The dilemma of hydrocephalus in prolonged disorders of consciousness

[en] Prolonged disorders of consciousness (DOC) are considered to be amongst the most severe outcomes after acquired brain injury. Medical care for these patients is mainly focused on minimizing complications, since treatment options for patients with unresponsive wakefulness or minimal consciousness remain scarce. The complication rate in patients with DOC is high, both in the acute hospital setting as in the rehabilitation or long-term care phase. Hydrocephalus is one of these well-known complications and usually develops quickly following acute changes in cerebrospinal fluid (CSF) circulation after different types of brain damage. However, hydrocephalus may also develop with a significant delay, weeks or even months after the initial injury, reducing the potential for natural recovery of consciousness. In this phase, hydrocephalus is likely to be missed in DOC patients, since their limited behavioral responsiveness camouflages the classic signs of increased intracranial pressure or secondary normal-pressure hydrocephalus. Moreover, the development of late-onset hydrocephalus may exceed the period of regular outpatient follow-up. Several controversies remain about the diagnosis of clinical hydrocephalus in patients with ventricular enlargement after severe brain injury. In this article, we discuss both the difficulties in diagnosis and dilemmas in treatment of CSF disorders in patients with prolonged DOC and review evidence from the literature to advance an active surveillance protocol for the detection of this late, but treatable complication. Moreover, we advocate a low threshold for cerebrospinal fluid diversion when hydrocephalus is suspected, even months or years after brain injury.

Research center :

CHU de Liège-Centre du Cerveau² - ULiège

Disciplines :

Neurology

Author, co-author :

Arnts, Hisse; Universiteit van Amsterdam - UvA > Department of Neurosurgery > Amsterdam University Medical Centers, location AMC

van Erp, Willemijn ; Université de Liège - ULiège > GIGA

Sanz, Leandro ; Université de Liège - ULiège > GIGA Consciousness - Coma Science Group

Lavrijsen, Jan

Schuurman, Rick

Laureys, Steven ; Université de Liège - ULiège > Consciousness-Coma Science Group

Vandertop, William Peter

van den Munckhof, Pepijn

Language :

English

Title :

The dilemma of hydrocephalus in prolonged disorders of consciousness

Publication date :

June 2020

Journal title :

Journal of Neurotrauma

ISSN :

0897-7151

eISSN :

1557-9042

Publisher :

Mary Ann Liebert, United States - New York

Volume :

Issue :

Pages :

2150-2156

Peer reviewed :

Peer Reviewed verified by ORBi

Additional URL :

https://www.liebertpub.com/doi/abs/10.1089/neu.2020.7129

Funders :

F.R.S.-FNRS - Fonds de la Recherche Scientifique [BE]

Available on ORBi :

since 08 June 2020

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Bibliography

1. Giacino, J.T., Fins, J.J., Laureys, S., and Schiff, N.D. (2014). Disorders of consciousness after acquired brain injury: the state of the science. Nat. Rev. Neurol. 10, 99-114.
2. Katz, D.I., Polyak, M., Coughlan, D., Nichols, M., and Roche, A. (2009). Natural history of recovery from brain injury after prolonged disorders of consciousness: outcome of patients admitted to inpatient rehabilitation with 1-4 year follow-up. Prog. Brain Res. 177, 73-88.
3. Luaute, J., Maucort-Boulch, D., Tell, L., Quelard, F., Sarraf, T., Iwaz, J., Boisson, D., and Fischer, C. (2010). Long-term outcomes of chronic minimally conscious and vegetative states. Neurology 75, 246-252.
4. Giacino, J.T., Ashwal, S., Childs, N., Cranford, R., Jennett, B., Katz, D.I., Kelly, J.P., Rosenberg, J.H., Whyte, J., Zafonte, R.D., and Zasler, N.D. (2002). The minimally conscious state: definition and diagnostic criteria. Neurology 58, 349-353.
5. Laureys, S., Celesia, G.G., Cohadon, F., Lavrijsen, J., Leon-Carrion, J., Sannita, W.G., Sazbon, L., Schmutzhard, E., von Wild, K.R., Ze-man, A., and Dolce, G.; European Task Force on Disorders of Consciousness. (2010). Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med. 8, 68.
6. Ganesh, S., Guernon, A., Chalcraft, L., Harton, B., Smith, B., and Pape, T.L.B. (2013). Medical comorbidities in disorders of consciousness patients and their association with functional outcomes. Arch. Phys. Med. Rehab. 94, 1899-1907.
7. Whyte, J., Nordenbo, A.M., Kalmar, K., Merges, B., Bagiella, E., Chang, H., Yablon, S., Cho, S., Hammond, F., Khademi, A., and Giacino, J. (2013). Medical complications during inpatient rehabil-itation among patients with traumatic disorders of consciousness. Arch. Phys. Med. Rehabil. 94, 1877-1883.
8. Pickard, J.D., Coleman, M.R., and Czosnyka, M. (2005). Hydro-cephalus, ventriculomegaly and the vegetative state: a review. Neu-ropsychol. Rehabil. 15, 224-236.
9. Daou, B., Klinge, P., Tjoumakaris, S., Rosenwasser, R.H., and Jab-bour, P. (2016). Revisiting secondary normal pressure hydrocephalus: does it exist? A review. Neurosurg. Focus 41, E6.
10. Hebb, A.O., and Cusimano, M.D. (2001). Idiopathic normal pressure hydrocephalus: a systematic review of diagnosis and outcome. Neu-rosurgery 49, 1166-1184; discussion, 1184-1166.
11. Bhattathiri, P., Gregson, B., Prasad, K., and Mendelow, A.; STICH Investigators. (2006). Intraventricular hemorrhage and hydrocephalus after spontaneous intracerebral hemorrhage: results from the STICH trial. Acta Neurochir. Suppl. 96, 65-68.
12. Qureshi, A.I., Mendelow, A.D., and Hanley, D.F. (2009). Intracerebral haemorrhage. Lancet 373, 1632-1644.
13. Sheehan, J.P., Polin, R.S., Sheehan, J.M., Baskaya, M.K., and Kassell, N.F. (1999). Factors associated with hydrocephalus after aneurysmal subarachnoid hemorrhage. Neurosurgery 45, 1120-1127; discussion, 1127-1128.
14. Guyot, L.L., and Michael, D.B. (2000). Post-traumatic hydrocephalus. Neurol. Res. 22, 25-28.
15. Marmarou, A., Foda, M.A., Bandoh, K., Yoshihara, M., Yamamoto, T., Tsuji, O., Zasler, N., Ward, J.D., and Young, H.F. (1996). Posttraumatic ventriculomegaly: hydrocephalus or atrophy? A new approach for diagnosis using CSF dynamics. J. Neurosurg. 85, 1026-1035.
16. Kammersgaard, L.P., Linnemann, M., and Tibaek, M. (2013). Hy-drocephalus following severe traumatic brain injury in adults. Incidence, timing, and clinical predictors during rehabilitation. NeuroRehabilitation 33, 473-480.
17. Licata, C., Cristofori, L., Gambin, R., Vivenza, C., and Turazzi, S. (2001). Post-traumatic hydrocephalus. J. Neurosurg. Sci. 45, 141-149.
18. Denes, Z., Barsi, P., Szel, I., Boros, E., and Fazekas, G. (2011). Complication during postacute rehabilitation: patients with posttrau-matic hydrocephalus. Int. J. Rehabil. Res. 34, 222-226.
19. O'Dell, M.W., Bell, K.R., and Sandel, M.E. (1998). Brain injury rehabilitation. 2. Medical rehabilitation of brain injury. Arch. Phys. Med. Rehabil. 79, Suppl. I, S10-S15.
20. Sazbon, L., and Groswasser, Z. (1991). Medical complications and mortality of patients in the postcomatose unawareness (PC-U) state. Acta Neurochir. (Wien) 112, 110-112.
21. Adams, H., Ban, V.S., Leinonen, V., Aoun, S.G., Huttunen, J., Saavalainen, T., Lindgren, A., Frosen, J., Fraunberg, M., Koivisto, T., Hernesniemi, J., Welch, B.G., Jaaskelainen, J.E., and Huttunen, T.J. (2016). Risk of shunting after aneurysmal subarachnoid hemorrhage: a collaborative study and initiation of a consortium. Stroke 47, 2488-2496.
22. Hirashima, Y., Hamada, H., Hayashi, N., Kuwayama, N., Origasa, H., and Endo, S. (2003). Independent predictors of late hydrocephalus in patients with aneurysmal subarachnoid hemorrhage-analysis by multivariate logistic regression model. Cerebrovasc. Dis. 16, 205-210.
23. Harris, T.C., de Rooij, R., and Kuhl, E. (2019). The shrinking brain: cerebral atrophy following traumatic brain injury. Ann. Biomed. Eng. 47, 1941-1959.
24. Giacino, J.T., Schnakers, C., Rodriguez-Moreno, D., Kalmar, K., Schiff, N., and Hirsch, J. (2009). Behavioral assessment in patients with disorders of consciousness: gold standard or fool's gold? Prog. Brain Res. 177, 33-48.
25. Giacino, J.T., Katz, D.I., Schiff, N.D., Whyte, J., Ashman, E.J., Ashwal, S., Barbano, R., Hammond, F.M., Laureys, S., Ling, G.S.F., Nakase-Richardson, R., Seel, R.T., Yablon, S., Getchius, T.S.D., Gronseth, G.S., and Armstrong, M.J. (2018). Comprehensive systematic review update summary: disorders of consciousness: report of the Guideline Development, Dissemination, and Implementation Subcommittee of the American Academy of Neurology; the American Congress of Rehabilitation Medicine; and the National Institute on Disability, Independent Living, and Rehabilitation Research. Neurology 91, 461-470.
26. Wannez, S., Heine, L., Thonnard, M., Gosseries, O., and Laureys, S.; Coma Science Group collaborators. (2017). The repetition of behavioral assessments in diagnosis of disorders of consciousness. Ann. Neurol. 81, 883-889.
27. Schnakers, C., Vanhaudenhuyse, A., Giacino, J., Ventura, M., Boly, M., Majerus, S., Moonen, G., and Laureys, S. (2009). Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol. 9, 35.
28. van Erp, W.S., Lavrijsen, J.C.M., Vos, P.E., Bor, H., Laureys, S., and Koopmans, R.T.C.M. (2015). The vegetative state: prevalence, mis-diagnosis, and treatment limitations. J. Am. Med. Dir. Assoc. 16. 2015 Jan;16(1):85.e9-85.e14.
29. Whyte, J., and Nakase-Richardson, R. (2013). Disorders of consciousness: outcomes, comorbidities, and care needs. Arch. Phys. Med. Rehab. 94, 1851-1854.
30. Mazzini, L., Campini, R., Angelino, E., Rognone, F., Pastore, I., and Oliveri, G. (2003). Posttraumatic hydrocephalus: a clinical, neuror-adiologic, and neuropsychologic assessment of long-term outcome. Arch. Phys. Med. Rehabil. 84, 1637-1641.
31. Marmarou, A., Bergsneider, M., Relkin, N., Klinge, P., and Black, P.M. (2005). Development of guidelines for idiopathic normal-pressure hydrocephalus: introduction. Neurosurgery 57, 1-3.
32. Hashimoto, M., Ishikawa, M., Mori, E., and Kuwana, N. (2010). Diagnosis of idiopathic normal pressure hydrocephalus is supported by MRI-based scheme: a prospective cohort study. Cerebrospinal Fluid Res. 7, 18.
33. Williams, M.A., and Relkin, N.R. (2013). Diagnosis and management of idiopathic normal-pressure hydrocephalus. Neurol. Clin. Pract. 3, 375-385.
34. Marmarou, A., Bergsneider, M., Klinge, P., Relkin, N., and Black, P.M. (2005). The value of supplemental prognostic tests for the pre-operative assessment of idiopathic normal-pressure hydrocephalus. Neurosurgery 57, 17-28.
35. Mori, E., Ishikawa, M., Kato, T., Kazui, H., Miyake, H., Miyajima, M., Nakajima, M., Hashimoto, M., Kuriyama, N., Tokuda, T., Ishii, K., Kaijima, M., Hirata, Y., Saito, M., and Arai, H. (2012). Guidelines for Management of Idiopathic Normal Pressure Hydrocephalus: Second Edition. Neurol. Med. Chir. 52, 775-809.
36. Agerskov, S., Wallin, M., Hellstrom, P., Ziegelitz, D., Wikkelso, C., and Tullberg, M. (2019). Absence of disproportionately enlarged subarachnoid space hydrocephalus, a sharp callosal angle, or other morphologic mri markers should not be used to exclude patients with idiopathic normal pressure hydrocephalus from shunt surgery. Am. J. Neuroradiol. 40, 74-79.
37. Perry, A., Graffeo, C.S., Fattahi, N., ElSheikh, M.M., Cray, N., Arani, A., Ehman, R.L., Glaser, K.J., Manduca, A., Meyer, F.B., and Huston, J. (2017). Clinical correlation of abnormal findings on magnetic resonance elastography in idiopathic normal pressure hydrocephalus. World Neurosurg. 99, 695-700.e1.
38. Yeom, K.W., Lober, R.M., Alexander, A., Cheshier, S.H., and Edwards, M.S.B. (2014). Hydrocephalus decreases arterial spin-labeled cerebral perfusion. Am. J. Neuroradiol. 35, 1433-1439.
39. Kahlon, B., Sundbarg, G., and Rehncrona, S. (2002). Comparison between the lumbar infusion and CSF tap tests to predict outcome after shunt surgery in suspected normal pressure hydrocephalus. J. Neurol. Neurosurg. Psychiatry 73, 721-726.
40. Savolainen, S., Hurskainen, H., Paljarvi, L., Alafuzoff, I., and Vapa-lahti, M. (2002). Five-year outcome of normal pressure hydrocephalus with or without a shunt: predictive value of the clinical signs, neu-ropsychological evaluation and infusion test. Acta Neurochir. (Wien) 144, 515-523.
41. Walchenbach, R., Geiger, E., Thomeer, R.T.W.M., and Vanneste, J.A.L. (2002). The value of temporary external lumbar CSF drainage in predicting the outcome of shunting on normal pressure hydro-cephalus. J Neurol. Neurosurg. Psychiatric 72, 503-506.
42. Eklund, A., Smielewski, P., Chambers, I., Alperin, N., Malm, J., Czosnyka, M., and Marmarou, A. (2007). Assessment of cerebrospinal fluid outflow resistance. Med. Biol. Eng. Comput. 45, 719-735.
43. Boon, A.J.W., Tans, J.T.J., Delwel, E.J., EgelerPeerdeman, S.M., Hanlo, P.W., Wurzer, H.A.L., Avezaat, C.J.J., DeJong, D.A., Goos-kens, R.H.J.M., and Hermans, J. (1997). Dutch Normal-Pressure Hy-drocephalus Study. prediction of outcome after shunting by resistance to outflow of cerebrospinal fluid. J. Neurosurg. 87, 687-693.
44. Pfisterer, W.K., Aboul-Enein, F., Gebhart, E., Graf, M., Aichholzer, M., and Muhlbauer, M. (2007). Continuous intraventricular pressure monitoring for diagnosis of normal-pressure hydrocephalus. Acta Neurochir. (Wien) 149, 983-990.
45. Fattahian, R., Bagheri, S.R., and Sadeghi, M. (2018). Development of posttraumatic hydrocephalus requiring ventriculoperitoneal shunt after decompressive craniectomy for traumatic brain injury: a systematic review and meta-analysis of retrospective studies. Med. Arch. 72, 214-219.
46. Waziri, A., Fusco, D., Mayer, S.A., McKhann, G.M., and Connolly, E.S. (2007). Postoperative hydrocephalus in patients undergoing de-compressive hemicraniectomy for ischemic or hemorrhagic stroke. Neurosurgery 61, 489-493.
47. Kim, J.Y., Hu, C., Whang, K., Hong, S.K., Pyen, J.S., and Han, Y.P. (2006). Hydrocephalus in persistent vegetative state. J. Korean Neu-rotraumatol. Soc. 2, 101-106.
48. Chen, Z., Yang, Y.H., Chen, G., Wang, M.B., and Song, W.Q. (2014). Impact of ventriculoperitoneal shunting on chronic normal pressure hydrocephalus in consciousness rehabilitation. J. Rehabil. Med. 46, 876-881.
49. Huang, X., Sun, Y., Xu, J., Wen, L., Cao, Y.L., and Yang, X.F. (2014). Long-term outcomes after shunt implantation in patients with post-traumatic hydrocephalus and severe conscious disturbance. J. Cra-niofac. Surg. 25, 1280-1283.
50. Tribl, G., and Oder, W. (2000). Outcome after shunt implantation in severe head injury with post-traumatic hydrocephalus. Brain Inj. 14, 345-354.
51. Merkler, A.E., Ch'ang, J., Parker, W.E., Murthy, S.B., and Kamel, H. (2017). The rate of complications after ventriculoperitoneal shunt surgery. World Neurosurg. 98, 654-658.
52. Reddy, G.K., Bollam, P., and Caldito, G. (2014). Long-term outcomes of ventriculoperitoneal shunt surgery in patients with hydrocephalus. World Neurosurg. 81, 404-410.
53. Khan, Q.U., Wharen, R.E., Grewal, S.S., Thomas, C.S., Deen, H.G., Reimer, R., Van Gerpen, J.A., Crook, J.E., and Graff-Radford, N.R. (2013). Overdrainage shunt complications in idiopathic normal-pressure hydrocephalus and lumbar puncture opening pressure. J. Neurosurg. 119, 1498-1502.
54. Jox, R.J., Bernat, J.L., Laureys, S. and Rocine, E. (2012). Disorders of consciousness: responding to requests for novel diagnostic and therapeutic interventions. Lancet Neurol. 11, 732-738.
55. Fins, J.J. (2003). Constructing an ethical stereotaxy for severe brain injury: balancing risks, benefits and access. Nat. Rev. Neurosci. 4, 323-327.
56. Thibaut, A., Schiff, N., Giacino, J., Laureys, S., and Gosseries, O. (2019). Therapeutic interventions in patients with prolonged disorders of consciousness. Lancet Neurol. 18, 600-614.
57. Kowalski, R.G., Weintraub, A.H., Rubin, B.A., Gerber, D.J., and Olsen, A.J. (2019). Impact of timing of ventriculoperitoneal shunt placement on outcome in posttraumatic hydrocephalus. J. Neurosurg. 130, 406-417.