IMAGES IN OBSTETRICS


https://doi.org/10.5005/jp-journals-10009-1945
Donald School Journal of Ultrasound in Obstetrics and Gynecology
Volume 16 | Issue 4 | Year 2022

Superb Microvascular Imaging Generation 4 for Depiction of Fetal Peripheral Microvessels


Toshiyuki Hata1, Tomomi Kawahara2, Aya Koyanagi3, Riko Takayoshi4, Takahito Miyake5

1,4,5Department of Obstetrics and Gynecology, Miyake Clinic, Minami-ku, Okayama, Japan; Department of Perinatology and Gynecology, Kagawa University Graduate School of Medicine, Miki, Kagawa, Japan

2,3Department of Obstetrics and Gynecology, Miyake 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: +810878912174, e-mail: hata.toshiyuki@kagawa-u.ac.jp

Received on: 22 August 2022; Accepted on: 30 August 2022; Published on: 26 December 2022

ABSTRACT

Objective: To demonstrate fetal peripheral microvessels using superb microvascular imaging generation 4 (SMI Gen4).

Materials and methods: A total of 20 healthy fetuses were studied to depict peripheral microvessels using SMI Gen4 with a transabdominal linear probe (5–18 MHz) at 13–36 weeks of gestation.

Results: Fetal intracranial vessels were clearly identified early in the second trimester of pregnancy. Superficial temporal and anterior auricular arteries could be recognized. The adrenal microvasculature was also evident. Microvessels of the fingers could be noted. Moreover, microvessels of the thigh, knee, foot, and digital vessels of the toes could be clearly identified.

Conclusion: Superb microvascular imaging generation 4 (SMI Gen4) will be a breakthrough approach for the depiction of fetal peripheral microvessels and organ microvasculature. Further studies involving a larger sample size are needed to ascertain the clinical relevance of SMI Gen4 in clinical fetal medicine and future fetal research.

How to cite this article: Hata T, Kawahara T, Koyanagi A, et al. Superb Microvascular Imaging Generation 4 for Depiction of Fetal Peripheral Microvessels. Donald School J Ultrasound Obstet Gynecol 2022;16(4):329-334.

Source of support: Nil

Conflict of interest: None

Keywords: Anterior auricular artery, Digital artery, Fetal peripheral microvessel, Popliteal artery, Superb microvascular imaging generation 4, superficial temporal artery

INTRODUCTION

There have been several studies on SMI imaging of fetal intracranial, intrathoracic, and intra-abdominal vessels and organ microvasculature,1-5 and normal and abnormal placentas.6-11 With the latest advances in SMI technology, SMI Gen4 has been generated to expand the range of visible blood flow that can be visualized from ultralow to high flow with low noise and good sensitivity. The characteristics of this novel technology are a higher velocity scale, less clutter noise, higher image quality in the background, and higher frame rate in the background. To the best of our knowledge, no study that detected fetal peripheral microvessels using SMI Gen4 has been reported. In the current study, we demonstrated fetal peripheral microvessels using this modality.

MATERIALS AND METHODS

A total of 20 healthy fetuses were studied to depict peripheral microvessels using SMI Gen4 (Canon Aplio i700, Canon Medical Systems, Tokyo, Japan) with a transabdominal linear probe (Canon i18LX5, 5–18 MHz, Canon Medical Systems, Tokyo, Japan) at 13–36 weeks of gestation. Pregnancies with a high maternal or fetal risk (hypertensive disorders of pregnancy, gestational diabetes, thyroid disease, fetal growth restriction (FGR), polyhydramnios, oligohydramnios, and chromosomal abnormalities) were excluded from the study. The gestational age was calculated from crown-rump length measurements at 8–10+6 weeks of gestation and confirmed by second-trimester two-dimensional sonographic examinations.

Superb microvascular imaging generation 4 (SMI Gen4) examinations were performed by one experienced examiner (T.H.). The study was conducted following approval by the Ethics Committee of Miyake Clinic. All participants provided oral informed consent after a full explanation of the aim of the study.

RESULTS

Fetal intracranial vessels and the hyaloid artery were clearly identified early in the second trimester of pregnancy (Figs 1 to 3). Superficial temporal and anterior auricular arteries could be recognized (Figs 4 and 5).

Fig. 1: Circle of Willis depicted with SMI G4 at 14 weeks of gestation. MCA, middle cerebral artery; PComm, posterior communicating artery

Fig. 2: Fetal intracranial blood vessels depicted with SMI Gen4 at 14 weeks of gestation. Lenticulostriate arteries (LSA) can be clearly recognized; MCA, middle cerebral artery

Fig. 3: Fetal hyaloid artery (FHA) depicted with SMI Gen4 at 17 weeks of gestation; L, lens

Fig. 4: Ear microvessels depicted with SMI Gen4 at 26 weeks and 1 day of gestation. Superficial temporal artery (STA) and its branches (arrows, anterior auricular arteries) are clearly noted; E, ear

Fig. 5: Ear microvessels depicted with SMI Gen4 at 26 weeks and 1 day of gestation. Anterior auricular arteries (arrows) are evident; E, ear

Hepatic, splenic, adrenal, and renal microvasculatures were also clearly evident using SMI Gen4 (Figs 6 to 9).

Fig. 6: Hepatic microvasculature depicted with SMI G4 at 17 weeks and 5 days of gestation. St, stomach

Fig. 7: Splenic microvasculature depicted with SMI Gen4 at 31 weeks and 6 days of gestation. Sp, spleen; St, stomach

Fig. 8: Adrenal microvasculature depicted with SMI Gen4 at 31 weeks and 6 days of gestation

Fig. 9: Renal microvasculature depicted with SMI Gen4 at 35 weeks and 5 days of gestation. LK, left kidney

Microvessels of fingers could be noted (Fig. 10). Microvessels of the thigh were clearly depicted (Fig. 11). Microvessels of the fetal knee could be depicted at 13 weeks and 4 days of gestation (Fig. 12). Moreover, microvessels of the foot and digital vessels of the toes could be clearly identified (Figs 13 and 14).

Fig. 10: Digital arteries (arrows) of the middle finger (MF) depicted with SMI Gen4 at 26 weeks and 1 day of gestation. RF, ring finger

Fig. 11: Thigh microvasculature depicted with SMI Gen4 at 26 weeks and 1 day of gestation. F, femur; FA, femoral artery; FV, femoral vein; RFM, rectus femoris muscle; SM, sartorius muscle; VIM, vastus intermedius muscle; VLM, vastus lateralis muscle; VMM, vastus medialis muscle

Fig. 12: Fetal leg microvessels depicted with SMI Gen4 at 13 weeks and 4 days of gestation. FA, femoral artery; K, knee; PA, popliteal artery; UA, umbilical artery

Fig. 13: Fetal foot microvessels depicted with SMI Gen4 at 26 weeks and 1 day of gestation. AA, arcuate artery; LTA, lateral tarsal artery

Fig. 14: Digital arteries (arrows) of toes depicted with SMI Gen4 at 35 weeks and 6 days of gestation. FirT, first toe; ST, second toe; TT, third toe; FoT, fourth toe; FifT, fifth toe

DISCUSSION

Conventional SMI or SlowflowHD demonstrated fetal intracranial vessels in detail.1-3,5,12 However, the image quality of brain vascularity before 20 weeks of gestation was poor because of its small target.1,2 In this investigation, SMI Gen4 clearly demonstrated fetal intracranial small vessels, such as lenticulostriate arteries using a transabdominal probe early in the second trimester of pregnancy. Moreover, this modality revealed fetal extracranial microvessels, namely the superficial temporal artery and its branches, the anterior auricular arteries, at 26 weeks of gestation. To the best of our knowledge, this is the first report of the depiction of fetal superficial temporal and anterior auricular arteries in utero. SMI Gen4 may become a breakthrough modality to herald new scientific fields, such as “fetal angiology” and “fetal microangiology.”

With respect to fetal intra-abdominal organ microvasculature, conventional SMI or SlowflowHD showed characteristic features of each organ.4,13 However, the microbranches of each organ could not be clearly depicted. In this study, SMI Gen4 revealed microbranches in each organ, especially the adrenal microvasculature, compared with conventional SMI and SlowflowHD. In FGR, the increased blood flow of the adrenal gland was reported.14 SMI Gen4 may be a novel diagnostic modality for antenatal detection of FGR and understanding the severity of FGR in clinical practice.

With respect to the microvessels of fetal extremities in previous studies, only SlowflowHD showed main arm and leg vessels such as brachial, femoral, popliteal, and tibial arteries.5,12 However, these studies were conducted after around 20 weeks of gestation. In the present investigation, SMI Gen4 clearly showed fetal knee microvascularity at 13 weeks and 4 days of gestation. Moreover, this modality demonstrated thigh and foot microvascularity, and digital arteries of the fingers and toes. To the best of our knowledge, this is also the first study to depict the fetal thigh microvasculature and digital arteries of the fingers and toes. Decreased femoral artery blood flow in fetal acidosis and an increased femoral artery pulsatility index in fetal hypoxemia were noted in fetal sheep experiments.15,16 These results suggest that SMI Gen4 may be a unique diagnostic modality to assess the vascularity and microvascularity of the extremities in fetal FGR in future research projects.

The advantages of SMI Gen4 were ultralow flow imaging, ultrahigh-resolution, and free-breathing capability with better penetration, better uniformity, and a higher frame rate. The main limitations of this technique were still motion artifacts and noise of fetal movements. Future technical advances in SMI Gen4 may resolve these limitations.

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