Document Type : Original Article(s)
Authors
- Azam Faraji 1
- Fereshteh Gharibpour 1
- Niloofar Namazi 2, 3
- Ali Mohammad Shakiba 4
- Maryam Kasraeian 1
- Nasrin Asadi 1
- Homeira Vafaei 1
- Marjan Zare 5
- Khadijeh Bazrafshan 5
- Zahra Oveisi 2
1 Department of Obstetrics and Gynecology, School of Medicine, Maternal-fetal medicine Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
2 Department of Obstetrics and Gynecology, School of Medicine, Shiraz University of Medical Sciences, Shiraz, Iran
3 Infertility Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
4 Division of Pediatric Cardiology, Shiraz University of Medical Sciences, Shiraz, Iran
5 Maternal-fetal medicine Research Center, Shiraz University of Medical Sciences, Shiraz, Iran
Abstract
Background: Routine Doppler study is a common tool for early diagnosis of Fetal Growth Restriction (FGR) and Small for Gestational Age (SGA) patients. It aimed to determine the role of the Foramen Ovale Pulsatility Index (FOPI) study beside routine Doppler study among patients with FGR and
SGA fetuses.
Methods: This prospective study was conducted on 35 FGR, 32 SGA, and 33 Appropriate for Gestational Age (AGA) fetuses. Demographic data, amniotic fluid index, neonatal outcome, and Doppler velocimetry, including Umbilical Artery Pulsatility Index (UMAPI), Uterine Artery Pulsatility Index (UTAPI), Middle Cerebral Artery Pulsatility Index (MCAPI), Ductus Venosus Pulsatility Index (DVPI), and FOPI were documented. Kolmogorov-Smirnov normality test, one-way ANOVA, Mann-Whitney U, Kruskal-Wallis, non-parametric pairwise comparisons adjusted for Bonferroni correction, Pearson correlation test, Chi square, Fisher’s exact test, and Receiver Operating Characteristic Curve (ROC) analysis with Youden’s Index (sensitivity+specificity-1) to estimate cut-off point were used to analyze the data at significance level <0.05 for all tests.
Results: FOPI cut-off points were 2.24 (sensitivity=77%, specificity=94%) and 1.15 (sensitivity=90%, specificity=20%) to predict FGR and SGA, respectively. FOPI showed a positive correlation with UMAPI and UTAPI (r=0.52 and r=0.30, P<0.001 and P=0.006, respectively), but not with MCAPI and DVPI (r=0.08 and r=0.12, P=0.50 and P=0.30, respectively). Besides, UMAPI, UTAPI, and FOPI were altered among patients with stages I and II FGR. Umbilical cord potential hydrogen (umbilical cord pH), 1- and 5-min Apgar score significantly increased by Birth weight centile; however, UMAPI, FOPI, and UTAPI significantly decreased.
Conclusion: UMAPI is recommended to predict short-term neonatal morbidities and demonstrate the early or late onset FGR. Besides, FOPI is suggested as the first-line Doppler study to detect abnormal growth velocity. More studies are warranted, especially considering long-term neonatal morbidities.
Keywords
- Tesfa D, Tadege M, Digssie A, Abebaw S. Intrauterine growth restriction and its associated factors in South Gondar zone hospitals, Northwest Ethiopia, 2019. Arch Public Health. 2020;78:89. doi: 10.1186/s13690-020-00475-2. PubMed PMID: 33005403; PubMed Central PMCID: PMCPMC7526174.
- Atallah A, Butin M, Moret S, Claris O, Massoud M, Gaucherand P, et al. Standardized healthcare pathway in intrauterine growth restriction and minimum evidence-based care. J Gynecol Obstet Hum Reprod. 2021;50:101998. doi: 10.1016/j.jogoh.2020.101998. PubMed PMID: 33221557.
- Giouleka S, Tsakiridis I, Mamopoulos A, Kalogiannidis I, Athanasiadis A, Dagklis T. Fetal Growth Restriction: A Comprehensive Review of Major Guidelines. Obstet Gynecol Surv. 2023;78:690-708. doi: 10.1097/OGX.0000000000001203. PubMed PMID: 38134339.
- Schlembach D. Fetal Growth Restriction - Diagnostic Work-up, Management and Delivery. Geburtshilfe Frauenheilkd. 2020;80:1016-25. doi: 10.1055/a-1232-1418. PubMed PMID: 33012833; PubMed Central PMCID: PMCPMC7518933.
- Mustafa HJ, Javinani A, Muralidharan V, Khalil A. Diagnostic performance of 32 vs 36 weeks ultrasound in predicting late-onset fetal growth restriction and small-for-gestational-age neonates: a systematic review and meta-analysis. Am J Obstet Gynecol MFM. 2024;6:101246. doi: 10.1016/j.ajogmf.2023.101246. PubMed PMID: 38072237.
- Sadat Jamal A, Modarresi M. Renal artery Doppler in fetal sonography: A narrative review. Int J Reprod Biomed. 2023;21:789-800. doi: 10.18502/ijrm.v21i10.14534. PubMed PMID: 38077940; PubMed Central PMCID: PMCPMC10698356.
- Nader ARL, Zielinsky P, Naujorks AA, Nicoloso LHS, Piccoli Junior AL, Sulis NM, et al. Behaviour of the Foramen Ovale Flow in Fetuses with Intrauterine Growth Restriction. Obstet Gynecol Int. 2018;2018:1496903. doi: 10.1155/2018/1496903. PubMed PMID: 29581724; PubMed Central PMCID: PMCPMC5822859.
- Hadlock FP, Harrist RB, Carpenter RJ, Deter RL, Park SK. Sonographic estimation of fetal weight. The value of femur length in addition to head and abdomen measurements. Radiology. 1984;150:535-40. doi: 10.1148/radiology.150.2.6691115. PubMed PMID: 6691115.
- Hughes DS, Magann EF, Whittington JR, Wendel MP, Sandlin AT, Ounpraseuth ST. Accuracy of the Ultrasound Estimate of the Amniotic Fluid Volume (Amniotic Fluid Index and Single Deepest Pocket) to Identify Actual Low, Normal, and High Amniotic Fluid Volumes as Determined by Quantile Regression. J Ultrasound Med. 2020;39:373-8. doi: 10.1002/jum.15116. PubMed PMID: 31423632.
- Caradeux J, Eixarch E, Mazarico E, Basuki TR, Gratacos E, Figueras F. Longitudinal growth assessment for prediction of adverse perinatal outcome in fetuses suspected to be small-for-gestational age. Ultrasound Obstet Gynecol. 2018;52:325-31. doi: 10.1002/uog.18824. PubMed PMID: 28782171.
- Lees CC, Stampalija T, Baschat A, da Silva Costa F, Ferrazzi E, Figueras F, et al. ISUOG Practice Guidelines: diagnosis and management of small-for-gestational-age fetus and fetal growth restriction. Ultrasound Obstet Gynecol. 2020;56:298-312. doi: 10.1002/uog.22134. PubMed PMID: 32738107.
- Vanlieferinghen S, Anselem O, Le Ray C, Shen Y, Marcellin L, Goffinet F. Prognostic value of umbilical and cerebral Doppler in fetal growth restriction: comparison of dichorionic twins and singletons. PLoS One. 2015;10:e0123067. doi: 10.1371/journal.pone.0123067. PubMed PMID: 25875366; PubMed Central PMCID: PMCPMC4395410.
- Baschat AA. Planning management and delivery of the growth-restricted fetus. Best Pract Res Clin Obstet Gynaecol. 2018;49:53-65. doi: 10.1016/j.bpobgyn.2018.02.009. PubMed PMID: 29606482.
- Burd I, Srinivas S, Pare E, Dharan V, Wang E. Is sonographic assessment of fetal weight influenced by formula selection? J Ultrasound Med. 2009;28:1019-24. doi: 10.7863/jum.2009.28.8.1019. PubMed PMID: 19643784.
- American College of O, Gynecologists’ Committee on Practice B-O, the Society f-F. ACOG Practice Bulletin No. 204: Fetal Growth Restriction. Obstet Gynecol. 2019;133:e97-e109. doi: 10.1097/AOG.0000000000003070. PubMed PMID: 30681542.
- Tang W, Luo Y, Zeng S, Zhou J, Xu G, Yang J. Evaluation of fetal foramen ovale blood flow by pulsed Doppler ultrasonography combined with spatiotemporal image correlation : To define the normal reference range of fetal foramen ovale blood volume for each gestational age: a cross-sectional study. Cardiovasc Ultrasound. 2021;19:18. doi: 10.1186/s12947-021-00247-0. PubMed PMID: 33952244; PubMed Central PMCID: PMCPMC8101195.
- Figueras F, Puerto B, Martinez JM, Cararach V, Vanrell JA. Cardiac function monitoring of fetuses with growth restriction. Eur J Obstet Gynecol Reprod Biol. 2003;110:159-63. doi: 10.1016/s0301-2115(03)00123-4. PubMed PMID: 12969576.
- Kiserud T, Chedid G, Rasmussen S. Foramen ovale changes in growth-restricted fetuses. Ultrasound Obstet Gynecol. 2004;24:141-6. doi: 10.1002/uog.1079. PubMed PMID: 15287050.
- Meler E, Martinez J, Boada D, Mazarico E, Figueras F. Doppler studies of placental function. Placenta. 2021;108:91-6. doi: 10.1016/j.placenta.2021.03.014. PubMed PMID: 33857819.
- Kanagawa T, Ishii K, Yamamoto R, Sasahara J, Mitsuda N. Fetal Outcomes Associated with the Sequence of Doppler Deterioration in Severely Growth-Restricted Fetuses. J Ultrasound Med. 2021;40:2307-15. doi: 10.1002/jum.15614. PubMed PMID: 33438784.
- Narendran N, Yusuf K. Fetal Doppler Assessment in Neonatal Care: Analysis of Fetal Doppler Abnormalities and Neonatal Outcomes. Neoreviews. 2019;20:e575-e83. doi: 10.1542/neo.20-10-e575. PubMed PMID: 31575779.
- Aditya I, Tat V, Sawana A, Mohamed A, Tuffner R, Mondal T. Use of Doppler velocimetry in diagnosis and prognosis of intrauterine growth restriction (IUGR): A Review. J Neonatal Perinatal Med. 2016;9:117-26. doi: 10.3233/NPM-16915132. PubMed PMID: 27197939.
- Moraitis AA, Bainton T, Sovio U, Brocklehurst P, Heazell AE, Thornton JG, et al. Fetal umbilical artery Doppler as a tool for universal third trimester screening: A systematic review and meta-analysis of diagnostic test accuracy. Placenta. 2021;108:47-54. doi: 10.1016/j.placenta.2021.03.011. PubMed PMID: 33819861.
- Tolu LB, Ararso R, Abdulkadir A, Feyissa GT, Worku Y. Perinatal outcome of growth restricted fetuses with abnormal umbilical artery Doppler waveforms compared to growth restricted fetuses with normal umbilical artery Doppler waveforms at a tertiary referral hospital in urban Ethiopia. PLoS One. 2020;15:e0234810. doi: 10.1371/journal.pone.0234810. PubMed PMID: 32555633; PubMed Central PMCID: PMCPMC7302535.
- Ali A, Ara I, Sultana R, Akram F, Zaib MJ. Comparison of perinatal outcome of growth restricted fetuses with normal and abnormal umbilical artery Doppler waveforms. J Ayub Med Coll Abbottabad. 2014;26:344-8. PubMed PMID: 25671944.
- Vollgraff Heidweiller-Schreurs CA, De Boer MA, Heymans MW, Schoonmade LJ, Bossuyt PMM, Mol BWJ, et al. Prognostic accuracy of cerebroplacental ratio and middle cerebral artery Doppler for adverse perinatal outcome: systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2018;51:313-22. doi: 10.1002/uog.18809. PubMed PMID: 28708272; PubMed Central PMCID: PMCPMC5873403.
- Martinez-Portilla RJ, Caradeux J, Meler E, Lip-Sosa DL, Sotiriadis A, Figueras F. Third-trimester uterine artery Doppler for prediction of adverse outcome in late small-for-gestational-age fetuses: systematic review and meta-analysis. Ultrasound Obstet Gynecol. 2020;55:575-85. doi: 10.1002/uog.21940. PubMed PMID: 31785172.
- Zarean E, Shabaninia S. The Assessment of Association between Uterine Artery Pulsatility Index at 30-34 Week’s Gestation and Adverse Perinatal Outcome. Adv Biomed Res. 2018;7:111. doi: 10.4103/abr.abr_112_17. PubMed PMID: 30123785; PubMed Central PMCID: PMCPMC6071441.
- Ramos DR, Araujo Junior E, Petrini CG, Dulgheroff FF, Caldas T, Peixoto AB. Increased pulsatility index of uterine artery Doppler between 26 and 28 weeks of gestation and adverse perinatal outcomes. J Matern Fetal Neonatal Med. 2022;35:4810-7. doi: 10.1080/14767058.2020.1865301. PubMed PMID: 33390064.
- Turan OM, Turan S, Berg C, Gembruch U, Nicolaides KH, Harman CR, et al. Duration of persistent abnormal ductus venosus flow and its impact on perinatal outcome in fetal growth restriction. Ultrasound Obstet Gynecol. 2011;38:295-302. doi: 10.1002/uog.9011. PubMed PMID: 21465604.
- Malutan AM, Clinciu D, Mirescu SC, Ciortea R, Dudea-Simon M, Mihu D. Ultrasound Probe Pressure on the Maternal Abdominal Wall and the Effect on Fetal Middle Cerebral Artery Doppler Indices. Medicina (Kaunas). 2019;55. doi: 10.3390/medicina55080410. PubMed PMID: 31357513; PubMed Central PMCID: PMCPMC6723937.
- Kim YH, Lee HJ, Shin JE, Lee Y, Shin JC, Park TC, et al. The predictive value of the uterine artery pulsatility index during the early third trimester for the occurrence of adverse pregnancy outcomes depending on the maternal obesity. Obes Res Clin Pract. 2015;9:374-81. doi: 10.1016/j.orcp.2014.12.001. PubMed PMID: 25534491.
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