Skip to main content

Advertisement

SpringerLink
Log in

Structural and functional connectivity in hydrocephalus: a scoping review

  • Review
  • Published:
Neurosurgical Review Aims and scope Submit manuscript

Abstract

Optimizing the treatment of hydrocephalus remains a major challenge in adult and pediatric neurosurgery. Currently, clinical treatment relies heavily on anatomic imaging of ventricular size and clinical presentation. The emergence of functional and structural brain connectivity imaging has provided the basis for a new paradigm in the management of hydrocephalus. Here we review the pertinent advances in this field. Following PRISMA-ScR guidelines for scoping reviews, we searched PubMed for relevant literature from 1994 to April 2023 using hydrocephalus and MRI-related terms. Included articles reported original MRI data on human subjects with hydrocephalus, while excluding non-English or pre-1994 publications that didn't match the study framework. The review identified 44 studies that investigated functional and/or structural connectivity using various MRI techniques across different hydrocephalus populations. While there is significant heterogeneity in imaging technology and connectivity analysis, there is broad consensus in the literature that 1) hydrocephalus is associated with disruption of functional and structural connectivity, 2) this disruption in cerebral connectivity can be further associated with neurologic compromise 3) timely treatment of hydrocephalus restores both cerebral connectivity and neurologic compromise. The robustness and consistency of these findings vary as a function of patient age, hydrocephalus etiology, and the connectivity region of interest studied. Functional and structural brain connectivity imaging shows potential as an imaging biomarker that may facilitate optimization of hydrocephalus treatment. Future research should focus on standardizing regions of interest as well as identifying connectivity analysis most pertinent to clinical outcome.

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

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

Explore related subjects

Discover the latest articles, news and stories from top researchers in related subjects.

Data availability

No datasets were generated or analysed during the current study.

References

  1. Adam R, Ghahari D, Morton JB, Eagleson R, de Ribaupierre S (2022) Brain network connectivity and executive function in children with infantile hydrocephalus. Brain Connect 12:784–798

    Article  PubMed  Google Scholar 

  2. Air EL, Yuan W, Holland SK, Jones BV, Bierbrauer K, Altaye M, Mangano FT (2010) Longitudinal comparison of pre- and postoperative diffusion tensor imaging parameters in young children with hydrocephalus. J Neurosurg Pediatr 5:385–391

    Article  PubMed  Google Scholar 

  3. Akbari SHA, Limbrick DD Jr, McKinstry RC, Altaye M, Ragan DK, Yuan W, Mangano FT, Holland SK, Shimony JS (2015) Periventricular hyperintensity in children with hydrocephalus. Pediatr Radiol 45:1189–1197

    Article  PubMed  PubMed Central  Google Scholar 

  4. Assaf Y, Ben-Sira L, Constantini S, Chang LC, Beni-Adani L (2006) Diffusion tensor imaging in hydrocephalus: initial experience. AJNR Am J Neuroradiol 27:1717–1724

    CAS  PubMed  PubMed Central  Google Scholar 

  5. Babaeeghazvini P, Rueda-Delgado LM, Gooijers J, Swinnen SP, Daffertshofer A (2021) Brain structural and functional connectivity: a review of combined works of diffusion magnetic resonance imaging and electro-encephalography. Front Hum Neurosci 15:721206

    Article  PubMed  PubMed Central  Google Scholar 

  6. Balédent O, Capel C, Metanbou S, Bouzerar R (2021) Diffusion and flow MR imaging to investigate hydrocephalus patients before and after endoscopic third ventriculostomy. Acta Neurochir Suppl 131:303–306

    Article  PubMed  Google Scholar 

  7. Bastos AM, Schoffelen J-M (2015) A tutorial review of functional connectivity analysis methods and their interpretational pitfalls. Front Syst Neurosci 9:175

    PubMed  Google Scholar 

  8. Ben-Sira L, Goder N, Bassan H, Lifshits S, Assaf Y, Constantini S (2015) Clinical benefits of diffusion tensor imaging in hydrocephalus. J Neurosurg Pediatr 16:195–202

    Article  PubMed  Google Scholar 

  9. Bir SC, Patra DP, Maiti TK, Sun H, Guthikonda B, Notarianni C, Nanda A (2016) Epidemiology of adult-onset hydrocephalus: institutional experience with 2001 patients. Neurosurg Focus 41:E5

    Article  PubMed  Google Scholar 

  10. Buckley RT, Yuan W, Mangano FT, Phillips JM, Powell S, McKinstry RC, Rajagopal A, Jones BV, Holland S, Limbrick DD Jr (2012) Longitudinal comparison of diffusion tensor imaging parameters and neuropsychological measures following endoscopic third ventriculostomy for hydrocephalus. J Neurosurg Pediatr 9:630–635

    Article  PubMed  PubMed Central  Google Scholar 

  11. Caligiuri ME, Quattrone A, Mechelli A, La Torre D, Quattrone A (2022) Semi-automated assessment of the principal diffusion direction in the corpus callosum: differentiation of idiopathic normal pressure hydrocephalus from neurodegenerative diseases. J Neurol 269:1978–1988

    Article  PubMed  Google Scholar 

  12. Fabbro S, Piccolo D, Vescovi MC, Bagatto D, Tereshko Y, Belgrado E, Maieron M, De Colle MC, Skrap M, Tuniz F (2023) Resting-state functional-MRI in iNPH: can default mode and motor networks changes improve patient selection and outcome? Preliminary report. Fluids Barriers CNS 20:7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Froudist-Walsh S, Karolis V, Caldinelli C, Brittain PJ, Kroll J, Rodríguez-Toscano E, Tesse M, Colquhoun M, Howes O, Dell’Acqua F, Thiebaut de Schotten M, Murray RM, Williams SCR, Nosarti C (2015) Very early brain damage leads to remodeling of the working memory system in adulthood: a combined fMRI/Tractography study. J Neurosci 35:15787–15799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Fukuhara T, Luciano MG, Liu JZ, Yue GH (2001) Functional magnetic resonance imaging before and after ventriculoperitoneal shunting for hydrocephalus–case report. Neurol Med Chir 41:626–630

    Article  CAS  Google Scholar 

  15. Ghaffari-Rafi A, Mehdizadeh R, Ghaffari-Rafi S, Leon-Rojas J (2020) Inpatient diagnoses of idiopathic normal pressure hydrocephalus in the United States: demographic and socioeconomic disparities. J Neurol Sci 418:117152

    Article  PubMed  Google Scholar 

  16. Griffa A, Bommarito G, Assal F, Herrmann FR, Van De Ville D, Allali G (2020) Dynamic functional networks in idiopathic normal pressure hydrocephalus: alterations and reversibility by CSF tap test. Hum Brain Mapp 42:1485–1502

    Article  PubMed  PubMed Central  Google Scholar 

  17. Huang W, Fang X, Li S, Mao R, Ye C, Liu W, Deng Y, Lin G (2024) Abnormal characteristic static and dynamic functional network connectivity in idiopathic normal pressure hydrocephalus. CNS Neurosci Ther 30(3):e14178

  18. Huang W, Fang X, Li S, Mao R, Ye C, Liu W, Lin G (2021) Preliminary exploration of the sequence of nerve fiber bundles involvement for idiopathic normal pressure hydrocephalus: a correlation analysis using diffusion tensor imaging. Front Neurosci 15:794046

    Article  PubMed  PubMed Central  Google Scholar 

  19. Isaacs AM, Riva-Cambrin J, Yavin D, Hockley A, Pringsheim TM, Jette N, Lethebe BC, Lowerison M, Dronyk J, Hamilton MG (2018) Age-specific global epidemiology of hydrocephalus: Systematic review, metanalysis and global birth surveillance. PLoS ONE 13:e0204926

    Article  PubMed  PubMed Central  Google Scholar 

  20. Isaacs AM, Smyser CD, Lean RE, Alexopoulos D, Han RH, Neil JJ, Zimbalist SA, Rogers CE, Yan Y, Shimony JS, Limbrick DD Jr (2019) MR diffusion changes in the perimeter of the lateral ventricles demonstrate periventricular injury in post-hemorrhagic hydrocephalus of prematurity. Neuroimage Clin 24:102031

    Article  PubMed  PubMed Central  Google Scholar 

  21. Jang SH, Chang CH, Jung YJ, Lee HD (2017) Recovery of akinetic mutism and injured prefronto-caudate tract following shunt operation for hydrocephalus and rehabilitation: a case report. Medicine 96:e9117

    Article  PubMed  PubMed Central  Google Scholar 

  22. Jang S, Lee H (2018) Change of ascending reticular activating system following shunt operation for hydrocephalus in a subarachnoid hemorrhage patient. J Neurol Surg A Cent Eur Neurosurg 80:62–66

    Article  PubMed  Google Scholar 

  23. Kahle KT, Kulkarni AV, Limbrick DD Jr, Warf BC (2015) Hydrocephalus in children. Lancet 387:788–799

    Article  PubMed  Google Scholar 

  24. Kalpakidou AK, Allin MPG, Walshe M, Giampietro V, McGuire PK, Rifkin L, Murray RM, Nosarti C (2014) Functional neuroanatomy of executive function after neonatal brain injury in adults who were born very preterm. PLoS ONE 9:e113975

    Article  PubMed  PubMed Central  Google Scholar 

  25. Kanno S, Ogawa K-I, Kikuchi H, Toyoshima M, Abe N, Sato K, Miyazawa K, Oshima R, Ohtomo S, Arai H, Shibuya S, Suzuki K (2021) Reduced default mode network connectivity relative to white matter integrity is associated with poor cognitive outcomes in patients with idiopathic normal pressure hydrocephalus. BMC Neurol 21:353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Keong NC, Lock C, Soon S, Hernowo AT, Czosnyka Z, Czosnyka M, Pickard JD, Narayanan V (2022) Diffusion tensor imaging profiles can distinguish diffusivity and neural properties of white matter injury in hydrocephalus vs. non-hydrocephalus using a strategy of a periodic table of DTI elements. Front Neurol 13:868026

    Article  PubMed  PubMed Central  Google Scholar 

  27. Kestle JR (2003) Pediatric hydrocephalus: current management. Neurol Clin 21:883–95.vii

    Article  PubMed  Google Scholar 

  28. Khoo HM, Kishima H, Tani N, Oshino S, Maruo T, Hosomi K, Yanagisawa T, Kazui H, Watanabe Y, Shimokawa T, Aso T, Kawaguchi A, Yamashita F, Saitoh Y, Yoshimine T (2015) Default mode network connectivity in patients with idiopathic normal pressure hydrocephalus. J Neurosurg 124:350–358

    Article  PubMed  Google Scholar 

  29. Kulesz PA, Ware AL, Orkisz JS, Williams VJ, Juranek J, Fletcher JM (2019) Are primary and secondary types of brain anomalies exclusive factors affecting the attention networks in individuals with spina bifida? Neuropsychology 33:1057–1064

    Article  PubMed  Google Scholar 

  30. Kulkarni AV, Donnelly R, Mabbott DJ, Widjaja E (2015) Relationship between ventricular size, white matter injury, and neurocognition in children with stable, treated hydrocephalus. J Neurosurg Pediatr 16:267–274

    Article  PubMed  Google Scholar 

  31. Lean RE, Han RH, Smyser TA, Kenley JK, Shimony JS, Rogers CE, Limbrick DD Jr, Smyser CD (2019) Altered neonatal white and gray matter microstructure is associated with neurodevelopmental impairments in very preterm infants with high-grade brain injury. Pediatr Res 86:365–374

    Article  PubMed  PubMed Central  Google Scholar 

  32. Lenfeldt N, Larsson A, Nyberg L, Andersson M, Birgander R, Eklund A, Malm J (2008) Idiopathic normal pressure hydrocephalus: increased supplementary motor activity accounts for improvement after CSF drainage. Brain 131:2904–2912

    Article  PubMed  Google Scholar 

  33. Lenfeldt N, Larsson A, Nyberg L, Birgander R, Eklund A, Malm J (2011) Diffusion tensor imaging reveals supplementary lesions to frontal white matter in idiopathic normal pressure hydrocephalus. Neurosurgery 68:1586–1593 (discussion 1593)

    Article  PubMed  Google Scholar 

  34. Li Y, Zhao C, Tan Z, Wang Y, Zhang H, Wang J, Guo H, Zeng B, Huang W (2015) Longitudinal changes in the brain following third ventriculostomy in a child with hydrocephalus: a case report. Medicine 94:e2095

    Article  PubMed  PubMed Central  Google Scholar 

  35. Lockwood Estrin G, Kyriakopoulou V, Makropoulos A, Ball G, Kuhendran L, Chew A, Hagberg B, Martinez-Biarge M, Allsop J, Fox M, Counsell SJ, Rutherford MA (2016) Altered white matter and cortical structure in neonates with antenatally diagnosed isolated ventriculomegaly. Neuroimage Clin 11:139–148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Mangano FT, Altaye M, McKinstry RC, Shimony JS, Powell SK, Phillips JM, Barnard H, Limbrick DD Jr, Holland SK, Jones BV, Dodd J, Simpson S, Mercer D, Rajagopal A, Bidwell S, Yuan W (2016) Diffusion tensor imaging study of pediatric patients with congenital hydrocephalus: 1-year postsurgical outcomes. J Neurosurg Pediatr 18:306–319

    Article  PubMed  PubMed Central  Google Scholar 

  37. Mangano FT, Stevenson CB, Nagaraj U, Conley A, Yuan W (2019) Abnormal anisotropic diffusion properties in pediatric myelomeningocele patients treated with fetal surgery: an initial DTI study. Childs Nerv Syst 36:827–833

    Article  PubMed  Google Scholar 

  38. Marumoto K, Koyama T, Hosomi M, Kodama N, Miyake H, Domen K (2012) Diffusion tensor imaging in elderly patients with idiopathic normal pressure hydrocephalus or Parkinson’s disease: diagnosis of gait abnormalities. Fluids Barriers CNS 9:20

    Article  PubMed  PubMed Central  Google Scholar 

  39. Ogata Y, Ozaki A, Ota M, Oka Y, Nishida N, Tabu H, Sato N, Hanakawa T (2017) Interhemispheric resting-state functional connectivity predicts severity of idiopathic normal pressure hydrocephalus. Front Neurosci 11:470

    Article  PubMed  PubMed Central  Google Scholar 

  40. Ou X, Snow JH, Byerley AK, Hall JJ, Glasier CM (2011) Decreased activation and increased lateralization in brain functioning for selective attention and response inhibition in adolescents with spina bifida. Child Neuropsychol 19:23–36

    Article  PubMed  Google Scholar 

  41. Park C-H, Ryu H, Kim C-H, Joa K-L, Kim M-O, Jung H-Y (2020) Injury of corticospinal tract in a patient with subarachnoid hemorrhage as determined by diffusion tensor tractography: a case report. Brain Sci 10(3):177

  42. Smyser CD, Snyder AZ, Shimony JS, Blazey TM, Inder TE, Neil JJ (2013) Effects of white matter injury on resting state fMRI measures in prematurely born infants. PLoS ONE 8:e68098

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Tallus J, Mohammadian M, Kurki T, Roine T, Posti JP, Tenovuo O (2023) A comparison of diffusion tensor imaging tractography and constrained spherical deconvolution with automatic segmentation in traumatic brain injury. Neuroimage Clin 37:103284

    Article  PubMed  Google Scholar 

  44. Tang Y, Yuan X, Duan J, Zhang X, Chen J, Zhou Y, Song F, Zhou D (2021) White matter characteristics of cognitive impairment in tap-test positive idiopathic normal pressure hydrocephalus: a diffusion tensor tract-based spatial study. Front Neurosci 15:774638

    Article  PubMed  PubMed Central  Google Scholar 

  45. Tricco AC, Lillie E, Zarin W, O’Brien KK, Colquhoun H, Levac D, Moher D, Peters MDJ, Horsley T, Weeks L, Hempel S, Akl EA, Chang C, McGowan J, Stewart L, Hartling L, Aldcroft A, Wilson MG, Garritty C, Lewin S, Godfrey CM, Macdonald MT, Langlois EV, Soares-Weiser K, Moriarty J, Clifford T, Tunçalp Ö, Straus SE (2018) PRISMA extension for scoping reviews (PRISMA-ScR): checklist and explanation. Ann Intern Med 169:467–473

    Article  PubMed  Google Scholar 

  46. Wright Z, Larrew TW, Eskandari R (2016) Pediatric hydrocephalus: current state of diagnosis and treatment. Pediatr Rev 37:478–490

    Article  PubMed  Google Scholar 

  47. Yang X, Li H, He W, Lv M, Zhang H, Zhou X, Wei H, Xu B, Chen J, Ma H, Xia J, Yang G (2022) Quantification of changes in white matter tract fibers in idiopathic normal pressure hydrocephalus based on diffusion spectrum imaging. Eur J Radiol 149:110194

    Article  PubMed  Google Scholar 

  48. Yuan W, Holland SK, Shimony JS, Altaye M, Mangano FT, Limbrick DD, Jones BV, Nash T, Rajagopal A, Simpson S, Ragan D, McKinstry RC (2015) Abnormal structural connectivity in the brain networks of children with hydrocephalus. Neuroimage Clin 8:483–492

    Article  PubMed  PubMed Central  Google Scholar 

  49. Yuan W, Mangano FT, Air EL, Holland SK, Jones BV, Altaye M, Bierbrauer K (2009) Anisotropic diffusion properties in infants with hydrocephalus: a diffusion tensor imaging study. AJNR Am J Neuroradiol 30:1792–1798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Yuan W, McKinstry RC, Shimony JS, Altaye M, Powell SK, Phillips JM, Limbrick DD Jr, Holland SK, Jones BV, Rajagopal A, Simpson S, Mercer D, Mangano FT (2012) Diffusion tensor imaging properties and neurobehavioral outcomes in children with hydrocephalus. AJNR Am J Neuroradiol 34:439–445

    Article  PubMed  Google Scholar 

  51. Yuan W, Stevenson CB, Altaye M, Jones BV, Leach J, Lovha M, Rennert N, Mangano FT (2021) Diffusion tensor imaging in children following prenatal myelomeningocele repair and its predictive value for the need and timing of subsequent CSF diversion surgery for hydrocephalus. J Neurosurg Pediatr 27(4):391–399

  52. Zhang H, He W-J, Liang L-H, Zhang H-W, Zhang X-J, Zeng L, Luo S-P, Lin F, Lei Y (2021) Diffusion spectrum imaging of corticospinal tracts in idiopathic normal pressure hydrocephalus. Front Neurol 12:636518

    Article  PubMed  PubMed Central  Google Scholar 

  53. Zhao C, Li Y, Cao W, Xiang K, Zhang H, Yang J, Gan Y (2016) Diffusion tensor imaging detects early brain microstructure changes before and after ventriculoperitoneal shunt in children with high intracranial pressure hydrocephalus. Medicine 95:e5063

    Article  PubMed  PubMed Central  Google Scholar 

  54. Zhao S-X, Xiao Y-H, Lv F-R, Zhang Z-W, Sheng B, Ma H-L (2017) Lateral ventricular volume measurement by 3D MR hydrography in fetal ventriculomegaly and normal lateral ventricles. J Magn Reson Imaging 48:266–273

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to acknowledge the Masonic Institute of the Developing Brain for the ongoing support in pediatric connectivity studies.

Funding

There were no funding sources for this scoping review.

Author information

Authors and Affiliations

  1. Department of Neurosurgery, University of Minnesota, Minneapolis, MN, USA

    Isabela Peña Pino, Robert A. McGovern III, Clark C. Chen & Carolina Sandoval-Garcia

  2. University of Minnesota Medical School, Minneapolis, MN, USA

    Emily Fellows

Authors
  1. Isabela Peña Pino
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Emily Fellows
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Robert A. McGovern III
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Clark C. Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Carolina Sandoval-Garcia
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

IPP, CSG made substantial contributions to the conception an design of the work, IPP, CSG, EF, RAM, CCC participated in the acquisition, analysis, and interpretation of data; IPP, CSG, RAM, CCC drafted the work and revised it critically for important intellectual content; IPP, CSG, EF, RAM, CCC approved the version to be published and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Corresponding author

Correspondence to Carolina Sandoval-Garcia.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Peña Pino, I., Fellows, E., McGovern, R.A. et al. Structural and functional connectivity in hydrocephalus: a scoping review. Neurosurg Rev 47, 201 (2024). https://doi.org/10.1007/s10143-024-02430-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10143-024-02430-z

Keywords

Search

Navigation