Perinatal outcomes of monochorionic multigestational pregnancies with different types of selective fetal growth restriction
Gladkova K.A., Frolova E.R., Sakalo V.A., Kostyukov K.V.
Background: Selective fetal growth restriction (sFGR) complicates 10–15% of pregnancies with monochorionic twins and is characterized by discordant fetal growth and a high level of perinatal and neonatal morbidity and mortality. sFGR is classified into three types according to the Doppler pattern of blood flow in the umbilical artery (UA) in growth-restricted twins. Each type is associated with a specific clinical course and perinatal and neonatal outcomes and differs in the degree of uneven placental separation and the functioning of placental-vascular anastomoses.
Objective: To assess the perinatal outcomes of expectant management of monochorionic diamniotic twin pregnancies complicated by sFGR according to the type of UA blood flow disorder in growth-restricted twins.
Materials and methods: A retrospective cohort study was conducted at V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia from January 2017 to January 2024. The course of pregnancy in 128 women with monochorionic diamniotic twin pregnancies complicated by sFGR was analyzed. Group 1 included patients with type I sFGR (n=72), group 2 included patients with type II sFGR (n=37), and group 3 included patients with type III sFGR (n=19).
Results: Perinatal parameters varied depending on the sFGR type. Antenatal fetal growth discordance was significantly different from the first trimester of pregnancy in types I and II sFGR, with the highest discordance observed in group 2. The age at delivery in sFGR type I was greater than that in types II and III (34.2, 31.4 and 31.6 weeks, respectively; p<0.001). Type II sFGR was characterized by the worst outcomes, including the highest discordance in neonatal body weight (42.9%, p<0.001) and the lowest length/height-for-age indicators of growth-restricted children– 988.5 g, 36 cm; body weight: p1/2<0.001, p2/3=0.0012, length: p1/2<0.001, p2/3=0.049). The proportion of children with growth restriction and severe and moderate birth asphyxia (Apgar score<5) was significantly higher in types II and III sFGR. In our study, the overall survival rate was 92.2% (20 children died, including 6 (2.34%) antenatally and 14 (5.5%) postnatally). Antenatal fetal death with growth restriction occurred in four cases (1.56%) with sFGR types I and II and co-twin death in one patient in group 2. Statistically significant adverse perinatal outcomes (χ2=19.713; p=0.003) were observed for sFGR type II.
Conclusion: The course of multigestational pregnancies complicated by type II sFGR is characterized by the most adverse perinatal outcomes. The classification of sFGR according to the type of UA blood flow disorder should form the basis for an individual management plan for pregnant women, with the level of observation corresponding to the degree of risk for perinatal loss.
Authors' contributions: Gladkova K.A. – conception and design of the study, review of the relevant literature, structuring and drafting of the manuscript; Kostyukov K.V. – material collection, data analysis, editing of the manuscript; Frolova E.R., Sakalo V.A. – data acquisition for analysis and statistical analysis, drafting of the manuscript.
Conflicts of interest: The authors have no conflicts of interest to declare.
Funding: There was no funding for this study.
Ethical Approval: The study was reviewed and approved by the Research Ethics Committee of the V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia.
Patient Consent for Publication: All patients provided informed consent for the publication of their data.
Authors' Data Sharing Statement: The data supporting the findings of this study are available upon request from the corresponding author after approval from the principal investigator.
For citation: Gladkova K.A., Frolova E.R., Sakalo V.A., Kostyukov K.V. Perinatal outcomes of
monochorionic multigestational pregnancies with different types of selective fetal growth restriction.
Akusherstvo i Ginekologiya/Obstetrics and Gynecology. 2025; (1): 35-43 (in Russian)
https://dx.doi.org/10.18565/aig.2024.322
Keywords
References
- Valsky D.V., Eixarch E., Martinez J.M., Crispi F., Gratacós E. Selective intrauterine growth restriction in monochorionic twins: pathophysiology, diagnostic approach and management dilemmas. Semin. Fetal Neonatal. Med. 2010; 15(6): 342-8. https://dx.doi.org/10.1016/j.siny.2010.07.002.
- Lewi L., Jani J., Blickstein I., Huber A., Gucciardo L., Van Mieghem T. et al. The outcome of monochorionic diamniotic twin gestations in the era of invasive fetal therapy: a prospective cohort study. Am. J. Obstet. Gynecol. 2008; 199(5): 514.e1-514.e8. https://dx.doi.org/10.1016/j.ajog.2008.03.050.
- Khalil A., Rodgers M., Baschat A., Bhide A., Gratacos E., Hecher K. et al. ISUOG Practice Guidelines: role of ultrasound in twin pregnancy. Ultrasound Obstet. Gynecol. 2016; 47(2): 247-63. https://dx.doi.org/10.1002/uog.15821.
- Lopriore E., Sluimers C., Pasman S.A., Middeldorp J.M., Oepkes D., Walther F.J. Neonatal morbidity in growth-discordant monochorionic twins: comparison between the larger and the smaller twin. Twin Res. Hum. Genet. 2012; 15(4): 541-6. https://dx.doi.org/10.1017/thg.2012.26.
- Костюков К.В., Гладкова К.А. Перинатальные исходы при монохориальной многоплодной беременности, осложненной синдромом селективной задержки роста плода. Акушерство и гинекология. 2020; 6: 50-8. [Kostyukov K.V., Gladkova K.A. Perinatal outcomes of monochorionic multiple pregnancies with selective intrauterine growth restriction. Obstetrics and Gynecology. 2020; (6): 50-8 (in Russian)]. https://dx.doi.org/10.18565/aig.2020.6.50-58.
- Фролова Е.Р., Гладкова К.А., Туманова У.Н., Сакало В.А., Костюков К.В., Ляпин В.М., Щеголев А.И., Ходжаева З.С. Морфологическая характеристика плаценты при монохориальной диамниотической двойне, осложненной синдромом селективной задержки роста плода. Проблемы репродукции. 2023; 29(1): 79-85. [Frolova E.R., Gladkova K.A., Tumanova U.N., Sakalo V.A., Kostyukov K.V., Lyapin V.M., Shchegolev A.I., Khodzhaeva Z.S. Placental characteristics of selective fetal growth restriction in monochorionic diamniotic twins. Russian Journal of Human Reproduction. 2023; 29(1): 79-85. (in Russian)]. https://dx.doi.org/10.17116/repro20232901179.
- Gratacós E., Lewi L., Muñoz B., Acosta-Rojas R., Hernandez-Andrade E., Martinez J.M. et al. A classification system for selective intrauterine growth restriction in monochorionic pregnancies according to umbilical artery Doppler flow in the smaller twin. Ultrasound Obstet. Gynecol. 2007; 30(1): 28-34. https://dx.doi.org/10.1002/uog.4046.
- Ishii K., Murakoshi T., Takahashi Y., Shinno T., Matsushita M., Naruse H. et al. Perinatal outcome of monochorionic twins with selective intrauterine growth restriction and different types of umbilical artery Doppler under expectant management. Fetal Diagn. Ther. 2009; 26(3): 157-61. https://dx.doi.org/10.1159/000253880.
- Batsry L., Matatyahu N., Avnet H., Weisz B., Lipitz S., Mazaki‐Tovi S. et al. Perinatal outcome of monochorionic diamniotic twin pregnancy complicated by selective intrauterine growth restriction according to umbilical artery Doppler flow pattern: single‐center study using strict fetal surveillance protocol. Ultrasound Obstet. Gynecol. 2021; 57(5): 748-55. https://dx.doi.org/10.1002/uog.22128.
- Buca D., Pagani G., Rizzo G., Familiari A., Flacco M.E., Manzoli L. et al. Outcome of monochorionic twin pregnancy with selective intrauterine growth restriction according to umbilical artery Doppler flow pattern of smaller twin: systematic review and meta‐analysis. Ultrasound Obstet. Gynecol. 2017; 50(5): 559-68. https://dx.doi.org/10.1002/uog.17362.
- Gratacós E., Carreras E., Becker J., Lewi L., Enríquez G., Perapoch J. et al. Prevalence of neurological damage in monochorionic twins with selective intrauterine growth restriction and intermittent absent or reversed end-diastolic umbilical artery flow. Ultrasound Obstet. Gynecol. 2004; 24(2): 159-63. https://dx.doi.org/10.1002/uog.1105.
- Van Mieghem T., Eixarch E., Gucciardo L., Done E., Gonzales I., Van Schoubroeck D. et al. Outcome prediction in monochorionic diamniotic twin pregnancies with moderately discordant amniotic fluid. Ultrasound Obstet Gynecol. 2011; 37(1): 15-21. https://dx.doi.org/10.1002/uog.8802.
- Sapantzoglou I., Rouvali A., Koutras A., Chatziioannou M.I., Prokopakis I., Fasoulakis Z. et al. sFLT1, PlGF, the sFLT1/PlGF ratio and their association with pre-eclampsia in twin pregnancies – a review of the literature. Medicina (B Aires). 2023; 59(7): 1232. https://dx.doi.org/10.3390/medicina59071232.
- Hong J., Kumar S. Circulating biomarkers associated with placental dysfunction and their utility for predicting fetal growth restriction. Clin. Sci. 2023; 137(8): 579-95. https://dx.doi.org/10.1042/CS20220300.
- Gratacós E., Antolin E., Lewi L., Martínez J.M., Hernandez‐Andrade E., Acosta‐Rojas R. et al. Monochorionic twins with selective intrauterine growth restriction and intermittent absent or reversed end‐diastolic flow (Type III): feasibility and perinatal outcome of fetoscopic placental laser coagulation. Ultrasound Obstet. Gynecol. 2008; 31(6): 669-75. https://dx.doi.org/10.1002/uog.5362.
- Peeva G., Bower S., Orosz L., Chaveeva P., Akolekar R., Nicolaides K.H. Endoscopic placental laser coagulation in monochorionic diamniotic twins with Type II selective fetal growth restriction. Fetal Diagn. Ther. 2015; 38(2): 86-93. https://dx.doi.org/10.1159/000374109.
- Colmant C., Lapillonne A., Stirnemann J., Belaroussi I., Leroy‐Terquem E., Kermovant‐Duchemin E. et al. Impact of different prenatal management strategies in short‐ and long‐term outcomes in monochorionic twin pregnancies with selective intrauterine growth restriction and abnormal flow velocity waveforms in the umbilical artery Doppler: a retrospective obse. BJOG. 2021; 128(2): 401-9. https://dx.doi.org/10.1111/1471-0528.16318.
- Khalil A., Beune I., Hecher K., Wynia K., Ganzevoort W., Reed K. et al. Consensus definition and essential reporting parameters of selective fetal growth restriction in twin pregnancy: a Delphi procedure. Ultrasound Obstet. Gynecol. 2019; 53(1): 47-54. https://dx.doi.org/10.1002/uog.19013.
- Monaghan C., Kalafat E., Binder J., Thilaganathan B., Khalil A. Prediction of adverse pregnancy outcome in monochorionic diamniotic twin pregnancy complicated by selective fetal growth restriction. Ultrasound Obstet. Gynecol. 2019; 53(2): 200-7. https://dx.doi.org/10.1002/uog.19078.
- Curado J., Sileo F., Bhide A., Thilaganathan B., Khalil A. Early‐ and late‐onset selective fetal growth restriction in monochorionic diamniotic twin pregnancy: natural history and diagnostic criteria. Ultrasound Obstet. Gynecol. 2020; 55(5): 661-6. https://dx.doi.org/10.1002/uog.20849.
- Kajiwara K., Ozawa K., Wada S., Samura O. Molecular mechanisms underlying twin-to-twin transfusion syndrome. Cells. 2022; 11(20): 3268. https://dx.doi.org/10.3390/cells11203268.
- Satorres E., Martínez-Varea A., Diago-Almela V. sFlt-1/PlGF ratio as a predictor of pregnancy outcomes in twin pregnancies: a systematic review. J. Matern. Fetal Neonatal. Med. 2023; 36(2): 2230514. https://dx.doi.org/10.1080/14767058.2023.2230514.
- D’Antonio F., Khalil A., Pagani G., Papageorghiou A.T., Bhide A., Thilaganathan B. Crown–rump length discordance and adverse perinatal outcome in twin pregnancies: systematic review and meta‐analysis. Ultrasound Obstet. Gynecol. 2014; 44(2): 138-46. https://dx.doi.org/10.1002/uog.13335.
- Litwinska E., Syngelaki A., Cimpoca B., Sapantzoglou I., Nicolaides K.H. Intertwin discordance in fetal size at 11–13 weeks’ gestation and pregnancy outcome. Ultrasound Obstet. Gynecol. 2020; 55(2): 189-97. https://dx.doi.org/10.1002/uog.21923.
Received 16.12.2024
Accepted 27.12.2024
About the Authors
Kristina A. Gladkova, PhD, Senior Researcher at the Fetal Medicine Unit, Institute of Obstetrics, Head of the 1st Obstetric Department of Pregnancy Pathology,V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia, 117997, Russia, Moscow, Ac. Oparin str., 4, +7(916)321-10-07, k_gladkova@oparina4.ru,
https://orcid.org/0000-0001-8131-4682
Ekaterina R. Frolova, PhD student at the 1st Obstetric Department of Pregnancy Pathology, V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia,
117997, Russia, Moscow, Ac. Oparin str., 4, +7(495)438-07-88, e_frolova@oparina4.ru, https://orcid.org/0000-0003-2817-3504
Viktoriya A. Sakalo, PhD, Junior Researcher at the Department of Pregnancy Pathology, Institute of Obstetrics, obstetrician-gynecologist at the 1st Obstetric Department of Pregnancy Pathology, V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia, 117997, Russia, Moscow, Ac. Oparin str., 4, +7(929)588-72-08, v_sakalo@oparina4.ru, https://orcid.org/0000-0002-5870-4655
Kirill V. Kostyukov, Dr. Med. Sci, Head of the Department of the Ultrasound and Functional Diagnosis, V.I. Kulakov NMRC for OG&P, Ministry of Health of Russia,
117997, Russia, Moscow, Ac. Oparin str., 4, +7(495)438-25-29, k_kostyukov@oparina4.ru, https://orcid.org/0000-0003-3094-4013