Nuchal Edema and Venous-Lymphatic Phenotype Disturbance in Human Fetuses and Mouse Embryos With Aneuploidy

Mireille N. Bekker, Nynke M.S. van den Akker, Margot M. Bartelings, Jenny B. Arkesteijn, Sigrid G.L. Fischer, Japke A.E. Polman, Monique C. Haak, Sandra Webb, Robert E. Poelmann, John M.G. van Vugt, Adriana C. Gittenberger-de Groot*

*Corresponding author for this work

Research output: Contribution to journalArticleAcademicpeer-review

26 Citations (Scopus)

Abstract

Objective: Nuchal edema (NE) is a clinical indicator for aneuploidy, cardiovascular anomalies, and several genetic syndromes. Its etiology, however, is unknown. In the nuchal area, the endothelium of the jugular lymphatic sacs (JLS) develops by budding from the blood vascular endothelium of the cardinal veins. Abnormal distension of the jugular sacs is associated with NE. We hypothesize that a disturbed lymphatic endothelial differentiation and sac formation causes NE. We investigated endothelial differentiation of the jugular lymphatic system in human and mouse species with NE. Methods: Aneuploid human fetuses (trisomy 21; trisomy 18) were compared with euploid controls (gestational age 12 to 18 weeks). Trisomy 16 mouse embryos were compared with wild type controls (embryonic day 10 to 18). Trisomy 16 mice are considered an animal model for human trisomy 21. Endothelial differentiation was investigated by immunohistochemistry using lymphatic markers (prox-1, podoplanin, lymphatic vessel endothelial hyaluronan receptor [LYVE]-1) and en blood vessel markers (neuropilin [NP]-1 and ligand vascular endothelial growth factor [VEGF]-A). Smooth muscle actin (SMA) was included as a smooth muscle cell marker. Results: We report a disturbed venous-lymphatic phenotype in aneuploid human fetuses and mouse embryos with enlarged jugular sacs and NE. Our results show absent or diminished expression of the lymphatic markers Prox-1 and podoplanin in the enlarged jugular sac, while LYVE-1 expression was normal. Additionally, the enlarged JLS showed blood vessel characteristics, including increased NP-1 and VEGF-A expression. The lumen contained blood cells and smooth muscle cells lined the wall. Conclusion: A loss of lymphatic identity seems to be the underlying cause for clinical NE. Also, abnormal endothelial differentiation provides a link to the cardiovascular anomalies associated with NE.

Original languageEnglish
Pages (from-to)209-216
Number of pages8
JournalJournal of the Society for Gynecologic Investigation
Volume13
Issue number3
DOIs
Publication statusPublished - 1 Apr 2006

Keywords

  • endothelial differentiation
  • jugular lymphatic sac
  • lymphangiogenesis
  • Nuchal translucency
  • pathophysiology

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