)			Significance
Cardiac view	GA (weeks)	Study	n	Good	Fair	Poor	Significance
Spatial 3VV	12–14 + 6	Hata et al.³	49	55.1	42.9	2	0.0000614
	15–17 + 6	Present study	99	81.8	16.2	2
	18–21 + 6	Hata et al.²	44	95.5	4.5	0
Panoramic view	12–14 + 6	Hata et al.³	49	36.7	51	12.3	NS
	15–17 + 6	Present study	99	27.3	64.6	8.1
	18–21 + 6	Hata et al.²	44	43.2	54.5	2.3

3VV, Three-vessel view; GA, Gestational age; NS, Not significant

Fig. 6: Success rates in the spatial 3VV at 12–14 + 6,³ 15–17 + 6, and 18–21 + 6² weeks of gestation

Fig. 7: Success rates in the PaV at 12–14 + 6,³ 15–17 + 6, and 18–21 + 6² weeks of gestation

Regarding the intraobserver agreement, Table 4 shows the mean difference between measurements and the limits of agreement for each of the parameters tested. The mean percentage difference and 95% limit of the intraobserver agreement were 0.006% (0.027, −0.015), 0.003% (0.014, −0.008), 0.001% (0.002 and 0.000), and 0.000% (0.002, −0.001) for FCC, spatial GSI, posterior ATI, and lateral ATI, respectively. No significant differences were observed between the mean difference and zero for any parameter. Table 4 also shows intraclass correlation coefficients (ICC) for each of the parameters tested. ICCs for FCC, spatial GSI, posterior ATI, and lateral ATI were 0.994, 0.970, 0.999, and 0.997, respectively (p < 0.001).

**Table 4:** ICC and intraobserver agreement for each parameter
Parameter	Mean difference	95% CI		p-value	Limits of agreement		ICC	p-value
Parameter	Mean difference	Lower	Upper	p-value	Lower	Upper	ICC	p-value
FCC	0.006	−0.015	0.027	0.580	−0.109	0.121	0.994	<0.001
Spatial GSI	0.003	−0.008	0.014	0.615	−0.060	0.066	0.970	<0.001
Posterior ATI	0.001	0.000	0.002	0.043	−0.005	0.008	0.999	<0.001
Lateral ATI	0.000	−0.001	0.002	0.488	−0.009	0.010	0.997	<0.001

95% CI, 95% confidence interval; ATI, Aortic tortuosity index; FCC, Fetal cardiac circumference; GSI, Global sphericity index; ICC, Intraclass correlation coefficient

Table 5 shows the mean difference between the two investigators (AK and TH) and the limits of agreement for each of the parameters tested. The mean percentage difference and 95% limits of intraobserver agreement were −0.018% (0.078, −0.115), 0.028% (0.066, −0.010), −0.002% (0.007, −0.012), and 0.005% (0.011, −0.001) for FCC, spatial GSI, posterior ATI, and lateral ATI, respectively. No significant difference was observed between the mean difference and zero for any parameter. Also shows ICCs for each of the parameters tested. Intraclass correlation coefficients for FCC, spatial GSI, posterior ATI, and lateral ATI were 0.918, 0.654, 0.947, and 0.983, respectively (p < 0.001).

**Table 5:** Interclass correlation coefficient and interobserver agreement for each parameter
Parameter	Mean difference	95% CI		p-value	Limits of agreement		ICC	p-value
Parameter	Mean difference	Lower	Upper	p-value	Lower	Upper	ICC	p-value
FCC	−0.018	−0.115	0.078	0.712	−0.547	0.511	0.918	<0.001
Spatial GSI	0.028	−0.010	0.066	0.162	−0.181	0.237	0.654	<0.001
Posterior ATI	−0.002	−0.012	0.007	0.647	−0.056	0.051	0.947	<0.001
Lateral ATI	0.005	−0.001	0.011	0.121	−0.030	0.041	0.983	<0.001

95% CI, 95% confidence interval; ATI, Aortic tortuosity index; FCC, Fetal cardiac circumference; GSI, Global sphericity index; ICC, Intraclass correlation coefficient

Collectively, the present results confirmed good intra and interclass correlation coefficients as well as intra and interobserver agreements for FCC, spatial GSI, posterior ATI, and lateral ATI. Therefore, the values measured by one examiner (AK) were used in statistical analyses.

Fetal cardiac circumference, spatial GSI, posterior ATI, and lateral ATI values are shown in Table 6. Due to insufficient Doppler data or excessive fetal movements, six fetuses for FCC, seven for spatial GSI, and 24 for posterior and lateral ATIs were excluded from the analysis. FCC was 3.59 (mean) ± 1.16 mm (SD). Spatial GSI was 1.15 (mean) ± 0.34 (SD). Posterior ATI was 0.97 (mean) ± 0.07 (SD). Posterior aortic tortuosity was detected in 11 out of 75 fetuses (14.7%). Lateral ATI was 0.988 (mean) ± 0.458 (SD). Lateral aortic tortuosity was detected in five out of 75 fetuses (6.7%). Tortuosity of the DAo was noted in two fetuses (2.7%) (Fig. 8).

**Table 6:** Each parameter value of the fetal heart at 15–17 + 6 weeks of gestation
Parameter	n	Mean (SD)
FCC (mm)	93	3.59 (1.16)
Spatial GSI	92	1.15 (0.34)
Posterior ATI	75	0.97 (0.07)
Lateral ATI	75	0.988 (0.458)

ATI, Aortic tortuosity index; FCC, Fetal cardiac circumference; GSI, Global sphericity index; SD, Standard deviation

DISCUSSION

Ito et al.¹ initially employed basic cardiac views, such as the spatial three-vessel and PaVs, using HDlive Flow to examine normal and abnormal cardiac structures at 18–34 weeks of gestation. They reported visualization rates in the spatial three-vessel and PaVs of 91.6 and 81.3%, respectively. However, a clear definition of each cardiac view was not provided. Hata et al.² defined the visualization of each cardiac view using HDlive Flow and showed that the rates of “good,” “fair,” and “poor” in the spatial 3VV were 95.5, 4.5, and 0%, respectively, at 18–21 weeks of gestation and 98.5, 1.5, and 0%, respectively, at 28–31 weeks of gestation. These rates in the PaV were 43.2, 54.5, and 2.3%, respectively, at 18–21 weeks of gestation and 46.2, 52.3, and 1.5%, respectively, at 28–31 weeks of gestation. Hata et al.³ also reported success rates in the spatial three-vessel and PaVs using HDlive Flow at 12–14 + 6 weeks of gestation. The rates of “good,” “fair,” and “poor” were 55.1, 42.9, and 2%, respectively, in the spatial 3VV and 36.7, 51, and 12.3%, respectively, in the PaV. In the present study, the rates of “good,” “fair,” and “poor” at 15–17 + 6 weeks were 81.8, 16.2, and 2%, respectively, in the spatial 3VV and 27.3, 64.6, and 8.1%, respectively, in the PaV. Therefore, success rates in the spatial 3VV late in the first trimester appeared to be inferior to those in the second trimester of pregnancy, whereas success rates in the PaV remained the same throughout pregnancy. Collectively, these results suggest that the HDlive Flow depiction of fetal cardiac structures is more accurate in the second trimester.

Hata et al.³ revealed different fetal cardiac shapes using HDlive Flow in the late stages of the first trimester. However, their judgments were subjective. DeVore et al.⁹ proposed GSI as an objective parameter to evaluate the fetal cardiac shape in the four-chamber view using 2D sonography. The 50th percentile of GSI in normal fetuses at 20–40 weeks of gestation was 1.233 (SD, 0.0953). In the present study, we constructed spatial GSI to assess the three-dimensional fetal cardiac shape using HDlive Flow. The mean spatial GSI at 15–17 + 6 weeks of gestation was 1.15, which was slightly lower than that at 20–40 weeks. These results indicate that the fetal cardiac shape at 15–17 + 6 weeks is still primitive because the fetal heart continues to develop before 20 weeks of gestation.³

A previous study reported fetal aortic tortuosity in normal fetuses at 12–14 + 6 weeks of gestation.³ We herein assessed fetal aortic tortuosity using ATI by HDlive Flow in normal fetuses at 15–17 + 6 weeks of gestation and detected posterior and lateral aortic tortuosity. Moreover, tortuosity of the DAo was identified. Fetal aortic tortuosity may still be a developmental phenomenon before 20 weeks of gestation. ATI may also become a new parameter for evaluating fetal aortic tortuosity during pregnancy.

Figs 8A and B: Tortuosity of the descending aorta (DAo) at 15 weeks and 3 days of gestation; (A) Panoramic view; (B) Posterior view

REFERENCES

1. Ito M, AboEllail MAM, Yamamoto K, et al. HDlive Flow silhouette mode and spatiotemporal image correlation for diagnosing congenital heart disease. Ultrasound Obstet Gynecol 2017;50(3):411–415. DOI: 10.1002/uog.17519

2. Hata T, Koyanagi A, Yamanishi T, et al. Success rate of five cardiac views using HDlive Flow with spatiotemporal image correlation at 18–21 and 28–31 weeks of gestation. J Perinat Med 2020;48(4):384–388. DOI: 10.1515/jpm-2019-0434

3. Hata T, Koyanagi A, Kawahara T, et al. HDlive Flow silhouette with STIC for assessment of fetal cardiac structures at 12 to 14 + 6 weeks of gestation. J Perinat Med 2021;50(3):313–318. DOI: 10.1515/jpm-2021-0252

4. Hata T, Hanaoka U, Kanenishi K. HDlive Flow silhouette mode for fetal heart. Donald School J Ultrasound Obstet Gynecol 2019;13(1):10–22. DOI: 10.5005/jp-journals-10009-1581

5. Iwamoto K. Estimation of gestational age with ultrasonic measurement of the fetus in each trimester. Nihon Sanka Fujinka Gakkai Zasshi 1983;35(12):2330–2338.

6. Kuno A, Akiyama M, Yanagihara T, et al. Comparison of fetal growth in singleton, twin, and triplet pregnancies. Hum Reprod 1999;14(5):1352–1360. DOI: 10.1093/humrep/14.5.1352

7. Mercé LT, Barco MJ, Bau S. Reproducibility of the study of placental vascularization by three-dimensional power Doppler. J Perinat Med 2004;32(3):228–233. DOI: 10.1515/JPM.2004.043

8. Bland JM, Altman DG. Statistical methods for assessing agreement between two methods of clinical measurement. Lancet 1986;1(8476):307–310. DOI: 10.1016/S0140-6736(86)90837-8

9. DeVore GR, Satou G, Sklansky M. Abnormal fetal findings associated with a global sphericity index of the 4-chamber view below the 5th centile. J Ultrasound Med 2017;36(11):2309–2318. DOI: 10.1002/jum.14261

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