All participants volunteered for a longitudinal three-dimensional ultrasound (3D-US) evaluation, with examinations during the first trimester of pregnancy at 9 and 11 weeks of GA. Three-dimensional ultrasound examinations were performed using the Voluson E8 ultrasound system (GE Medical Systems, Zipf, Austria) and a 6–12 MHz transvaginal transducer. During the ultrasound examinations different 3D-US sweeps were obtained, namely ones with focus on the whole embryo and separate ones with a focus on the embryonic head. Additionally, different sweeps were obtained, by using two orthogonal planes as a starting point.

The semi-automated embryonic volume (EV) measurements were performed using a virtual reality system called the Barco I-Space (Barco N.V., Kortrijk, Belgium). The virtual reality system, special software (V-Scope) creates an interactive hologram for the EV measurement (Rousian et al., 2010, 2013). Embryonic brain measurements were performed offline using specialized software (4D View, version 5.0, GE Medical Systems), available on the ultrasound machine. Only volumes with clear demarcation of the brain structures and without motion artifacts were used for analysis. Embryonic brain measurements included diencephalon total diameter (DTD), mesencephalon total diameter (MTD) and left and right telencephalon thickness (TTL and TTR) (Fig. 1). The methods and reliability of these embryonic brain measurements have been described previously by our group, with intraclass correlation coefficient values of the inter- and intra-observer variability analysis above 0.98, representing very good reliability between the measurements (Gijtenbeek et al., 2014). In an axial plane, demarcation of the borders of the diencephalon and mesencephalon was determined, and the maximal diameter of the structures was measured by placing the calipers on the outer borders. The TTL and TTR were measured in the same axial plane in a 45-degree line from the longitudinal axis of the embryonic brain.

Embryonic brain measurements. (A) Midsagittal plane showing the place (yellow line) where the axial plane is made to perform the embryonic brain measurements, 9 weeks of GA. (B) Axial plane, 9 weeks of GA; 1 = DTD, 2 = MTD, 3 =TTL, 4 = TTR. (C) Axial plane, 11 weeks of GA; 1 = DTD, 2 = MTD, 3 = TTL, 4 = TTR. (D) Diagram of the axial plane, 11 weeks of GA, 1 = DTD, 2 = MTD, 3 = TTL, 4 = TTR. GA, gestational age; DTD, diencephalon total diameter; MTD, mesencephalon total diameter; TTL, telencephalon thickness left; TTR, telencephalon thickness right.

The measurements in the reconstructed axial plane at 9 and 11 weeks of GA are depicted in Fig. 1A–D. To enhance precision one investigator, trained according to protocol, performed all measurements. This investigator was blinded for the maternal characteristics while performing the brain measurements.

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