Etiology- and region-specific characteristics of transependymal cerebrospinal fluid flow

Peter H. YangDepartment of Neurological Surgery, Washington University School of Medicine, St. Louis;

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Alison Almgren-BellDepartment of Neurological Surgery, Washington University School of Medicine, St. Louis;

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Hongjie GuDivision of Biostatistics, Washington University in St. Louis, Missouri; and

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Anna V. DowlingDepartment of Neurological Surgery, Washington University School of Medicine, St. Louis;

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Sangami PugazenthiDepartment of Neurological Surgery, Washington University School of Medicine, St. Louis;

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Kimberly MackeyDepartment of Neurological Surgery, Children’s Hospital of The King’s Daughters, Norfolk, Virginia

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Esther B. DupépéDepartment of Neurological Surgery, Washington University School of Medicine, St. Louis;

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Jennifer M. StrahleDepartment of Neurological Surgery, Washington University School of Medicine, St. Louis;

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OBJECTIVE

Transependymal flow (TEF) of CSF, often delineated as T2-weighted hyperintensity adjacent to the lateral ventricles on MRI, is a known imaging finding, usually in the setting of CSF flow disturbances. Specific radiological features of TEF and their relationships with clinical markers of hydrocephalus and underlying disease pathology are not known. Here, the authors describe the radiological features and clinical associations of TEF with implications for CSF circulation in the setting of intracranial pathology.

METHODS

After obtaining IRB review and approval, the authors reviewed the radiological records of all patients who underwent intracranial imaging with CT or MRI at St. Louis Children’s Hospital, St. Louis, Missouri, between 2008 and 2019 to identify individuals with TEF. Then, under direct review of imaging, TEF pattern, degree, and location and underlying pathology and other radiological and clinical features pertaining to CSF circulation and CSF disturbances were noted.

RESULTS

TEF of CSF was identified in 219 patients and was most prevalent in the setting of neoplasms (72%). In 69% of the overall cohort, TEF was seen adjacent to the anterior aspect of the frontal horns and the posterior aspect of the occipital horns of the lateral ventricles, and nearly half of these patients also had TEF dorsal to the third ventricle near the splenium of the corpus callosum. This pattern was independently associated with posterior fossa medulloblastoma when compared with pilocytic astrocytoma (OR 4.75, 95% CI 1.43–18.53, p = 0.0157). Patients with congenital or neonatal-onset hydrocephalus accounted for 13% of patients and were more likely to have TEF circumferentially around the ventricles without the fronto-occipital distribution. Patients who ultimately required permanent CSF diversion surgery were more likely to have the circumferential TEF pattern, a smaller degree of TEF, and a lack of papilledema at the time of CSF diversion surgery.

CONCLUSIONS

CSF transmigration across the ependyma is usually restricted to specific periventricular regions and is etiology specific. Certain radiological TEF characteristics are associated with tumor pathology and may reflect impaired or preserved ependymal fluid handling and global CSF circulation. These findings have implications for TEF as a disease-specific marker and in understanding CSF handling within the brain.

ABBREVIATIONS

EVD = external ventricular drain; FO = fronto-occipital; FOHR = FO horn ratio; IVH = intraventricular hemorrhage; PHH = posthemorrhagic hydrocephalus; TEF = transependymal flow.

Supplementary Materials

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Image from Tran et al. (pp 394–399).

  • 1

    Isaacs AM, Riva-Cambrin J, Yavin D, et al. Age-specific global epidemiology of hydrocephalus: systematic review, metanalysis and global birth surveillance. PLoS One. 2018;13(10):e0204926.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Naidich TP, Epstein F, Lin JP, Kricheff II, Hochwald GM. Evaluation of pediatric hydrocephalus by computed tomography. Radiology. 1976;119(2):337345.

  • 3

    James AE Jr, Strecker EP, Sperber E, Flor WJ, Merz T, Burns B. An alternative pathway of cerebrospinal fluid absorption in communicating hydrocephalus. Transependymal movement. Radiology. 1974;111(1):143146.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Weller RO, Mitchell J. Cerebrospinal fluid edema and its sequelae in hydrocephalus. Adv Neurol. 1980;28:111123.

  • 5

    Sahar A, Hochwald GM, Sadik AR, Ransohoff J. Cerebrospinal fluid absorption in animals with experimental obstructive hydrocephalus. Arch Neurol. 1969;21(6):638644.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Bowsher D. Pathways of absorption of protein from the cerebrospinal fluid: an autoradiographic study in the cat. Anat Rec. 1957;128(1):2339.

  • 7

    Bering EA Jr, Sato O. Hydrocephalus: changes in formation and absorption of cerebrospinal fluid within the cerebral ventricles. J Neurosurg. 1963;20(12):10501063.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Kim H, Jeong EJ, Park DH, et al. Finite element analysis of periventricular lucency in hydrocephalus: extravasation or transependymal CSF absorption?. J Neurosurg. 2016;124(2):334341.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9

    Moseley IF, Radü EW. Factors influencing the development of periventricular lucencies in patients with raised intracranial pressure. Neuroradiology. 1979;17(2):6569.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Asada M, Tamaki N, Kanazawa Y, et al. Computer analysis of periventricular lucency on the CT scan. Neuroradiology. 1978;16(1):207211.

  • 11

    O’Hayon BB, Drake JM, Ossip MG, Tuli S, Clarke M. Frontal and occipital horn ratio: a linear estimate of ventricular size for multiple imaging modalities in pediatric hydrocephalus. Pediatr Neurosurg. 1998;29(5):245249.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Gideon P, Thomsen C, Gjerris F, Sørensen PS, Henriksen O. Increased self-diffusion of brain water in hydrocephalus measured by MR imaging. Acta Radiol. 1994;35(6):514519.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Sørensen PS, Thomsen C, Gjerris F, Henriksen O. Brain water accumulation in pseudotumour cerebri demonstrated by MR-imaging of brain water self-diffusion. In: Reulen HJ, Baethmann A, Fenstermacher J, Marmarou A, Spatz M, eds.Brain Edema VIII. Springer;1990:363365.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14

    Liedtke W, Choe Y, Martí-Renom MA, et al. Vanilloid receptor-related osmotically activated channel (VR-OAC), a candidate vertebrate osmoreceptor. Cell. 2000;103(3):525535.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Stadlbauer A, Salomonowitz E, van der Riet W, Buchfelder M, Ganslandt O. Insight into the patterns of cerebrospinal fluid flow in the human ventricular system using MR velocity mapping. Neuroimage. 2010;51(1):4252.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    D’Gama PP, Qiu T, Cosacak MI, et al. Diversity and function of motile ciliated cell types within ependymal lineages of the zebrafish brain. Cell Rep. 2021;37(1):109775.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Lehtinen MK, Zappaterra MW, Chen X, et al. The cerebrospinal fluid provides a proliferative niche for neural progenitor cells. Neuron. 2011;69(5):893905.

  • 18

    Lehtinen MK, Bjornsson CS, Dymecki SM, Gilbertson RJ, Holtzman DM, Monuki ES. The choroid plexus and cerebrospinal fluid: emerging roles in development, disease, and therapy. J Neurosci. 2013;33(45):1755317559.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 19

    Sawamoto K, Wichterle H, Gonzalez-Perez O, et al. New neurons follow the flow of cerebrospinal fluid in the adult brain. Science. 2006;311(5761):629632.

  • 20

    Kim HS, Park JB, Gwak HS, Kwon JW, Shin SH, Yoo H. Clinical outcome of cerebrospinal fluid shunts in patients with leptomeningeal carcinomatosis. World J Surg Oncol. 2019;17(1):59.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Foreman P, McClugage S III, Naftel R, et al. Validation and modification of a predictive model of postresection hydrocephalus in pediatric patients with posterior fossa tumors. J Neurosurg Pediatr. 2013;12(3):220226.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Domínguez-Pinos MD, Páez P, Jiménez AJ, et al. Ependymal denudation and alterations of the subventricular zone occur in human fetuses with a moderate communicating hydrocephalus. J Neuropathol Exp Neurol. 2005;64(7):595604.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Ibañez-Tallon I, Pagenstecher A, Fliegauf M, et al. Dysfunction of axonemal dynein heavy chain Mdnah5 inhibits ependymal flow and reveals a novel mechanism for hydrocephalus formation. Hum Mol Genet. 2004;13(18):21332141.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Baas D, Meiniel A, Benadiba C, et al. A deficiency in RFX3 causes hydrocephalus associated with abnormal differentiation of ependymal cells. Eur J Neurosci. 2006;24(4):10201030.

    • Crossref
    • PubMed
    • Search Google Scholar
    • Export Citation

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