Current views on the diagnosis and prognosis of fetal growth restriction (A literature review)

Abstract

Fetal growth restriction remains a leading cause of preterm birth and neurological disorders in children and is associated with high neonatal and perinatal morbidity and mortality. Fetal growth restriction is strongly associated with preeclampsia, placental insufficiency, and does not tend to decrease in frequency. The terms “small for gestational age” and “fetal growth restriction” are similar in terms of fetometry, however, in modern literature, these concepts differ based on blood flow disorders in the “mother-placenta-fetus” system and perinatal complications. A deep understanding of the multifactorial pathogenesis of early and late fetal growth restriction will allow for developing targeted therapy of placental insufficiency. Determining the role of new placental growth biomarkers plays a significant role in understanding the pathogenesis of placental dysfunction and developing measures to predict placenta-associated pregnancy complications.

This review article highlights new approaches to effective fetal growth restriction screening. Recent advances in ultrasound diagnosis of fetal growth restriction provide the basis for multivariate testing that can provide cost-effective screening for placental-associated pregnancy complications, including fetal growth restriction.

Keywords

placental insufficiency / fetal growth restriction / fetal growth restriction biomarkers / management for fetal growth restriction / perinatal outcomes of fetal growth restriction / centile scale / small for gestational age

References

[1] Audette MC, Kingdom JC. Screening for fetal growth restriction and placental insufficiency. Semin Fetal Neonatal Med. 2018;23(2):119–125. DOI: 10.1016/j.siny.2017.11.004

[2] Audette M.C., Kingdom J.C. Screening for fetal growth restriction and placental insufficiency // Semin. Fetal Neonatal. Med. 2018. Vol. 23. No. 2. P. 119–125. DOI: 10.1016/j.siny.2017.11.004

[3] Damodaram M, Story L, Kulinskaya E, et al. Early adverse perinatal complications in preterm growth-restricted fetuses. Aust N Z J Obstet Gynaecol. 2011;51(3):204–209. DOI: 10.1111/j.1479-828X.2011.01299.x

[4] Damodaram M., Story L., Kulinskaya E., et al. Early adverse perinatal complications in preterm growth-restricted fetuses //Aust. N. Z. J. Obstet. Gynaecol. 2011. Vol. 51. No. 3. P. 204–209. DOI: 10.1111/j.1479-828X.2011.01299.x

[5] Lees C, Marlow N, Arabin B, et al.; TRUFFLE Group. Perinatal morbidity and mortality in early-onset fetal growth restriction: cohort outcomes of the trial of randomized umbilical and fetal flow in Europe (TRUFFLE). Ultrasound Obstet Gynecol. 2013;42 (4):400–408. DOI: 10.1002/uog.13190

[6] Lees C., Marlow N., Arabin B., et al. Perinatal morbidity and mortality in early-onset fetal growth restriction: cohort outcomes of the trial of randomized umbilical and fetal flow in Europe (TRUFFLE) // Ultrasound Obstet. Gynecol. 2013. Vol. 42. No. 4. P. 400–408. DOI: 10.1002/uog.13190

[7] Nardozza LM, Caetano AC, Zamarian AC, et al. Fetal growth restriction: current knowledge. Arch Gynecol Obstet. 2017;295(5):1061–1077. DOI: 10.1007/s00404-017-4341-9

[8] Nardozza L.M., Caetano A.C., Zamarian A.C., et al. Fetal growth restriction: current knowledge // Arch. Gynecol. Obstet. 2017. Vol. 295. No. 5. P. 1061–1077. DOI: 10.1007/s00404-017-4341-9

[9] Flenady V, Wojcieszek AM, Middleton P, et al. Stillbirths: recall to action in high-income countries. Lancet. 2016;387(100190):691–702. DOI: 10.1016/S0140-6736(15)01020-X

[10] Flenady V., Wojcieszek A.M., Middleton P., et al. Stillbirths: recall to action in high-income countries // Lancet. 2016. Vol. 387. No. 10019. P. 691–702. DOI: 10.1016/S0140-6736(15)01020-X

[11] International Stillbirth Alliance Collaborative for Improving Classification of Perinatal Deaths, Flenady V, Wojcieszek AM, Ellwood D, et al. Classification of causes and associated conditions for stillbirths and neonatal deaths. Semin Fetal Neonatal Med. 2017;22(3):176–185. DOI: 10.1016/j.siny.2017.02.009

[12] International Stillbirth Alliance Collaborative for Improving Classification of Perinatal Deaths; Flenady V., Wojcieszek A.M., Ellwood D., et al. Classification of causes and associated conditions for stillbirths and neonatal deaths // Semin. Fetal Neonatal. Med. 2017. Vol. 22. No. 3. P. 176–185. DOI: 10.1016/j.siny.2017.02.009

[13] Barker DJ. Fetal origins of coronary heart disease. BMJ. 1995;311(6998):171–174. DOI: 10.1136/bmj.311.6998.171

[14] Barker D.J. Fetal origins of coronary heart disease // BMJ. 1995. Vol. 311. No. 6998. P. 171–174. DOI: 10.1136/bmj.311.6998.171

[15] Barker DJ. In utero programming of chronic disease. Clin Sci (Lond). 1998;95(2):115–128.

[16] Barker D.J. In utero programming of chronic disease // Clin. Sci. (Lond.). 1998. Vol. 95. No. 2. P. 115–128.

[17] Kurtser MA, Sichinava LG, Shishkina DI, et al. Fetal growth restriction: current diagnostic criteria, management of pregnancy and labor. Gynecology, Obstetrics and Perinatology. 2023;22(1):5–11. (In Russ.) DOI: 10.20953/1726-1678-2023-1-5-11

[18] Курцер М.А., Сичинава Л.Г., Шишкина Д.И., и др. Задержка роста плода: современные критерии диагностики, тактика ведения беременности и родов // Вопросы гинекологии, акушерства и перинатологии. 2023. Т. 22. № 1. С. 5–11. DOI: 10.20953/1726-1678-2023-1-5-11

[19] Gordijn SJ, Beune IM, Thilaganathan B, et al. Consensus definition of fetal growth restriction: a Delphi procedure. Ultrasound Obstet Gynecol. 2016;48(3):333–339. DOI: 10.1002/uog.15884

[20] Gordijn S.J., Beune I.M., Thilaganathan B., et al. Consensus definition of fetal growth restriction: a Delphi procedure // Ultrasound Obstet. Gynecol. 2016. Vol. 48. No. 3. P. 333–339. DOI: 10.1002/uog.15884

[21] Podzolkova NM, Denisova YuV, Skvortsova MYu, et al. Fetal growth restriction: unresolved issues of risk stratification, early diagnosis, and obstetric management. Gynecology, Obstetrics and Perinatology. 2021;20(5):76–86. (In Russ.) DOI: 10.20953/1726-1678-2021-5-76-86

[22] Подзолкова Н.М., Денисова Ю.В., Скворцова М.Ю., и др. Синдром задержки роста плода: нерешенные вопросы стратификации рисков, ранней диагностики и акушерской тактики // Вопросы гинекологии, акушерства и перинатологии. 2021. Т. 20. № 5. С. 76–86 DOI: 10.20953/1726-1678-2021-5-76-86

[23] Melamed N, Baschat A, Yinon Y, et al. FIGO (international Federation of Gynecology and obstetrics) initiative on fetal growth: best practice advice for screening, diagnosis, and management of fetal growth restriction. Int J Gynaecol Obstet. 2021;152(1):3–57. DOI: 10.1002/ijgo.13522

[24] Melamed N., Baschat A., Yinon Y., et al. FIGO (international Federation of Gynecology and obstetrics) initiative on fetal growth: best practice advice for screening, diagnosis, and management of fetal growth restriction // Int. J. Gynaecol. Obstet. 2021. Vol. 152. No. 1. P. 3–57. DOI: 10.1002/ijgo.13522

[25] Hung TH, Hsieh TT, Chen SF. Risk of abnormal fetal growth in women with early- and late-onset preeclampsia. Pregnancy Hypertens. 2018;12:201–206. DOI: 10.1016/j.preghy.2017.09.003

[26] Hung T.H., Hsieh T.T., Chen S.F. Risk of abnormal fetal growth in women with early- and late-onset preeclampsia // Pregnancy Hypertens. 2018. Vol. 12. P. 201–206. DOI: 10.1016/j.preghy.2017.09.003

[27] Crovetto F, Triunfo S, Crispi F, et al. Differential performance of first-trimester screening in predicting small-for-gestational-age neonate or fetal growth restriction. Ultrasound Obstet Gynecol. 2017;49(3):349–356. DOI: 10.1002/uog.15919

[28] Crovetto F., Triunfo S., Crispi F., et al. Differential performance of first-trimester screening in predicting small-for-gestational-age neonate or fetal growth restriction // Ultrasound Obstet. Gynecol. 2017. Vol. 49. No. 3. P. 349–356. DOI: 10.1002/uog.15919

[29] Ignatko IV, Miryushchenko MM. Predictive factors for intrauterine fetal growth restriction. Health and Education Millennium. 2016;18(1):1–4. (In Russ.)

[30] Игнатко И.В., Мирющенко М.М. Прогностические маркеры синдрома задержки роста плода // Журнал научных статей: Здоровье и образование в XXI веке. 2016. Т. 18. № 1. С. 1–4.

[31] Cignini P, Maggio Savasta L, Gulino FA, et al. Predictive value of pregnancy-associated plasma protein-A (PAPP-A) and free beta-hCG on fetal growth restriction: results of a prospective study. Arch Gynecol Obstet. 2016;293(6):1227–1233. DOI: 10.1007/s00404-015-3947-z

[32] Cignini P., Maggio Savasta L., Gulino F.A., et al. Predictive value of pregnancy-associated plasma protein-A (PAPP-A) and free beta-hCG on fetal growth restriction: results of a prospective study // Arch. Gynecol. Obstet. 2016. Vol. 293. No. 6. P. 1227–1233. DOI: 10.1007/s00404-015-3947-z

[33] Karagiannis G, Akolekar R, Sarquis R, et al. Prediction of small-for-gestation neonates from biophysical and biochemical markers at 11-13 weeks. Fetal Diagn Ther. 2011;29(2):148–154. DOI: 10.1159/000321694

[34] Karagiannis G., Akolekar R., Sarquis R., et al. Prediction of small-for-gestation neonates from biophysical and biochemical markers at 11–13 weeks // Fetal Diagn. Ther. 2011. Vol. 29. No. 2. P. 148–154. DOI: 10.1159/000321694

[35] Smith GC, Stenhouse EJ, Crossley JA, et al. Early pregnancy levels of pregnancy-associated plasma protein a and the risk of intrauterine growth restriction, premature birth, preeclampsia, and stillbirth. J Clin Endocrinol Metab. 2002;87(4):1762–1767. DOI: 10.1210/jcem.87.4.8430

[36] Smith G.C., Stenhouse E.J., Crossley J.A., et al. Early pregnancy levels of pregnancy-associated plasma protein-A and the risk of intrauterine growth restriction, premature birth, preeclampsia, and stillbirth // J. Clin. Endocrinol. Metab. 2002. Vol. 87. No. 4. P. 1762–1767. DOI: 10.1210/jcem.87.4.8430

[37] D’Antonio F, Rijo C, Thilaganathan B, et al. Association between first-trimester maternal serum pregnancy-associated plasma protein-A and obstetric complications. Prenat Diagn. 2013;33(9):839–847. DOI: 10.1002/pd.4141

[38] D’Antonio F., Rijo C., Thilaganathan B., et al. Association between first-trimester maternal serum pregnancy-associated plasma protein-A and obstetric complications // Prenat. Diagn. 2013. Vol. 33. No. 9. P. 839–847. DOI: 10.1002/pd.4141

[39] Khalil A, Sodre D, Syngelaki A, et al. Maternal hemodynamics at 11–13 weeks of gestation in pregnancies delivering small for gestational age neonates. Fetal Diagn Ther. 2012;32(4):231–238. DOI: 10.1159/000339480

[40] Khalil A., Sodre D., Syngelaki A., et al. Maternal hemodynamics at 11-13 weeks of gestation in pregnancies delivering small for gestational age neonates // Fetal. Diagn. Ther. 2012. Vol. 32. No. 4. P. 231–238. DOI: 10.1159/000339480

[41] Zafiridi NV. Klinicheskoe znachenie angiogennykh markerov dlya vyrabotki taktiki beremennykh s platsento-asotsiirovannymi oslozhneniyami [dissertation abstract]. Moscow; 2022. (In Russ.) [cited 2023 May 25]. Available from: https://www.dissercat.com/content/klinicheskoe-znachenie-angiogennykh-markerov-dlya-vyrabotki-taktiki-vedeniya-beremennykh-s

[42] Зафириди Н.В. Клиническое значение ангиогенных маркеров для выработки тактики беременных с плаценто-асоциированными осложнениями: автореф. дис. … кан. мед. наук. Москва, 2022 [дата обращения 12.04.2023]. Доступ по ссылке: https://www.dissercat.com/content/klinicheskoe-znachenie-angiogennykh-markerov-dlya-vyrabotki-taktiki-vedeniya-beremennykh-s

[43] Romero R, Nien JK, Espinoza J, et al. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate. J Matern Fetal Neonatal Med. 2008;21(1):9–23. DOI: 10.1080/14767050701830480

[44] Romero R., Nien J.K., Espinoza J., et al. A longitudinal study of angiogenic (placental growth factor) and anti-angiogenic (soluble endoglin and soluble vascular endothelial growth factor receptor-1) factors in normal pregnancy and patients destined to develop preeclampsia and deliver a small for gestational age neonate // J. Matern. Fetal. Neonatal. Med. 2008. Vol. 21. No. 1. P. 9–23. DOI: 10.1080/14767050701830480

[45] Maynard SE, Min JY, Merchan J, et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia. J Clin Invest. 2003;111(5):649–658. DOI: 10.1172/JCI17189

[46] Maynard S.E., Min J.Y., Merchan J., et al. Excess placental soluble fms-like tyrosine kinase 1 (sFlt1) may contribute to endothelial dysfunction, hypertension, and proteinuria in preeclampsia // J. Clin. Invest. 2003. Vol. 111. No. 5. P. 649–658. DOI: 10.1172/JCI17189

[47] Venkatesha S, Toporsian M, Lam C, et al. Soluble endo glin contributes to the pathogenesis of preeclampsia. Nat Med. 2006;12(6):642–649. DOI: 10.1038/nm1429

[48] Venkatesha S., Toporsian M., Lam C., et al. Soluble endoglin contributes to the pathogenesis of preeclampsia // Nat. Med. 2006. Vol. 12. No. 6. P. 642–649. DOI: 10.1038/nm1429

[49] McCowan LM, Thompson JM, Taylor RS, et al.; SCOPE consortium. Prediction of small for gestational age infants in healthy nulliparous women using clinical and ultrasound risk factors combined with early pregnancy biomarkers. PLoS One. 2017;12(1). DOI: 10.1371/journal.pone.0169311

[50] McCowan L.M., Thompson J.M., Taylor R.S., et al.; SCOPE consortium. prediction of small for gestational age infants in healthy nulliparous women using clinical and ultrasound risk factors combined with early pregnancy biomarkers // PLoS One. 2017. Vol. 12. No. 1. DOI: 10.1371/journal.pone.0169311

[51] Witwicki J, Chaberek K, Szymecka-Samaha N, et al. sFlt-1/PlGF ratio in prediction of short-term neonatal outcome of small for gestational age neonates. Children (Basel). 2021;8(8). DOI: 10.3390/children8080718

[52] Witwicki J., Chaberek K., Szymecka-Samaha N., et al. sFlt-1/PlGF ratio in prediction of short-term neonatal outcome of small for gestational age neonates // Children (Basel). 2021. Vol. 8. No. 8. DOI: 10.3390/children8080718

[53] Quezada MS, Rodríguez-Calvo J, Villalaín C, et al. sFlt-1/PlGF ratio and timing of delivery in early-onset fetal growth restriction with antegrade umbilical artery flow. Ultrasound Obstet Gynecol. 2020;56(4):549–556. DOI: 10.1002/uog.21949

[54] Quezada M.S., Rodríguez-Calvo J., Villalaín C., et al. sFlt-1/PlGF ratio and timing of delivery in early-onset fetal growth restriction with antegrade umbilical artery flow // Ultrasound Obstet. Gynecol. 2020. Vol. 56. No. 4. P. 549–556. DOI: 10.1002/uog.21949

[55] Lesmes C, Gallo DM, Gonzalez R, et al. Prediction of small-for-gestational-age neonates: screening by maternal serum biochemical markers at 19–24 weeks. Ultrasound Obstet Gynecol. 2015;46(3):341–349. DOI: 10.1002/uog.14899

[56] Lesmes C., Gallo D.M., Gonzalez R., et al. Prediction of small-for-gestational-age neonates: screening by maternal serum biochemical markers at 19–24 weeks // Ultrasound Obstet. Gynecol. 2015. Vol. 46. No. 3. P. 341–349. DOI: 10.1002/uog.14899

[57] Valiño N, Giunta G, Gallo DM, et al. Biophysical and biochemical markers at 30-34 weeks’ gestation in the prediction of adverse perinatal outcome. Ultrasound Obstet Gynecol. 2016;47(2):194–202. DOI: 10.1002/uog.14928

[58] Valiño N., Giunta G., Gallo D.M., et al. Biophysical and biochemical markers at 30-34 weeks’ gestation in the prediction of adverse perinatal outcome // Ultrasound Obstet. Gynecol. 2016. Vol. 47. No. 2. P. 194–202. DOI: 10.1002/uog.14928

[59] Gaccioli F, Aye ILMH, Sovio U, et al. Screening for fetal growth restriction using fetal biometry combined with maternal biomarkers. Am J Obstet Gynecol. 2018;218(2S):S725–S737. DOI: 10.1016/j.ajog.2017.12.002

[60] Gaccioli F., Aye I.L.M.H., Sovio U., et al. Screening for fetal growth restriction using fetal biometry combined with maternal biomarkers // Am. J. Obstet. Gynecol. 2018. Vol. 218. No. 2S. P. S725–S737. DOI: 10.1016/j.ajog.2017.12.002

[61] Kudinova EI. Rol’ placentarnogo belka PP13 v formirovanii placentarnoj nedostatochnosti I zaderzhki rosta ploda [abstract dissertation]. Moscow; 2016. (In Russ.) [cited 2023 May 25]. Available from: https://www.dissercat.com/content/rol-platsentarnogo-belka-pp-13-v-formirovanii-platsentarnoi-nedostatochnosti-i-zaderzhki-ros

[62] Кудинова Е.И. Роль плацентарного белка РР13 в формировании плацентарной недостаточности и задержке роста плода: автореф. дис. ... канд. мед. наук. Москва, 2017 [дата обращения 12.04.2023]. Доступ по ссылке: https://www.dissercat.com/content/rol-platsentarnogo-belka-pp-13-v-formirovanii-platsentarnoi-nedostatochnosti-i-zaderzhki-ros

[63] Aghababaei M, Perdu S, Irvine K, et al. A disintegrin and metalloproteinase 12 (ADAM12) localizes to invasive trophoblast, promotes cell invasion and directs column outgrowth in early placental development. Mol Hum Reprod. 2014;20(3):235–249. DOI: 10.1093/molehr/gat084

[64] Aghababaei M., Perdu S., Irvine K., et al. A disintegrin and metalloproteinase 12 (ADAM12) localizes to invasive trophoblast, promotes cell invasion and directs column outgrowth in early placental development // Mol. Hum. Reprod. 2014. Vol. 20. No. 3. P. 235–249. DOI: 10.1093/molehr/gat084

[65] Biadasiewicz K, Fock V, Dekan S, et al. Extravillous trophoblast-associated ADAM12 exerts pro-invasive properties, including induction of integrin beta 1-mediated cellular spreading. Biol Reprod. 2014;90(5). DOI: 10.1095/biolreprod.113.115279

[66] Biadasiewicz K., Fock V., Dekan S., et al. Extravillous trophoblast-associated ADAM12 exerts pro-invasive properties, including induction of integrin beta 1-mediated cellular spreading // Biol. Reprod. 2014. Vol. 90. No. 5. DOI: 10.1095/biolreprod.113.115279

[67] Yu N, Cui H, Chen X, et al. First trimester maternal serum analytes and second trimester uterine artery Doppler in the prediction of preeclampsia and fetal growth restriction. Taiwan J Obstet Gynecol. 2017;56(3):358–361. DOI: 10.1016/j.tjog.2017.01.009

[68] Yu N., Cui H., Chen X., et al. First trimester maternal serum analytes and second trimester uterine artery Doppler in the prediction of preeclampsia and fetal growth restriction // Taiwan J. Obstet. Gynecol. 2017. Vol. 56. No. 3. P. 358–361. DOI: 10.1016/j.tjog.2017.01.009

[69] El-Sherbiny W, Nasr A, Soliman A. Metalloprotease (ADAM12-S) as a predictor of preeclampsia: correlation with severity, maternal complications, fetal outcome, and Doppler parameters. Hypertens Pregnancy. 2012;31(4):442–450. DOI: 10.3109/10641955.2012.690059

[70] El-Sherbiny W., Nasr A., Soliman A. Metalloprotease (ADAM12-S) as a predictor of preeclampsia: correlation with severity, maternal complications, fetal outcome, and Doppler parameters // Hypertens. Pregnancy. 2012. Vol. 31. No. 4. P. 442–450. DOI: 10.3109/10641955.2012.690059

[71] Grigorieva KN, Bitsadze VO, Khizroeva JK, et al. Metalloproteinases as biochemical markers of pregnancy pathology. Obstetrics, Gynecology and Reproduction. 2022;16(1):38–47. (In Russ.) DOI: 10.17749/2313-7347/ob.gyn.rep.2022.275

[72] Григорьева К.Н., Бицадзе В.О., Хизроева Д.Х., и др. Металлопротеиназы как биохимические маркеры патологии беременности // Акушерство, Гинекология и Репродукция. 2022. Т. 16. № 1. С. 38–47. DOI: 10.17749/2313-7347/ob.gyn.rep.2022.275

[73] Yakovleva NY, Vasileva EY, Kuznetsova LV, et al. The content of matrix metalloproteinase-12 in pregnancy complicated by preeclampsia. Journal of Obstetrics and Women’s Diseases. 2017;66(6):66–72. (In Russ.) DOI: 10.17816/JOWD66666-72

[74] Яковлева Н.Ю., Васильева Е.Ю., Кузнецова Л.В., и др. Содержание матриксной металлопротеиназы-12 при беременности, осложненной преэклампсией // Журнал акушерства и женских болезней. 2017. Т. 66. № 6. С. 66–72. DOI: 10.17816/JOWD66666-72

[75] Swissa SS, Walfisch A, Yaniv-Salem S, et al. Maternal blood angiogenic factors and the prediction of critical adverse perinatal outcomes among small-for-gestational-age pregnancies. Am J Perinatol. 2022. DOI: 10.1055/a-1798-1829

[76] Swissa S.S., Walfisch A., Yaniv-Salem S., et al. Maternal blood angiogenic factors and the prediction of critical adverse perinatal outcomes among small-for-gestational-age pregnancies // Am. J. Perinatol. 2022. Vol. 10. DOI: 10.1055/a-1798-1829

[77] Zamarian AC, Araujo Júnior E, Daher S, et al. Evaluation of biochemical markers combined with uterine artery Doppler parameters in fetuses with growth restriction: a case-control study. Arch Gynecol Obstet. 2016;294(4):715–723. DOI: 10.1007/s00404-016-4024-y

[78] Zamarian A.C., Araujo Júnior E., Daher S, et al. Evaluation of biochemical markers combined with uterine artery Doppler parameters in fetuses with growth restriction: a case-control study // Arch. Gynecol. Obstet. 2016. Vol. 294. No. 4. P. 715–723. DOI: 10.1007/s00404-016-4024-y

[79] Ignatko IV, Yakubova DI, Megrabyan AD, et al. Clinical significance of assessing autoantibody level in diagnostics of early and late fetal growth retardation. Obstetrics, Gynecology and Reproduction. 2022;16(4):450–462. (In Russ.) DOI: 10.17749/2313-7347/ob.gyn.rep.2022.340

[80] Игнатко И.В., Якубова Д.И., Меграбян А.Д., и др. Клиническое значение определения уровня аутоантител в диагностике ранней и поздней формы задержки роста плода // Акушерство, Гинекология и Репродукция. 2022. Т. 16. № 4. С. 450–462. DOI: 10.17749/2313-7347/ob.gyn.rep.2022.340

[81] Horgan RP, Broadhurst DI, Walsh SK, et al. Metabolic profiling uncovers a phenotypic signature of small for gestational age in early pregnancy. J Proteome Res. 2011;10(8):3660–3673. DOI: 10.1021/pr2002897

[82] Horgan R.P., Broadhurst D.I., Walsh S.K., et al. Metabolic profiling uncovers a phenotypic signature of small for gestational age in early pregnancy // J. Proteome Res. 2011. Vol. 10. No. 8. P. 3660–3673. DOI: 10.1021/pr2002897

[83] Heazell AE, Bernatavicius G, Warrander L, et al. A metabolomic approach identifies differences in maternal serum in third trimester pregnancies that end in poor perinatal outcome. Reprod Sci. 2012;19(8):863–875. DOI: 10.1177/1933719112438446

[84] Heazell A.E., Bernatavicius G., Warrander L., et al. A metabolomic approach identifies differences in maternal serum in third trimester pregnancies that end in poor perinatal outcome // Reprod. Sci. 2012. Vol. 19. No. 8. P. 863–875. DOI: 10.1177/1933719112438446

[85] Maitre L, Fthenou E, Athersuch T, et al. Urinary metabolic profiles in early pregnancy are associated with preterm birth and fetal growth restriction in the Rhea mother-child cohort study. BMC Med. 2014;12. DOI: 10.1186/1741-7015-12-110

[86] Maitre L., Fthenou E., Athersuch T., et al. Urinary metabolic profiles in early pregnancy are associated with preterm birth and fetal growth restriction in the Rhea mother-child cohort study // BMC Med. 2014. Vol. 12. DOI: 10.1186/1741-7015-12-110

[87] Chim SS, Shing TK, Hung EC, et al. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem. 2008;54(3):482–490. DOI: 10.1373/clinchem.2007.097972

[88] Chim S.S., Shing T.K., Hung E.C., et al. Detection and characterization of placental microRNAs in maternal plasma // Clin. Chem. 2008. Vol. 54. No. 3. P. 482–490. DOI: 10.1373/clinchem.2007.097972

[89] Tagliaferri S, Cepparulo P, Vinciguerra A, et al. miR-16-5p, miR-103-3p, and miR-27b-3p as early peripheral biomarkers of fetal growth restriction. Front Pediatr. 2021;9. DOI: 10.3389/fped.2021.611112

[90] Tagliaferri S., Cepparulo P., Vinciguerra A., et al. miR-16-5p, miR-103-3p, and miR-27b-3p as early peripheral biomarkers of fetal growth restriction // Front. Pediatr. 2021. Vol. 9. DOI: 10.3389/fped.2021.611112

[91] Velauthar L, Plana MN, Kalidindi M, et al. First-trimester uterine artery Doppler and adverse pregnancy outcome: a meta-analysis involving 55,974 women. Ultrasound Obstet Gynecol. 2014;43(5):500–507. DOI: 10.1002/uog.13275

[92] Velauthar L., Plana M.N., Kalidindi M., et al. First-trimester uterine artery Doppler and adverse pregnancy outcome: a meta-analysis involving 55,974 women // Ultrasound Obstet. Gynecol. 2014. Vol. 43. No. 5. P. 500–507. DOI: 10.1002/uog.13275

[93] Levytska K, Higgins M, Keating S, et al. Placental patho logy in relation to uterine artery doppler findings in pregnancies with severe intrauterine growth restriction and abnormal umbilical artery Doppler changes. Am J Perinatol. 2017;34(5):451–457. DOI: 10.1055/s-0036-1592347

[94] Levytska K., Higgins M., Keating S., et al. Placental pathology in relation to uterine artery doppler findings in pregnancies with severe intrauterine growth restriction and abnormal umbilical artery Doppler changes // Am. J. Perinatol. 2017. Vol. 34. No. 5. P. 451–457. DOI: 10.1055/s-0036-1592347

[95] Martin AM, Bindra R, Curcio P, et al. Screening for pre-eclampsia and fetal growth restriction by uterine artery Doppler at 11–14 weeks of gestation. Ultrasound Obstet Gynecol. 2001;18(6):583–586. DOI: 10.1046/j.0960-7692.2001.00594.x

[96] Martin A.M., Bindra R., Curcio P., et al. Screening for pre-eclampsia and fetal growth restriction by uterine artery Doppler at 11-14 weeks of gestation // Ultrasound Obstet. Gynecol. 2001. Vol. 18. No. 6. P. 583–586. DOI: 10.1046/j.0960-7692.2001.00594.x

[97] DeVore GR. The importance of the cerebroplacental ratio in the evaluation of fetal well-being in SGA and AGA fetuses. Am J Obstet Gynecol. 2015;213(1):5–15. DOI: 10.1016/j.ajog.2015.05.024

[98] DeVore G.R. The importance of the cerebroplacental ratio in the evaluation of fetal well-being in SGA and AGA fetuses // Am. J. Obstet. Gynecol. 2015. Vol. 213. No. 1. P. 5–15. DOI: 10.1016/j.ajog.2015.05.024

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