Startseite The value of ultrasound spectra of middle cerebral artery and umbilical artery blood flow in adverse pregnancy outcomes
Artikel Open Access

The value of ultrasound spectra of middle cerebral artery and umbilical artery blood flow in adverse pregnancy outcomes

  • Xuan Zhao und Ya Shen EMAIL logo
Veröffentlicht/Copyright: 25. November 2024
Artikel downloaden (PDF)
Journal of Perinatal Medicine
Aus der Zeitschrift Journal of Perinatal Medicine Band 53 Heft 2

Abstract

Objectives

To evaluate the diagnostic value of ultrasound spectra of the middle cerebral artery (MCA) and umbilical artery (UA) blood flow in predicting adverse pregnancy outcomes.

Methods

Data from 202 late singleton pregnancies (32–34 weeks gestation) were analyzed. Group A included 155 normal pregnancies, while Group B comprised 47 high-risk pregnancies. Color Doppler ultrasonography was used to measure and compare pulsatility index (PI), resistance index (RI), and end-systolic peak/end-diastolic peak (S/D) ratios of fetal MCA and UA between the groups.

Results

UA-related parameters (PI, RI, and S/D) were significantly higher in Group B compared to Group A, whereas MCA-related parameters (PI, RI, and S/D) were significantly lower in Group B than in Group A. In pregnancies with adverse outcomes, fetal UtA and UA-related parameters were elevated, while MCA parameters were decreased compared to those with favorable outcomes.

Conclusions

Ultrasound spectra of MCA and UA blood flow provide valuable clinical information for assessing fetal intrauterine growth and predicting adverse pregnancy outcomes.

Keywords: ultrasonic spectrum of blood flow; middle cerebral artery; pregnancy outcomes; high-risk pregnancy; late pregnancy; umbilical artery blood flow

Introduction

High-risk pregnancies can lead to adverse maternal and infant outcomes such as postpartum hemorrhage, fetal growth restriction, intrauterine distress, and neonatal asphyxia, and are significant contributors to fetal and maternal mortality. Conditions such as oligohydramnios, placental abruption, premature placental maturation, and pregnancy-related complications can induce high-risk pregnancies [1], 2]. In recent years, the incidence of high-risk pregnancies in China has been steadily increasing, presenting a considerable challenge to clinical obstetrics. Therefore, early prediction, prevention, and intervention in high-risk pregnancies are crucial for improving adverse pregnancy outcomes.

Currently, fetal heart monitoring is a key for assessing the intrauterine condition of the fetus, with the fetal heart rate serving as a gauge to determine the normalcy of fetal development within the uterus [3], 4]. However, in cases of mild fetal hypoxia, fetal heart monitoring may remain relatively normal, potentially leading to clinical misdiagnosis. Ultrasound examination is the most widely used imaging method in obstetrics, offering advantages such as safety, non-invasiveness, speed, sensitivity, and excellent repeatability. Compared to routine two-dimensional ultrasound, color Doppler flow imaging (CDFI) can assess fetal growth, determine fetal position, placental location, amniotic fluid volume, and placental maturity, and also quantitatively measure and reflect blood flow distribution and passage in vessels by combining blood flow distribution and spectral Doppler analysis. This comprehensive evaluation of the intrauterine condition of the fetus is primarily achieved through three indicators: resistance index (RI), pulsatility index (PI), and the end-systolic peak/end-diastolic peak (S/D) ratio [5]. This study aims to evaluate the application value of ultrasound spectra of middle cerebral artery (MCA) and umbilical artery (UA) blood flow in predicting adverse pregnancy outcomes.

Materials and methods

Baseline data

A retrospective analysis was conducted on valid data from 202 late singleton pregnancies (32–34 weeks gestation) in women who underwent prenatal examinations and delivered at our hospital between April 2020 and April 2024. Of these, 155 cases of normal pregnancies and 47 cases of high-risk pregnancies were categorized as Group A and B, respectively. All 202 women were followed-up until the end of their pregnancies. This study was approved by the Ethics Committee of the Children’s Hospital (Wuhan Maternal and Child Healthcare Hospital), Tongji Medical College, Huazhong University of Science & Technology. Written informed consent was obtained from all participants prior to their inclusion in the study.

Inclusion and exclusion criteria

Inclusion criteria

Pregnant women meeting the following inclusion criteria were included in the study: (1) Individuals in Group B who fulfilled the diagnostic criteria for high-risk pregnancy [6], women <18 years old or ≥35 years old, pregnancies complicated by conditions including heart disease, diabetes, hypertension, placental issues (e.g., placenta previa, placental abruption), nutritional factors, medication factors, or a history of adverse pregnancy outcomes; meeting one or more of these conditions qualified as a high-risk pregnancy; (2) patients who underwent prenatal examination and delivery at our hospital with complete clinical data available; (3) women with singleton pregnancies in late gestation (32–34 weeks); (4) no history of special medication during pregnancy; (5) normal umbilical cord and placenta, with no congenital fetal malformations; (6) women with normal communication abilities who were able to cooperate during ultrasound examinations.

Exclusion criteria

Pregnant women were excluded from the study if they had: (1) genital diseases or malformations; (2) acute infections; (3) history of pelvic or lower abdominal surgeries; (4) severe organ dysfunction or hematological disorders; (5) unclear imaging results; (6) fetuses with congenital heart disease, hydrocephalus, or other significant abnormalities.

Instrument and method

MCA

Changes in the blood flow of the MCA can reflect fetal neurodevelopmental state and cerebral perfusion. Relevant studies have demonstrated a close association between these changes and adverse fetal outcomes, such as fetal growth restriction.

UA

The ultrasound spectrum of UA blood flow reflects the functional status of the placenta and serves as a crucial indicator for assessing fetal oxygenation and nutrient supply. Abnormal UA blood flow patterns are often indicative of underlying pregnancy complications, such as fetal distress. This study explored the predictive value of these two indicators for adverse pregnancy outcomes through quantitative analysis. The instrument used was a GE Voluson E10 ultrasound diagnostic device with a probe (C1-5) frequency of 1.0–5.0 MHz. Pregnant women were positioned in a lateral or supine position, exposing the abdomen for routine two-dimensional ultrasound examination. These measurements included fetal head circumference, biparietal diameter, and observations of amniotic fluid and fetal heart conditions. The examination mode was then switched to CDFI mode, and parameters related to UtA-, UA- and MCA-related blood flow parameters were recorded.

  1. UtA measurements: Two-dimensional ultrasonography was employed to visualize the UtA at the junction of the corpus and cervix. CDFI was utilized to depict UtA blood flow signals. The sampling point was placed approximately 1–2 cm from the internal iliac artery, with a sampling volume of 2 mm. The ultrasound beam was adjusted to an angle of 0°–30° relative to the direction of blood flow. Once five or more clear and stable characteristic spectra were obtained, the image was frozen, and UtA blood flow parameters, including RI, PI, and S/D ratio were automatically measured. Each measurement was performed three times, and the average value was recorded.

  2. UA measurements: The connection point between the placental umbilical cord and the fetal abdominal umbilical cord entrance was located, the free umbilical cord was identified. The probe angle and position were adjusted, and sampling from the arterial spectrum with blood flow filling was selected. The sampling line was taken parallel to the direction of blood flow, and related parameters were measured, including end-systolic flow velocity (PSV), end-diastolic flow velocity (EDV), PI, RI, and S\D. Five consecutive stable waveforms were recorded. (3) MCA measurements: Cross-sectional images of the fetal brain were obtained to expose the brain and the cerebral arterial circle. Color blood flow perpendicular to the midline of the brain was observed. Sampling was taken at the proximal end, with the sampling line oriented as parallel as possible to the direction of blood flow (angle < 30°). Measurements of various blood flow parameters were recorded, with five consecutive stable waveforms were collected. If measurement errors occurred due to fetal position or movement, the measurements were repeated after a period of rest.

Criteria for adverse pregnancy outcomes

All pregnant women were followed-up until the end of their pregnancies. Neonatal asphyxia, preterm birth, or other adverse maternal or infant conditions were classified as adverse outcomes.

Results

Baseline data

No significant differences were observed between the groups in terms of age, proportion of primiparas, gestational weeks, and other relevant variables, indicating that the two groups were comparable (p>0.05) (Table 1).

Table 1:

Comparison of baseline data.

Group Number of cases Average age, years Proportion of primipara/pluripara Gestational weeks, weeks
Group A 155 30.8 ± 3.9 69/86 34.13 ± 2.32
Group B 47 31.7 ± 4.2 21/26 33.57 ± 2.21
t/χ2 1.361 2.418 1.465
p 0.175 0.120 0.144

UtA blood flow parameters

UtA-related parameters, including PI, RI, and S/D ratio, were significantly higher in Group B compared to Group A, with a statistically significant difference (p<0.05). This finding indicates that blood flow parameters in high-risk pregnancies are elevated, suggesting reduced blood flow and an increased resistance index in UtA (Figure 1).

Figure 1: Comparison of UtA blood flow parameters between the two groups. Figure 1 shows that the parameters of UtA blood flow [(A) PI, (B) RI, and (C) S/D] are significantly increased in women with high-risk pregnancies, indicating elevated blood flow resistance index. Compared with the control group, ***p<0.001.
Figure 1:

Comparison of UtA blood flow parameters between the two groups. Figure 1 shows that the parameters of UtA blood flow [(A) PI, (B) RI, and (C) S/D] are significantly increased in women with high-risk pregnancies, indicating elevated blood flow resistance index. Compared with the control group, ***p<0.001.

UA blood flow parameters

UA-related parameters (PI, RI, and S/D ratio) were significantly higher in Group B compared to Group A, with a statistically significant difference (p<0.05). This suggests that blood flow resistance in the UA is elevated in high-risk pregnancies, reflecting abnormal placental terminal circulation (Figure 2).

Figure 2: Comparison of UA blood flow parameters between the two groups. (A–C) shows that the parameters of UA blood flow [(A) PI, (B) RI, and (C) S/D] are significantly increased in women with high-risk pregnancies, indicating elevated blood flow resistance index. (D and E) shows UA images of two groups: the fetal middle cerebral artery Doppler spectrum [control group (maximum velocity: 43.57 cm/s, S/D: 2.85, PI: 1.13, RI: 0.65); high-risk pregnancy group (maximum velocity: 41.41 cm/s, S/D: 2.51, PI: 0.95, RI: 0.60)]. Compared with the control group, ***p<0.001.
Figure 2:

Comparison of UA blood flow parameters between the two groups. (A–C) shows that the parameters of UA blood flow [(A) PI, (B) RI, and (C) S/D] are significantly increased in women with high-risk pregnancies, indicating elevated blood flow resistance index. (D and E) shows UA images of two groups: the fetal middle cerebral artery Doppler spectrum [control group (maximum velocity: 43.57 cm/s, S/D: 2.85, PI: 1.13, RI: 0.65); high-risk pregnancy group (maximum velocity: 41.41 cm/s, S/D: 2.51, PI: 0.95, RI: 0.60)]. Compared with the control group, ***p<0.001.

MCA blood flow parameters

In contrast, MCA-related parameters (PI, RI, and S/D ratio) in Group B were significantly lower than those in Group A, showing a statistically significant difference (p<0.05). This suggests that the various blood flow parameters of MCA in high-risk pregnant women are lower than those in normal pregnant women, and the dilated and thickened vascular diameter of MCA with decreased resistance initiates cerebral protective effects (Figure 3).

Figure 3: Comparison of MCA blood flow parameters between the two groups. (A–C) shows that the parameters of MCA blood flow [(A) PI, (B) RI, and (C) S/D] in women with high-risk pregnancies are significantly reduced, indicating decreased MCA vascular resistance and the initiation of cerebral protective effects. (D and E) shows MCA images of the two groups: the fetal umbilical artery Doppler spectrum [control group (S/D: 2.41, PI: 0.92, RI: 0.59); high-risk pregnancy group: S/D: 2.85, PI: 1.09, RI: 0.65]. Compared with the control group, ***p<0.001.
Figure 3:

Comparison of MCA blood flow parameters between the two groups. (A–C) shows that the parameters of MCA blood flow [(A) PI, (B) RI, and (C) S/D] in women with high-risk pregnancies are significantly reduced, indicating decreased MCA vascular resistance and the initiation of cerebral protective effects. (D and E) shows MCA images of the two groups: the fetal umbilical artery Doppler spectrum [control group (S/D: 2.41, PI: 0.92, RI: 0.59); high-risk pregnancy group: S/D: 2.85, PI: 1.09, RI: 0.65]. Compared with the control group, ***p<0.001.

Pregnancy outcomes

The rate of adverse pregnancy outcomes in Group B was significantly higher than in Group A, with a statistically significant difference (p<0.05) (Table 2).

Table 2:

Comparison of pregnancy outcomes between the two groups of patients.

Group Number of cases Preterm birth Fetal growth restriction Intrauterine distress Neonatal asphyxia
Group A 155 3 (1.94) 4 (2.58) 5 (3.23) 0 (0)
Group B 47 9 (19.15) 3 (6.38) 6 (12.77) 4 (8.51)
χ2 16.168a 0.629a 4.657a –b
p <0.001 0.428 0.031 0.003

  1. aContinuity correction test. bFisher’s exact probability method.

Comparison of blood flow parameters of different pregnancy outcomes in high-risk pregnancy group

In Group B, pregnant women with adverse outcomes exhibited higher UtA and UA blood flow parameters (PI, RI, and S/D values) and lower MCA parameters (PI, RI, and S/D values) compared to those with favorable pregnancy outcomes. These differences were statistically significant (p<0.05) (Table 3).

Table 3:

Comparison of blood flow parameters of different pregnancy outcomes in high-risk pregnancy group.

Group Ultrasonic blood flow parameter Normal outcome of high-risk pregnancy Abnormal outcome of high-risk pregnancy t p-Value
UtA PI 0.96 ± 0.11 1.17 ± 0.17 4.950 <0.001
RI 0.64 ± 0.10 0.71 ± 0.13 2.047 0.047
S/D 2.36 ± 0.35 2.74 ± 0.29 4.070 <0.001
UA PI 0.61 ± 0.08 0.92 ± 0.13 9.681 <0.001
RI 0.83 ± 0.11 1.12 ± 0.22 5.593 <0.001
S/D 2.51 ± 0.20 2.71 ± 0.33 2.479 0.017
MCA PI 0.67 ± 0.08 0.57 ± 0.07 4.571 <0.001
RI 1.24 ± 0.14 1.06 ± 0.11 4.930 <0.001
S/D 3.95 ± 0.57 3.11 ± 0.49 5.434 <0.001

  1. UtA, uterine artery; UA, umbilical artery; MCA, middle cerebral artery; PI, pulsatility index; RI, resistance index; S/D, end-systolic peak/end-diastolic peak.

Diagnostic efficacy of various blood flow parameters

ROC curve analysis demonstrated that the blood flow parameters of the fetal UtA, UA, and MCA had good diagnostic efficacy for predicting adverse pregnancy outcomes in high-risk pregnancies, with AUC values exceeding 0.7. Among them, the RI of UtA, the S/D ratio of UA, and the S/D ratio of MCA had the highest diagnostic value (Figure 4).

Figure 4: Diagnostic efficacies of fetal UtA, UA, and MCA ultrasound flow parameters for adverse pregnancy outcomes. Figure 4 shows that the ultrasonic blood flow parameters of the fetal (A) UtA, (B) UA, and (C) MCA all demonstrated good diagnostic efficacy for adverse pregnancy outcomes in high-risk pregnancies, with AUC values all >0.7.
Figure 4:

Diagnostic efficacies of fetal UtA, UA, and MCA ultrasound flow parameters for adverse pregnancy outcomes. Figure 4 shows that the ultrasonic blood flow parameters of the fetal (A) UtA, (B) UA, and (C) MCA all demonstrated good diagnostic efficacy for adverse pregnancy outcomes in high-risk pregnancies, with AUC values all >0.7.

Discussion

Previous research [7], 8] indicates that adverse maternal and neonatal outcomes, such as postpartum hemorrhage, fetal growth restriction, intrauterine distress, and neonatal asphyxia, are significantly more prevalent in high-risk pregnancies than in normal ones. This study found that the incidence of adverse pregnancy outcomes in Group B was significantly higher than in Group A. It indicates that high-risk pregnancies pose substantial harm to maternal and infant health. Therefore, a thorough and proactive assessment of the intrauterine conditions of fetuses in high-risk pregnancies is of great significance for preventing adverse pregnancy outcomes. In this study, ultrasound spectra of the MCA and UA blood flow were assessed to effectively predict adverse pregnancy outcomes and assess fetal intrauterine conditions.

The UA is commonly used in clinical practice to observe fetal hemodynamic changes, as it accurately reflects fetal-placental circulation status [9], 10]. As gestational age advances, the maturation of the placenta and tertiary villi leads to increased placental volume and blood flow, which correspondingly decreases blood flow parameters (RI, PI, and S/D values) [11], [12], [13]. The results of this study indicated that various parameters of UA (PI, RI, and S/D values) were significantly higher in Group B members compared to Group A. This suggests that high-risk pregnant women exhibit elevated UA blood flow parameters, indicating increased blood flow resistance and abnormal placental terminal circulation. During high-risk pregnancies, factors such as pregnancy-induced hypertension and gestational diabetes cause spasms and edema in the placental capillaries, leading to arterial lumen narrowing, reduced overall arterial cross-sectional area, increased blood circulation resistance, and elevated fetal UA blood flow parameters. Therefore, monitoring variations in fetal UA blood flow parameters (RI, PI, and S/D values) can provide insights into placental blood supply and circulatory function, aiding in the prediction of adverse pregnancy outcomes and the assessment of fetal intrauterine conditions.

Although the predictive accuracy of the cerebroplacental ratio (CPR) and umbilicocerebral ratio (UCR) for late-stage fetal growth restriction (FGR) remains controversial in related studies, they continue to exhibit an association with adverse perinatal outcomes. Some studies suggest that, despite the lower AUC values, CPR and UCR can serve as auxiliary tools in assessing fetal intrauterine conditions under specific circumstances [14], 15]. In our research, parameter monitoring of UA and MCA provided more direct predictive evidence.

Approximately 80 % of the cerebral hemispheric blood supply is provided by the MCA, which is situated in cerebral vessels that can be readily monitored via ultrasound. Changes in MCA blood flow parameters reflect cerebral circulation and fetal hypoxia [16], [17], [18], [19]. As the gestational weeks progress, the fetus continues to grow and develop, resulting in an increase in cerebral vascular diameter, thereby reducing blood flow resistance and consequently increasing blood flow. However, when the placenta is hypoxic, peripheral vascular resistance increases, reducing blood flow, while cerebral arterial lumen resistance decreases, enhancing blood flow and velocity, thus exerting a “cerebral protective effect” [20], [21], [22]. This study found that the MCA-related parameters (PI, RI, and S/D) in Group B were significantly lower than those in Group A. This suggests that the various blood flow parameters of MCA in high-risk pregnant women are lower than those in normal pregnant women, and the dilated and thickened vascular diameter of MCA with decreased resistance initiates such cerebral protective effects.

Although the literature indicates a correlation between changes in MCA parameters and adverse perinatal outcomes, the early intervention effectiveness of CPR and UCR in high-risk pregnancies remains limited. Our research highlights the importance of monitoring UA and MCA blood flow parameters, which provide substantial value in assessing fetal conditions and managing complications in high-risk pregnancies [23]. In this study, we found that adverse pregnancy outcomes were associated with higher fetal UtA- and UA-related parameters (PI, RI, and S/D values) and lower MAC parameters (PI, RI, and S/D values), and ultrasonic blood flow parameters of the fetal UtA, UA. MCA parameters demonstrated good diagnostic efficacy for adverse pregnancy outcomes in high-risk pregnancies, with the AUC values exceeding 0.7. Specifically, the RI of UtA, the S/D ratio of UA, and the S/D ratio of MCA had the highest diagnostic value, underscoring the utility of UA and MCA as valuable indicators for assessing fetal intrauterine conditions and predicting adverse pregnancy outcomes.

In a study by Buca et al. [24], it was found that cerebroplacental and maternal Doppler assessments showed no significant correlation with adverse pregnancy outcomes in term-appropriate fetuses nearing full-term, nor could they effectively predict such outcomes. This finding differs somewhat from the results of our study, which indicated that the ultrasound spectrum of MCA and UA blood flow holds potential predictive value. The disparity may stem from differences in sample selection, research methods, or the timing of observations. First, the research by Buca et al. [24] primarily focuses on near-term appropriate-for-gestational-age fetuses, whereas our study emphasized early-stage blood flow analysis, which may be more sensitive in assessing fetal health. Second, methodological differences might also account for the varying results, particularly in terms of the technical specifics of data collection and analysis. Last, individual patient differences, including pregnancy-related complications and maternal health conditions, may influence the clinical significance of these ultrasound parameters. Therefore, further research will help elucidate the predictive capabilities of these blood flow ultrasound markers at different gestational stages and in specific populations. As a result, we recommend future research to make improvements in regards the following aspects: First, the sample size should be expanded to enhance statistical power and the applicability of the results; second, a longitudinal study design should be adopted to track the relationship between ultrasound findings and pregnancy outcomes at different gestational stages in the same group of women. Additionally, incorporating more potential confounding variables for multifactorial analysis will allow for a comprehensive assessment of their impact on ultrasound results and pregnancy outcomes. Last, the relationship between ultrasound findings and fetal physiological mechanisms should be explored, and a multicenter collaborative study should be conducted, thereby enhancing the external validity of the results.

In conclusion, the ultrasound spectra of MCA and UA blood flow hold significant clinical value in assessing fetal intrauterine growth and predicting adverse pregnancy outcomes.

Corresponding author: Ya Shen, Gynecologic, Children’s Hospital (Wuhan Maternal and Child Healthcare Hospital), Tongji Medical College, Huazhong University of Science & Technology, Wuhan Children’s Hospital, No. 100 Hong Kong Road, Jiangan District, Wuhan 430000, Hubei, China, E-mail:

Funding source: Knowledge Innovation Special Basic Research Project in 2022 Year

Award Identifier / Grant number: 2022020801010566

  1. Research ethics: This study has been approved by the Ethics Committee of Children’s Hospital (Wuhan Maternal and Child Healthcare Hospital), Tongji Medical College, Huazhong University of Science & Technology.

  2. Informed consent: All study participants provided written informed consent before participating in the study.

  3. Author contributions: Xuan Zhao and Ya Shen designed the study, performed the research, analyzed the data and wrote the paper. The authors have accepted responsibility for the entire content of this manuscript and approved its submission.

  4. Use of Large Language Models, AI and Machine Learning Tools: None declared.

  5. Conflict of interests: The authors state no conflict of interest.

  6. Research funding: This work was supported by the Knowledge Innovation Special Basic Research Project in 2022 Year [2022020801010566].

  7. Data availability: All data generated or used during the study appear in the submitted article.

References

1. Agrawal, M, Poulsen, G, Colombel, JF, Allin, KH, Jess, T. Maternal antibiotic exposure during pregnancy and risk of IBD in offspring: a population-based cohort study. Gut 2023;72:804–5. https://doi.org/10.1136/gutjnl-2022-327724.Suche in Google Scholar PubMed PubMed Central

2. Perkins, JD, Akhtar, N, Singh, R, Kamran, A, Ilyas, S. Partitioning risk factors for embolic stroke of undetermined source using exploratory factor analysis. Int J Stroke 2022;17:407–14. https://doi.org/10.1177/17474930211009847.Suche in Google Scholar PubMed PubMed Central

3. Meisgen, S, Hedlund, M, Ambrosi, A, Folkersen, L, Ottosson, V, Forsberg, D, et al.. Auxilin is a novel susceptibility gene for congenital heart block which directly impacts fetal heart function. Ann Rheum Dis 2022;81:1151–61. https://doi.org/10.1136/annrheumdis-2021-221714.Suche in Google Scholar PubMed PubMed Central

4. Evans, MI, Britt, DW, Evans, SM, Devoe, LD. Evolving frameworks for the foundation and practice of electronic fetal monitoring. Maternal-Fetal Med 2022;4:141–51. https://doi.org/10.1097/fm9.0000000000000148.Suche in Google Scholar

5. Inal, B, Ateser, G, Orhan, B, Topkaya, C, Polat, S. Angiogenesis factors and uterine artery Doppler ultrasound resistance index and pulsatility index in pregnancies with high-risk of preeclampsia. J Clin Case Rep 2017;7:2. https://doi.org/10.4172/2165-7920.10001038.Suche in Google Scholar

6. Xie, X, Kong, BH, Duan, T. Obstetricsand Gynecology. Beijing: People’s Health Publishing House; 2018:375–6 pp.Suche in Google Scholar

7. Afifi, HH, Gaber, KR, Thomas, MM, Taher, MB, Tosson, AM. Genetic implications in high-risk pregnancy and its outcome: a 2-year study. Am J Perinatol 2022;39:1659–67. https://doi.org/10.1055/s-0041-1724002.Suche in Google Scholar PubMed

8. Bai, S, Du, S, Liu, H, Lin, S, Zhao, X, Wang, Z, et al.. The causal and independent effect of ozone exposure during pregnancy on the risk of preterm birth: evidence from northern China. Environ Res 2022;214:113879. https://doi.org/10.1016/j.envres.2022.113879.Suche in Google Scholar PubMed

9. Ozturk, FU, Tezcan, S, Soy, EHA, Uslu, N, Haberal, M. Doppler ultrasonography blood flow changes of the hepatic artery in liver transplants complicated with cholangitis. J Clin Ultrasound 2023;51:860–5. https://doi.org/10.1002/jcu.23466.Suche in Google Scholar PubMed

10. Botting-Lawford, K, Horler, R, White, A, Mizani, S, Crombie, G, Dehbi, H-M, et al.. Maternal nutrient restriction in Guinea pigs increases resistance in the umbilical artery at mid-gestation. Placenta 2023;140:e46. https://doi.org/10.1016/j.placenta.2023.07.156.Suche in Google Scholar

11. Kim, EH, Park, JB, Kang, P, Ji, SH, Jang, YE, Lee, JH, et al.. Response of internal carotid artery blood flow velocity to fluid challenge under general anesthesia in pediatric patients with moyamoya disease: a prospective observational study. Paediatr Anaesth 2022;32:1330–8. https://doi.org/10.1111/pan.14558.Suche in Google Scholar PubMed

12. Wu, S, Liao, G, Yang, J. Effects of right lateral position on changes of fetal hemodynamics in late pregnancy. J Ultrasound Med 2023;42:2341–7. https://doi.org/10.1002/jum.16261.Suche in Google Scholar PubMed

13. Le, TM, Vu, NB, Nguyen, PT, Huynh, PD, Van Pham, P. Safety and efficacy of injection of exosomes derived from human umbilical cord mesenchymal stem cells in the treatment of limb ischemia: an in-vivo evaluation in mice. Minerva Biotechnol Biomol 2022;34. https://doi.org/10.23736/s2724-542x.22.02936-4.Suche in Google Scholar

14. Villalain, C, Galindo, A, Di Mascio, D, Buca, D, Morales-Rosello, J, Loscalzo, G, et al.. Diagnostic performance of cerebroplacental and umbilicocerebral ratio in appropriate for gestational age and late growth restricted fetuses attempting vaginal delivery: a multicenter, retrospective study. J Matern Fetal Neonatal Med 2022;35:6853–9. https://doi.org/10.1080/14767058.2021.1926977.Suche in Google Scholar PubMed

15. Di Mascio, D, Herraiz, I, Villalain, C, Buca, D, Morales-Rosello, J, Loscalzo, G, et al.. Comparison between cerebroplacental ratio and umbilicocerebral ratio in predicting adverse perinatal outcome in pregnancies complicated by late fetal growth restriction: a multicenter, retrospective study. Fetal Diagn Ther 2021;48:448–56. https://doi.org/10.1159/000516443.Suche in Google Scholar PubMed

16. Lobo, G, Nowak, P, Panigassi, A, Boute, T, Caetano, A, Moron, A, et al.. P13. 01: middle cerebral artery peak systolic velocity changes after intra‐uterine transfusion in a hydropic fetus. Ultrasound Obstet Gynecol 2011;38:213. https://doi.org/10.1002/uog.9777.Suche in Google Scholar

17. Cui, X-J, Zhu, J-F. Predicting obstetric outcomes of advanced maternal age through determination of hemodynamics of uterine artery, umbilical artery and fetal cerebral middle artery. J Hainan Med Univ 2017;23:121–5.Suche in Google Scholar

18. Barati, M, Masihi, S, Barahimi, E, Khorrami, MA. Relationship between placental calcification and estimated fetal weight percentile at 30-34 weeks of pregnancy. Int J Women’s Health Reproduct Sci 2019;7:478–82. https://doi.org/10.15296/ijwhr.2019.79.Suche in Google Scholar

19. Fu, M. The value of Doppler ultrasonography in evaluating the hemodynamics of the middle cerebral artery in the umbilical cord around the neck of the fetus to predict the outcome of pregnancy. Chin J Clin Ration Drug Use 2018;11:21–22.Suche in Google Scholar

20. Hassidov, D, Asher, UA, Ben-Ami, M, Keselman, L, Sabri, R, Haddad, S. The effect of maternal mathematical activities on the fetal brain. Open J Obstet Gynecol 2018;8:826–35. https://doi.org/10.4236/ojog.2018.810086.Suche in Google Scholar

21. Zarrinkalam, E, Arabi, SM, Komaki, A, Ranjbar, K. The preconditioning effect of different exercise training modes on middle cerebral artery occlusion induced-behavioral deficit in senescent rats. Heliyon 2023;9. https://doi.org/10.1016/j.heliyon.2023.e17992.Suche in Google Scholar PubMed PubMed Central

22. Kubota, H, Tsutsui, M, Kuniyoshi, K, Yamashita, H, Shimokawa, H, Sugahara, K, et al.. Alleviated cerebral infarction in male mice lacking all nitric oxide synthase isoforms after middle cerebral artery occlusion. J Anesth 2024;38:44–56. https://doi.org/10.1007/s00540-023-03271-8.Suche in Google Scholar PubMed

23. Di Mascio, D, Rizzo, G, Buca, D, D’Amico, A, Leombroni, M, Tinari, S, et al.. Comparison between cerebroplacental ratio and umbilicocerebral ratio in predicting adverse perinatal outcome at term. Eur J Obstet Gynecol Reprod Biol 2020;252:439–43. https://doi.org/10.1016/j.ejogrb.2020.07.032.Suche in Google Scholar PubMed

24. Buca, D, Rizzo, G, Gustapane, S, Mappa, I, Leombroni, M, Bascietto, F, et al.. Diagnostic accuracy of Doppler ultrasound in predicting perinatal outcome in appropriate for gestational age fetuses: a prospective study. Ultraschall der Med 2021;42:404–10. https://doi.org/10.1055/a-1072-5161.Suche in Google Scholar PubMed

Received: 2024-07-18
Accepted: 2024-10-24
Published Online: 2024-11-25
Published in Print: 2025-02-25

© 2025 the author(s), published by De Gruyter, Berlin/Boston

This work is licensed under the Creative Commons Attribution 4.0 International License.

Artikel in diesem Heft

  1. Frontmatter
  2. Review
  3. Sex differences in lung function of adolescents or young adults born prematurely or of very low birth weight: a systematic review
  4. Original Articles – Obstetrics
  5. Shifts in peak month of births and socio-economic factors: a study of divided and reunified Germany 1950–2022
  6. The predictive role of serial transperineal sonography during the first stage of labor for cesarean section
  7. Gestational weight gain and obstetric outcomes in women with obesity in an inner-city population
  8. Placental growth factor as a predictive marker of preeclampsia in twin pregnancy
  9. Learning curve for the perinatal outcomes of radiofrequency ablation for selective fetal reduction: a single-center, 10-year experience from 2013 to 2023
  10. External validation of a non-invasive vaginal tool to assess the risk of intra-amniotic inflammation in pregnant women with preterm labor and intact membranes
  11. Placental fetal vascular malperfusion in maternal diabetes mellitus
  12. The importance of the cerebro-placental ratio at term for predicting adverse perinatal outcomes in appropriate for gestational age fetuses
  13. Comparing achievability and reproducibility of pulsed wave Doppler and tissue Doppler myocardial performance index and spatiotemporal image correlation annular plane systolic excursion in the cardiac function assessment of normal pregnancies
  14. Characteristics of the pregnancy and labour course in women who underwent COVID-19 during pregnancy
  15. Original Articles – Fetus
  16. Sonographic visualization and measurement of the fetal optic chiasm and optic tract and association with the cavum septum pellucidum
  17. The association among fetal head position, fetal head rotation and descent during the progress of labor: a clinical study of an ultrasound-based longitudinal cohort study in nulliparous women
  18. Fetal hypoplastic left heart syndrome: key factors shaping prognosis
  19. The value of ultrasound spectra of middle cerebral artery and umbilical artery blood flow in adverse pregnancy outcomes
  20. Original Articles – Neonates
  21. A family-centric, comprehensive nurse-led home oxygen programme for neonatal chronic lung disease: home oxygen policy evaluation (HOPE) study
  22. Effects of a respiratory function indicator light on visual attention and ventilation quality during neonatal resuscitation: a randomised controlled crossover simulation trial
  23. Short Communication
  24. Incidence and awareness of dysphoric milk ejection reflex (DMER)
https://doi.org/10.1515/jpm-2024-0323
Schlagwörter für diesen Artikel
ultrasonic spectrum of blood flow; middle cerebral artery; pregnancy outcomes; high-risk pregnancy; late pregnancy; umbilical artery blood flow
Creative Commons
BY 4.0

Artikel in diesem Heft

  1. Frontmatter
  2. Review
  3. Sex differences in lung function of adolescents or young adults born prematurely or of very low birth weight: a systematic review
  4. Original Articles – Obstetrics
  5. Shifts in peak month of births and socio-economic factors: a study of divided and reunified Germany 1950–2022
  6. The predictive role of serial transperineal sonography during the first stage of labor for cesarean section
  7. Gestational weight gain and obstetric outcomes in women with obesity in an inner-city population
  8. Placental growth factor as a predictive marker of preeclampsia in twin pregnancy
  9. Learning curve for the perinatal outcomes of radiofrequency ablation for selective fetal reduction: a single-center, 10-year experience from 2013 to 2023
  10. External validation of a non-invasive vaginal tool to assess the risk of intra-amniotic inflammation in pregnant women with preterm labor and intact membranes
  11. Placental fetal vascular malperfusion in maternal diabetes mellitus
  12. The importance of the cerebro-placental ratio at term for predicting adverse perinatal outcomes in appropriate for gestational age fetuses
  13. Comparing achievability and reproducibility of pulsed wave Doppler and tissue Doppler myocardial performance index and spatiotemporal image correlation annular plane systolic excursion in the cardiac function assessment of normal pregnancies
  14. Characteristics of the pregnancy and labour course in women who underwent COVID-19 during pregnancy
  15. Original Articles – Fetus
  16. Sonographic visualization and measurement of the fetal optic chiasm and optic tract and association with the cavum septum pellucidum
  17. The association among fetal head position, fetal head rotation and descent during the progress of labor: a clinical study of an ultrasound-based longitudinal cohort study in nulliparous women
  18. Fetal hypoplastic left heart syndrome: key factors shaping prognosis
  19. The value of ultrasound spectra of middle cerebral artery and umbilical artery blood flow in adverse pregnancy outcomes
  20. Original Articles – Neonates
  21. A family-centric, comprehensive nurse-led home oxygen programme for neonatal chronic lung disease: home oxygen policy evaluation (HOPE) study
  22. Effects of a respiratory function indicator light on visual attention and ventilation quality during neonatal resuscitation: a randomised controlled crossover simulation trial
  23. Short Communication
  24. Incidence and awareness of dysphoric milk ejection reflex (DMER)
Jetzt anmelden und 20% sparen
Institutioneller Zugang
Wie funktioniert Authentifizierung?
Haben Sie eine Idee, wie wir unsere Website verbessern können?
Bitte schreiben Sie uns.
© 2025 De Gruyter Brill
Heruntergeladen am 17.9.2025 von https://www.degruyterbrill.com/document/doi/10.1515/jpm-2024-0323/html
Button zum nach oben scrollen