Selective Fetal Growth Restriction: Parts of Pathogenesis

Cover Page

Cite item

Full Text

Abstract

Monochorionic diamniotic twin gestations have a higher risk of perinatal complications than both dichorionic twins and singleton pregnancies. One of the complications of multiple pregnancies is selective fetal growth restriction (sFGR), the incidence of which varies from 10 to 25%. sFGR is a condition of twin pregnancy in which the development of one fetus is restricted, despite normal growth of the other fetus; one of the fetuses is supplied with insufficient nutrient and oxygen content through the placenta to grow at a normal rate. The pathogenesis of sFGR has a multifactorial nature, including disorders of trophoblast invasion, vasculo- and angiogenesis, gestational formation of the placenta with discordant separation of intertwin territories and unbalanced blood flow through interfetal anastomoses oxidative stress, growth factor imbalance, and changes in the metabolomic profile of cord blood and placental tissue. The prenatal diagnosis of sFGR is sometimes problematic and it is not possible to find all the cases. A more detailed study of the various predictors of the occurrence of sFGR will allow the discovery of new markers that will help in early diagnosis, determining the optimal management for pregnancy and predicting perinatal outcome.

Full Text

Restricted Access

About the authors

E. R. Frolova

Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology

Author for correspondence.
Email: kattirella@gmail.com
Russian Federation, Moscow

K. A. Gladkova

Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology

Email: kattirella@gmail.com
Russian Federation, Moscow

U. N. Tumanova

Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology

Email: kattirella@gmail.com
Russian Federation, Moscow

V. A. Sakalo

Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology

Email: kattirella@gmail.com
Russian Federation, Moscow

A. I. Shchegolev

Kulakov National Medical Research Center for Obstetrics, Gynecology and Perinatology

Email: kattirella@gmail.com
Russian Federation, Moscow

References

  1. Гладкова К.А., Сакало В.А., Вторушина В.В. и др. Роль факторов васкуло- и ангиогенеза в развитии селективной задержки роста плода при монохориальной многоплодной беременности // Акуш. гинекол. 2023. № 1. С. 48–54.
  2. Низяева Н.В., Дубова Е.А., Кан Н.Е. и др. Роль дендритных клеток и паттерн-распознающих рецепторов в развитии патологии беременности // Успехи соврем. биол. 2014. Т. 134 (6). С. 563–572.
  3. Павлов К.А., Дубова Е.А., Щеголев А.И. Фетоплацентарный ангиогенез при нормальной беременности: роль плацентарного фактора роста и ангиопоэтинов // Акуш. гинекол. 2010. № 6. С. 10–15.
  4. Павлов К.А., Дубова Е.А., Щеголев А.И. Фетоплацентарный ангиогенез при нормальной беременности: роль сосудистого эндотелиального фактора роста // Акуш. гинекол. 2011. № 3. С. 11–16.
  5. Туманова У.Н., Ляпин В.М., Щеголев А.И. Патология плаценты при двойне // Соврем. пробл. науки образ. 2017. № 5. С. 56.
  6. Фролова Е.Р., Гладкова К.А., Туманова У.Н. и др. Морфологическая характеристика плаценты при монохориальной диамниотической двойне, осложненной синдромом селективной задержки роста плода // Пробл. репрод. 2023. Т. 29 (1). С. 79–85.
  7. Ходжаева З.С., Шмаков Р.Г., Коган Е.А. и др. Клинико-анамнестические особенности, плацента и плацентарная площадка при ранней и поздней преэклампсии // Акуш. гинекол. 2015. № 4. С. 25–31.
  8. Щеголев А.И. Современная морфологическая классификация повреждений плаценты // Акуш. гинекол. 2016. № 4. С. 16–23.
  9. Щеголев А.И., Туманова У.Н. Патология плаценты при задержке роста плода // Междунар. журн. прикл. фунд. иссл. 2017. Т. 12 (2). С. 297–301.
  10. Щеголев А.И., Серов В.Н. Клиническая значимость поражений плаценты // Акуш. гинекол. 2019. № 3. С. 54–62.
  11. Щеголев А.И., Дубова Е.А., Павлов К.А. Морфология плаценты. М.: РЦАГиП, 2010. 46 с.
  12. Щеголев А.И., Павлов К.А., Дубова Е.А., Фролова О.Г. Ранняя неонатальная смертность в Российской Федерации в 2010 г. // Арх. патол. 2013. Т. 75 (4). С. 15–19.
  13. Щеголев А.И., Туманова У.Н., Шувалова М.П., Фролова О.Г. Гипоксия как причина мертворождаемости в Российской Федерации // Здоровье, демография, экология финно-угорских народов. 2014. № 3. С. 96–98.
  14. Щеголев А.И., Туманова У.Н., Ляпин В.М. Нарушения структуры и васкуляризации ворсин плаценты при задержке роста плода // Соврем. пробл. образ. 2018. № 4. С. 12—18.
  15. Щеголев А.И., Туманова У.Н., Ляпин В.М., Серов В.Н. Синцитиотрофобласт ворсин плаценты в норме и при преэклампсии // Акуш. гинекол. 2020. № 6. С. 21–28.
  16. Щеголев А.И., Туманова У.Н., Серов В.Н. Роль плаценты в развитии поражений головного мозга новорожденного // Акуш. гинекол. 2023. № 8. С. 38–47.
  17. Ali K.Z., Burton G.J., Khalid M.E. et al. Concentrations of free vascular endothelial growth factor in the maternal and foetal circulations during pregnancy: a cross-sectional study // J. Matern. Fetal Neonatal. Med. 2010. V. 23. P. 1244–1248.
  18. Bajoria R., Sooranna S.R., Ward S. et al. Placental transport rather than maternal concentration of amino acids regulates fetal growth in monochorionic twins: implications for fetal origin hypothesis // Am. J. Obstet. Gynecol. 2001. V. 185. P. 1239–1246.
  19. Barker D.J. The fetal and infant origins of adult disease // BMJ. 1990. V. 301 (6761). P. 1111.
  20. Bartel D.P. MicroRNAs: genomics, biogenesis, mechanism, and function // Cell. 2004. V. 116 (2). P. 281–297.
  21. Brocato J., Chervona Y., Costa M. Molecular responses to hypoxia-inducible factor 1α and beyond // Mol. Pharmacol. 2014. V. 85 (5). P. 651–657.
  22. Cameo P., Bischof P., Calvo J.C. Effect of leptin on progesterone, human chorionic gonadotropin, and interleukin-6 secretion by human term trophoblast cells in culture1 // Biol. Reprod. 2003. V. 68 (2). P. 472–477.
  23. Chan M.P., Hecht J.L., Kane S.E. Incidence and clinicopathologic correlation of fetal vessel thrombosis in mono- and dichorionic twin placentas // J. Perinatol. 2010. V. 30 (10). P. 660–664.
  24. Chang Y.-L., Wang C.-N., Wei P.-C. et al. Mitochondrial activation in the growth-restricted fetus of monochorionic twins // Fertil Steril. 2013. V. 100 (1). P. 241–246.e1–2.
  25. Chang Y.-L., Chao A.-S., Peng H.-H. et al. Effects of inter-twin vascular anastomoses of monochorionic twins with selective intrauterine growth restriction on the contents of placental mitochondria DNA // BMC Pregn. Childbirth. 2018. V. 18 (1). P. 74.
  26. Clark D.E., Smith S.K., Sharkey A.M., Charnock-Jones D.S. Localization of VEGF and expression of its receptors flit and KDR in human placenta throughout pregnancy // Hum. Reprod. 1996. V. 11 (5). P. 1090–1098.
  27. Cosmi E., Visentin S., Favretto D. et al. Selective intrauterine growth restriction in monochorionic twin pregnancies: markers of endothelial damage and metabolomic profile // Twin Res. Hum. Genet. 2013. V. 16 (4). P. 816–826.
  28. Diplas A.I., Lambertini L., Lee M.-J. et al. Differential expression of imprinted genes in normal and IUGR human placentas // Epigenetics. 2009. V. 4 (4). P. 235–240.
  29. Dröge L., Herraìz I., Zeisler H. et al. Maternal serum sFlt-1/PlGF ratio in twin pregnancies with and without pre-eclampsia in comparison with singleton pregnancies // Ultrasound Obstet. Gynecol. 2015. V. 45 (3). P. 286–293.
  30. Dubova E.A., Pavlov K.A., Lyapin V.M. et al. Vascular endothelial growth factor and its receptors in the placental villi of pregnant patients with pre-eclampsia // Bull. Exp. Biol. Med. 2013. V. 154 (6). P. 792– 795.
  31. El Emrani S., Groene S.G., Verweij E.J. et al. Gestational age at birth and outcome in monochorionic twins with different types of selective fetal growth restriction: a systematic literature review // Prenat. Diagn. 2022. V. 42 (9). P. 1094–1110.
  32. Emmrich P. Pathology of the placenta. XI. Feto-fetal transfusion syndrome // Zentralbl. Pathol. 1992. V. 138. P. 255–259.
  33. Ferrara N., Houck K., Jakeman L., Leung D.W. Molecular and biological properties of the vascular endothelial growth factor family of proteins // Endocr. Rev. 1992. V. 13 (1). P. 18–32.
  34. Galea P., Barigye O., Wee L. et al. The placenta contributes to activation of the renin angiotensin system in twin–twin transfusion syndrome // Placenta. 2008. V. 29 (8). P. 734–742.
  35. Ge L., Wang Y., Cao Y. et al. MiR-429 improved the hypoxia tolerance of human amniotic cells by targeting HIF-1α // Biotechnol. Lett. 2018. V. 40 (11–12). P. 1477–1486.
  36. Glinianaia S.V., Rankin J., Khalil A. et al. Prevalence, antenatal management and perinatal outcome of monochorionic monoamniotic twin pregnancy: a collaborative multicenter study in England, 2000–2013 // Ultrasound Obstet. Gynecol. 2019. V. 53 (2). P. 184–192.
  37. Gluckman P.D., Hanson M.A., Beedle A.S. Early life events and their consequences for later disease: a life history and evolutionary perspective // Am. J. Hum. Biol. 2007. V. 19 (1). P. 1–19.
  38. Gou C., Liu X., Shi X. et al. Placental expressions of CDKN1C and KCNQ1OT1 in monozygotic twins with selective intrauterine growth restriction // Twin Res. Hum. Genet. 2017. V. 20 (5). P. 389–394.
  39. Gratacós E., Lewi L., Muñoz B. 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. V. 30 (1). P. 28–34.
  40. Green B.B., Houseman E.A., Johnson K.C. et al. Hydroxymethylation is uniquely distributed within term placenta, and is associated with gene expression // FASEB J. 2016. V. 30 (8). P. 2874–2884.
  41. Groene S.G., Tollenaar L.S.A., van Klink J.M.M. et al. Twin–twin transfusion syndrome with and without selective fetal growth restriction prior to fetoscopic laser surgery: short and long-term outcome // J. Clin. Med. 2019. V. 8 (7). P. 969.
  42. Groene S.G., Openshaw K.M., Jansén-Storbacka L.R. et al. Impact of placental sharing and large bidirectional anastomoses on birthweight discordance in monochorionic twins: a retrospective cohort study in 449 cases // Am. J. Obstet. Gynecol. 2022. V. 227 (5). P. 755.e1–755.e10.
  43. He Z., Lu H., Luo H. et al. The promoter methylomes of monochorionic twin placentas reveal intrauterine growth restriction-specific variations in the methylation patterns // Sci. Rep. 2016. V. 6 (1). P. 20181.
  44. Horgan R.P., Broadhurst D.I., Dunn W.B. et al. Changes in the metabolic footprint of placental explant-conditioned medium cultured in different oxygen tensions from placentas of small for gestational age and normal pregnancies // Placenta. 2010. V. 31 (10). P. 893–901.
  45. Huang X., Le Q.-T., Giaccia A.J. MiR-210 – micromanager of the hypoxia pathway // Trends Mol. Med. 2010. V. 16 (5). P. 230–237.
  46. Jackson M.R., Carney E.W., Lye S.J., Ritchie J.W. Localization of two angiogenic growth factors (PDECGF and VEGF) in human placentae throughout gestation // Placenta. 1994. V. 15 (4). P. 341–353.
  47. Khaliq A., Li X.F., Shams M. et al. Localisation of placenta growth factor (PlGF) in human term placenta // Growth Factors. 1996. V. 13 (3–4). P. 243–250.
  48. Kozinszky Z., Surányi A. The high-risk profile of selective growth restriction in monochorionic twin pregnancies // Medicina (Kaunas). 2023. V. 59 (4). P. 1–16.
  49. Kumazaki K., Nakayama M., Suehara N., Wada Y. Expression of vascular endothelial growth factor, placental growth factor, and their receptors Flt-1 and KDR in human placenta under pathologic conditions // Hum. Pathol. 2002. V. 33 (11). P. 1069–1077.
  50. Lattuada D., Colleoni F., Martinelli A. et al. Higher mitochondrial DNA content in human IUGR placenta // Placenta. 2008. V. 29 (12). P. 1029–1033.
  51. Lee H.C., Yin P.H., Lu C.Y. et al. Increase of mitochondria and mitochondrial DNA in response to oxidative stress in human cells // Biochem. J. 2000. V. 348 (2). P. 425–432.
  52. Lee P., Chandel N.S., Simon M.C. Cellular adaptation to hypoxia through hypoxia inducible factors and beyond // Nat. Rev. Mol. Cell Biol. 2020. V. 21 (5). P. 268–283.
  53. Lee S.-A., Ding C. The dysfunctional placenta epigenome: causes and consequences // Epigenomics. 2012. V. 4 (5). P. 561–569.
  54. Levytska K., Kingdom J., Baczyk D., Drewlo S. Heme oxygenase-1 in placental development and pathology // Placenta. 2013. V. 34 (4). P. 291–298.
  55. Lewi L., van Schoubroeck D., Gratacós E. et al. Monochorionic diamniotic twins: complications and management options // Curr. Opin. Obstet. Gynecol. 2003. V. 15 (2). P. 177–194.
  56. Lewi L., Cannie M., Blickstein I. et al. Placental sharing, birthweight discordance, and vascular anastomoses in monochorionic diamniotic twin placentas // Am. J. Obstet. Gynecol. 2007. V. 197 (6). P. 587.e1–587.e8.
  57. Lewi L., Gucciardo L., Huber A. et al. Clinical outcome and placental characteristics of monochorionic diamniotic twin pairs with early- and late-onset discordant growth // Am. J. Obstet. Gynecol. 2008. V. 199 (5). P. 511.e1–511.e7.
  58. Li L., Huang X., He Z. et al. miRNA‐210‐3p regulates trophoblast proliferation and invasiveness through fibroblast growth factor 1 in selective intrauterine growth restriction // J. Cell. Mol. Med. 2019. V. 23 (6). P. 4422–4433.
  59. Lim L.P., Lau N.C., Garrett-Engele P. et al. Microarray analysis shows that some microRNAs downregulate large numbers of target mRNAs // Nature. 2005. V. 433 (7027). P. 769–773.
  60. Ma M., Zhou Q.J., Xiong Y. et al. Preeclampsia is associated with hypermethylation of IGF-1 promoter mediated by DNMT1 // Am. J. Transl. Res. 2018. V. 10 (1). P. 16–39.
  61. Maglione D., Guerriero V., Viglietto G. et al. Isolation of a human placenta cDNA coding for a protein related to the vascular permeability factor // PNAS USA. 1991. V. 88 (20). P. 9267–9271.
  62. Mayhew T., Charnock-Jones D., Kaufmann P. Aspects of human fetoplacental vasculogenesis and angiogenesis. III. Changes in complicated pregnancies // Placenta. 2004. V. 25 (2–3). P. 127–139.
  63. Meng M., Cheng Y.K.Y., Wu L. et al. Whole genome miRNA profiling revealed miR-199a as potential placental pathogenesis of selective fetal growth restriction in monochorionic twin pregnancies // Placenta. 2020. V. 92. P. 44–53.
  64. Monaghan C., Kalafat E., Binder J. et al. Prediction of adverse pregnancy outcome in monochorionic diamniotic twin pregnancy complicated by selective fetal growth restriction // Ultrasound Obstet. Gynecol. 2019. V. 53 (2). P. 200–207.
  65. Morikawa M., Yamada T., Yamada T. et al. Prospective risk of intrauterine fetal death in monoamniotic twin pregnancies // Twin Res. Hum. Genet. 2012. V. 15 (4). P. 522–526.
  66. Morine M., Nobunaga T., Mizutani T. et al. Vascular endothelial growth factor in monochorionic twins with twin–twin transfusion syndrome // J. Endocrinol. Invest. 2008. V. 31 (11). P. 966–970.
  67. Morley R., Dwyer T., Carlin J.B. Studies of twins: can they shed light on the fetal origins of adult disease hypothesis? // Twin Res. 2003. V. 6 (6). P. 520–525.
  68. Nakayama S., Ishii K., Kawaguchi H. et al. Perinatal outcome of monochorionic diamniotic twin pregnancies managed from early gestation at a single center // J. Obstet. Gynaecol. Res. 2012. V. 38 (4). P. 692–697.
  69. Nikkels P.G., Hack K.E., van Gemert M.J. Pathology of twin placentas with special attention to monochorionic twin placentas // J. Clin. Pathol. 2008. V. 61 (12). P. 1247–1253.
  70. Oldenburg A., Rode L., Bødker B. et al. Influence of chorionicity on perinatal outcome in a large cohort of Danish twin pregnancies // Ultrasound Obstet. Gynecol. 2012. V. 39 (1). P. 69–74.
  71. Pandey K., Dubay P., Bhagoliwal A. et al. Hyperhomocysteinemia as a risk factor for IUGR // J. Obstet. Gynaecol. India. 2012. V. 62 (4). P. 406–408.
  72. Paolini C.L., Marconi A.M., Ronzoni S. et al. Placental transport of leucine, phenylalanine, glycine, and proline in intrauterine growth-restricted pregnancies // J. Clin. Endocrinol. Metab. 2001. V. 86 (11). P. 5427–5432.
  73. Parrott M.S., von Versen-Hoeynck F., Ness R.B. et al. System A amino acid transporter activity in term placenta is substrate specific and inversely related to amino acid concentration // Reprod. Sci. 2007. V. 14 (7). P. 687–693.
  74. Pe’er J., Shweiki D., Itin A. et al. Hypoxia-induced expression of vascular endothelial growth factor by retinal cells is a common factor in neovascularizing ocular diseases // Lab. Invest. 1995. V. 72. P. 638–664.
  75. Rana S., Burke S.D., Karumanchi S.A. Imbalances in circulating angiogenic factors in the pathophysiology of preeclampsia and related disorders // Am. J. Obstet. Gynecol. 2022. V. 226 (2). P. 1019–1034.
  76. Redline R.W., Pappin A. Fetal thrombotic vasculopathy: the clinical significance of extensive avascular villi // Hum. Pathol. 1995. V. 26 (1). P. 80–85.
  77. Roberts J.M., Rajakumar A. Preeclampsia and soluble fms-like tyrosine kinase 1 // J. Clin. Endocrinol. Metab. 2009. V. 94 (7). P. 2252–2254.
  78. Salmaso N., Jablonska B., Scafidi J. et al. Neurobiology of premature brain injury // Nat. Neurosci. 2014. V. 17 (3). P. 341–346.
  79. Samanta D., Prabhakar N.R., Semenza G.L. Systems biology of oxygen homeostasis // Wiley Interdiscip. Rev. Syst. Biol. Med. 2017. V. 9 (4). P. e1382.
  80. Schrey S., Kingdom J., Baczyk D. et al. Leptin is differentially expressed and epigenetically regulated across monochorionic twin placenta with discordant fetal growth // Mol. Hum. Reprod. 2013. V. 19 (11). P. 764–772.
  81. Semenza G.L. Hydroxylation of HIF-1: oxygen sensing at the molecular level // Physiology (Bethesda). 2004. V. 19 (4). P. 176–182.
  82. Shchyogolev A.I., Dubova E.A., Pavlov K.A. et al. Morphometric characteristics of terminal villi of the placenta in pre-eclampsia // Bull. Exp. Biol. Med. 2012. V. 154 (1). P. 92–95.
  83. Shchegolev A.I., Tumanova U.N., Lyapin V.M. et al. Complex method of CT and morphological examination of placental angioarchitechtonics // Bull. Exp. Biol. Med. 2020. V. 169 (3). P. 405–411.
  84. Steffensen T.S., Gilbert-Barness E., Spellacy W., Quintero R.A. Placental pathology in trap sequence: clinical and pathogenetic implications // Fetal Pediatr. Pathol. 2008. V. 27 (1). P. 13–29.
  85. Sun L.-M., Li Y., Zou G. et al. Monochorionic twins with unequal placental sharing: why can the outcome still be favorable? // J. Matern. Fetal Neonatal. Med. 2016. V. 29 (8). P. 1261–1264.
  86. Townsend R., D’Antonio F., Sileo F.G. et al. Perinatal outcome of monochorionic twin pregnancy complicated by selective fetal growth restriction according to management: systematic review and meta‐analysis // Ultrasound Obstet. Gynecol. 2019. V. 53 (1). P. 36–46.
  87. Valsky D.V., Eixarch E., Martinez J.M. et al. Selective intrauterine growth restriction in monochorionic twins: pathophysiology, diagnostic approach and management dilemmas // Semin. Fetal Neonatal. Med. 2010. V. 15 (6). P. 342–348.
  88. Verma S., Pillay P., Naicker T. et al. Placental hypoxia inducible factor-1α & CHOP immuno-histochemical expression relative to maternal circulatory syncytiotrophoblast microvesicles in preeclamptic and normotensive pregnancies // Eur. J. Obstet. Gynecol. Reprod. Biol. 2018. V. 220. P. 18–24.
  89. Vuorela P., Hatva E., Lymboussaki A. et al. Expression of vascular endothelial growth factor and placenta growth factor in human placental // Biol. Reprod. 1997. V. 56 (2). P. 489–494.
  90. Wang L., Han T.-L., Luo X. et al. Metabolic biomarkers of monochorionic twins complicated with selective intrauterine growth restriction in cord plasma and placental tissue // Sci. Rep. 2018. V. 8 (1). P. 15914.
  91. Wang X., Li L., Yuan P. et al. Comparison of pregnancy outcomes and placental characteristics between selective fetal growth restriction with and without thick arterio-arterial anastomosis in monochorionic diamniotic twins // BMC Pregn. Childbirth. 2022. V. 22 (1). P. 15.
  92. Wee L.Y., Sebire N.J., Bhundia J. et al. Histomorphometric characterisation of shared and non-shared cotyledonary villus territories of monochorionic placentae in relation to pregnancy complications // Placenta. 2006. V. 27 (4–5). P. 475–482.
  93. Yang L., Shao H., Yuan P.-B. et al. Expressions of HIF-α and its target gene in monochorionic twin placentas with twin–twin transfusion syndrome // Beijing Da Xue Xue Bao Yi Xue Ban. 2011. V. 43. P. 792–797.
  94. Zhang G.-L., He Z.-M., Shi X.-M. et al. Discordant HIF1A mRNA levels and oxidative stress in placental shares of monochorionic twins with selective intra-uterine growth restriction // Placenta. 2015. V. 36 (3). P. 297–303.
  95. Zhou Y., McMaster M., Woo K. et al. Vascular endothelial growth factor ligands and receptors that regulate human cytotrophoblast survival are dysregulated in severe preeclampsia and hemolysis, elevated liver enzymes, and low platelets syndrome // Am. J. Pathol. 2002. V. 160 (4). P. 1405–1423.

Supplementary files

Supplementary Files
Action
1. JATS XML

Copyright (c) 2024 Russian Academy of Sciences