Skip to main content

Advertisement

SpringerLink
Log in

Site- and stage-dependent differences in vascular density of the human fetal brain

  • Original Paper
  • Published:
Child's Nervous System Aims and scope Submit manuscript

Abstract

Background and purpose

Less information is available about site-dependent differences in fetal intrabrain angiogenesis. Quantitative evaluation is especially limited, with the measured area limited to the cerebral gray and white matters and the periventricular germinal matrix.

Patients and methods

We measured vascular density (number of vessels per square millimeter) and percent vascular area (percentage of areas occupied by vessels) of CD34-positive microvessels in 14 human fetal brains, including 4 fetuses at 14–16 weeks of gestation, 5 at 25–28 weeks, and 5 at 35–37 weeks. Site-dependent differences were examined among the cerebral cortex, thalamus, internal capsule, corpus callosum, ganglionic eminence, midbrain, and cerebellar cortex and nuclei.

Results

The parameters examined tended to be high in the cerebral germinal matrix, thalamus, midbrain, and cerebellum. Significant site-dependent differences were observed: lower vascular densities were observed in the internal capsule and corpus callosum than in other parts of the brain (p < 0.05) and a larger percent area was observed in the cerebellar nuclei than in other areas. Vascular density was higher during the early than late stage because of the larger numbers of CD34-positive islands of cells in the early stage, although there were several exceptions. Percent area was not stage dependent but was almost constant at many sites.

Conclusion

Consequently, except for developing nuclei, the prenatal development of intrabrain vessels after 15 weeks may proceed without any significant changes in density.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  1. Padget DH (1948) The development of cranial arteries in the human embryo. Contrib Embryol 212:205–271

    Google Scholar 

  2. Padget DH (1956) The cranial venous system in man in reference to development, adult configuration, and relation to the arteries. Am J Anat 98:307–355

    Article  CAS  PubMed  Google Scholar 

  3. Raybaud C (2010) Normal and abnormal embryology and development of the intracranial vascular system. Neurosurg Clin N Am 21:399–426

    Article  PubMed  Google Scholar 

  4. Ballabh P, Braun A, Nedergaard M (2004) Anatomic analysis of blood vessles in germinal matrix, cerebral cortex, and white matter in developing infants. Pediatr Res 56:117–124

    Article  PubMed  Google Scholar 

  5. Ulfig N, Neudörfer F, Bohl J (2000) Transient structures of the human fetal brain: subplate, thalamic reticular complex, ganglionic eminence. Histol Histopathol 15:7771–7790

    Google Scholar 

  6. Bystron I, Blakemore C, Rakic P (2008) Development of the human cerebral cortex: Boulder Committee revisited. Nat Rev Neurosci 9:110–122

    Article  CAS  PubMed  Google Scholar 

  7. Kuban KC, Gilles FH (1985) Human telencephalic angiogenesis. Ann Neurol 17:539–548

    Article  CAS  PubMed  Google Scholar 

  8. Marinkoviċ R, Markoviċ L (1990) Stereological analysis of the vascular network of the ganglionic eminence and the corpus striatum during brain development in man (Croatian). Med Pregl 43:13–15

    PubMed  Google Scholar 

  9. Nakamura Y, Okudera T, Hashimoto T (1994) Vascular architecture in white matter of neonates: its relationship to periventricular leukomalacia. J Neuropathol Exp Neurol 53:582–589

    Article  CAS  PubMed  Google Scholar 

  10. Okudera T, Huang YP, Fukusumi A, Nakamura Y, Hatazawa J, Uremura K (1999) Micro-angiographical studies of the medullary venous system of the cerebral hemispheres. Neuropathology 19:93–111

    Article  CAS  PubMed  Google Scholar 

  11. Rahmah NN, Sakai K, Li Y, Sano K, Hongo K (2012) Comparison of manual and digital microvascular density counting of RECK expression in glioma. Neuropathology 32:245–251

    Article  PubMed  Google Scholar 

  12. Miyawaki T, Matsui K, Takashima S (1998) Developmental characteristics of vessel density in the human fetal and infant brains. Early Hum Dev 53:65–72

    Article  CAS  PubMed  Google Scholar 

  13. Netto GC, Bleil CB, Hilbig A, Coutinho LM (2008) Immunohistochemical evaluation of the microvascular density through the expression of TGF-beta (CD 105/endoglin) and CD34 receptors and expression of the vascular endothelial growth factor (VEGF) in oligodendrogliomas. Neuropathology 28:17–23

    Article  PubMed  Google Scholar 

  14. Rotondo F, Sharma S, Scheithauer BW, Horvath E, Syro LV, Cusimano M, Nassiri F, Yousef GM (2010) Endoglin and CD-34 immunoreactivity in the assessment of microvessel density in normal pituitary and adenoma subtypes. Neoplasma 57:590–593

    Article  CAS  PubMed  Google Scholar 

  15. Vinukonda G, Dummula K, Malik S, Hu F, Thompson CI, Csiszar A, Ungvari Z, Ballabh P (2010) Effect of glucocorticoids on cerebral vasculature of the developing brain. Stroke 41:1766–1773

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  16. Mahzouni P, Mohammadizadeh F, Mougouei K, Moghaddam NA, Chehrei A, Mesbah A (2010) Determining the relationship between “microvascular density” and different grades of astrocytoma based on immunohistochemistry for “factor VIII-related antigen” (von Willebrand factor) expression in tumor microvessels. Indian J Pathol Microbiol 53:605–610

    Article  PubMed  Google Scholar 

  17. Holley JE, Newcombe J, Whatmore JL, Gutowski NJ (2010) Increase blood vessel density and endothelial cell proliferation in multiple sclerosis cerebral white matter. Neurosci Lett 470:65–70

    Article  CAS  PubMed  Google Scholar 

  18. Mito T, Konomi H, Houdou S, Takashima S (1991) Immunohistochemical study of the vasculature in the developing brain. Pediatr Neurol 7:18–22

    Article  CAS  PubMed  Google Scholar 

  19. Abe S, Suzuki M, Cho KH, Murakami G, Cho BH, Ide Y (2011) CD34-positive developing vessels and other structures in human fetuses: an immunohistochemical study. Surg Radiol Anat 33:919–927

    Article  PubMed  Google Scholar 

  20. Katori Y, Kiyokawa H, Kawase T, Murakami G, Cho BH (2011) CD34-positive primitive vessels and fascial structures in the ear, nose and throat of human fetuses: an immunohistochemical study. Acta Otolaryngol 131:1086–1090

    Article  PubMed  Google Scholar 

  21. Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J, Duenzi M, Lucas PA, Black AC Jr (2001) Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 264:51–62

    Article  CAS  PubMed  Google Scholar 

  22. Kopher RA, Penchev VR, Islam MS, Hill KL, Khosla S, Kaufman DS (2010) Human embryonic stem cell-derived CD34+ cells function as MSC progenitor cells. Bone 47:718–728

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  23. Lin CS, Xin ZC, Deng CH, Ning H, Lin G, Lue TF (2010) Defining adipose tissue-derived stem cells in tissue and in culture. Histol Histopathol 25:807–815

    PubMed  Google Scholar 

  24. Miller JL, Watkin KL, Chen MF (2002) Muscle, adipose, and connective tissue variations in intrinsic musculature of the adult human tongue. J Speech Lang Hear Res 45:51–65

    Article  PubMed  Google Scholar 

  25. Norman MG, O’Kusky JR (1986) The groth and development of microvasculature in the human cerebral cortex. J Neuropathol Exp Neurol 45:222–232

    Article  CAS  PubMed  Google Scholar 

  26. Allsopp G, Gamble HJ (1979) Light and electron microscopic observations on the development of the blood vascular system of the human brain. J Anat 128:161–177

    Google Scholar 

  27. Eichmann A, Makinen T, Alitalo K (2005) Neuronal guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev 19:1012–1021

    Article  Google Scholar 

  28. Rakic P, Sidman RL (1970) Histogenesis of cortical layers in human cerebellum, particularly the lamina dissecans. J Comp Neurol 139:473–500

    Article  CAS  PubMed  Google Scholar 

  29. Kollias SS, Ball WS, Prenger EC (1993) Cystic malformations of the posterior fossa: differential diagnosis clarified through embryonic analysis. Radiographics 13:1211–1231

    Article  CAS  PubMed  Google Scholar 

  30. Merrill JD, Piecuch RE, Fell SC, Barkovich AJ, Ruth B (1998) A new pattern of cerebellar hemorrhages in preterm infants. Pediatrics 102:e62–e66

    Article  CAS  PubMed  Google Scholar 

  31. Ballabh P, Hu F, Kumarasiri M, Braun A, Nedergaard M (2005) Development of tight junction molecules in blood vessels of germinal matrix, cerebral cortex, and white matter. Pediatr Res 58:791–798

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Neurology, Wonkwang University School of Medicine, Iksan, Republic of Korea

    Hyuk Chang & Kwang Ho Cho

  2. Department of Anatomy, Tokyo Medical University, Tokyo, Japan

    Shogo Hayashi

  3. Department of Anatomy, Chonbuk National University College of Medicine, Jeonju, Republic of Korea

    Ji Hyun Kim

  4. Department of Anatomy, Akita University School of Medicine, Akita, Japan

    Hiroshi Abe

  5. Department of Anatomy and Embryology II, Faculty of Medicine, Universidad Complutense, Madrid, Spain

    Jose Francisco Rodriguez-Vazquez

  6. Division of Internal Medicine, Iwamizawa Kojin-kai Hospital, Iwamizawa, Japan

    Gen Murakami

  7. Jeonbuk Regional Cardiocerebrovascular Disease Center, Institute of Wonkwang Medical Science, 895, Muwang-ro, Iksan, Jeonbuk, 570-711, Republic of Korea

    Kwang Ho Cho

Authors
  1. Hyuk Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kwang Ho Cho
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Shogo Hayashi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ji Hyun Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hiroshi Abe
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jose Francisco Rodriguez-Vazquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gen Murakami
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kwang Ho Cho.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Chang, H., Cho, K.H., Hayashi, S. et al. Site- and stage-dependent differences in vascular density of the human fetal brain. Childs Nerv Syst 30, 399–409 (2014). https://doi.org/10.1007/s00381-013-2272-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00381-013-2272-8

Keywords

Search

Navigation