Skip to main content

Advertisement

SpringerLink
Log in

Brain motion in patients with skull defects: B-mode ultrasound observations on respiration-induced movements

  • Clinical Article - Brain Injury
  • Published:
Acta Neurochirurgica Aims and scope Submit manuscript

Abstract

Background

Since ancient times, brain motion has captured the attention of human beings. However, there are no reports about morphological changes that occur below the cortex or skin flap when a patient, with an open skull breathes, coughs, or engages effort. Thus, the aim of this study was to characterize brain motion caused by breathing movements in adults with an open skull.

Methods

Twenty-five craniectomized patients were studied using B-mode ultrasonography during early and late postoperative periods. Twelve patients were analysed during surgery. Brain movements induced by breathing activity were assessed in this prospective observational study.

Results

Taking as a reference the cranial base, an increase in intrathoracic pressure was accompanied by a rise of the brain due to the expansion of the basal cisterns. Greater increases in intrathoracic pressure (resulting from the Valsalva manoeuvre and coughing) propelled the brain in a block from the foramen magnum towards the craniectomy, mainly in structures near the tentorial incisure. Prolonging the Valsalva manoeuvre also resulted in thickening of the cortical mantle attributable to vascular congestion. The magnitude of these movements was directly related to breathing effort.

Conclusions

The increase in intrathoracic pressure was immediately transmitted to the brain by the rise of cerebrospinal fluid, while brain swelling attributable to vascular congestion showed a brief delay. The Valsalva manoeuvre and coughing caused abrupt morphological changes in the tentorial hiatus neighbouring structures because of the distension of the basal cisterns. These movements could play a role in the pathophysiology of the syndrome of trephined.

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

Similar content being viewed by others

References

  1. Agner C, Dujovny M, Gaviria M (2002) Neurocognitive assessment before and after cranioplasty. Acta Neurochir 144:1033–1040

    Article  PubMed  CAS  Google Scholar 

  2. Akins PT, Guppy KH (2008) Sinking skin flaps, paradoxical herniation, and external brain tamponade: a review of decompressive craniectomy management. Neurocrit Care 9:269–276

    Article  PubMed  Google Scholar 

  3. Alperin N, Lee SH, Sivaramakrishnan A, Hushek SG (2005) Quantifying the effect of posture on intracranial physiology in humans by MRI flow studies. J Magn Reson Imaging 22:591–596

    Article  PubMed  Google Scholar 

  4. Batson OV (1940) The function of the vertebral veins and their role in the spread of metastases. Ann Surg 112:138–149

    Article  PubMed  CAS  Google Scholar 

  5. Britt RH, Rossi GT (1982) Quantitative analysis of methods for reducing physiological brain pulsations. J Neurosci Methods 6:219–229

    Article  PubMed  CAS  Google Scholar 

  6. Campbell JK, Clark JM, White DN, Jenkins CO (1970) Pulsatile echo-encephalography. Acta Neurol Scand 46(Suppl 45):1–57

    Google Scholar 

  7. Chandler WF, Knake JE, McGillicuddy JE, Lillehei KO, Silver TM (1982) Intraoperative use of real-time ultrasonography in neurosurgery. J Neurosurg 57:157–163

    Article  PubMed  CAS  Google Scholar 

  8. Chen C, Smith ER, Ogilvy CS, Carter BS (2006) Decompressive craniectomy: physiologic rationale, clinical indications, and surgical considerations. In: Schmidek HH, Roberts DW (eds) Schmidek & Sweet. Operative Neurosurgical Techniques. Indications, methods and results. Saunders – Elsevier, Philadelphia, pp 70–80

    Google Scholar 

  9. Ciric J, Michael M, Stafford M, Lawson L, Garces R (1983) Transsphenoidal microsurgery of pituitary macroadenomas with long term follow-up results. J Neurosurg 59:395–401

    Article  PubMed  CAS  Google Scholar 

  10. Clarke E, O’Malley CD (1968) The Human Brain and Spinal Cord. A Historical Study Illustrated by Writings from antiquity to the Twentieth Century. University of California Press, Berkeley, p 737

    Google Scholar 

  11. Czosnika M, Copeman J, Czosnika Z, McConnell RS, Dickinson C, Pickard JD (2000) Post-traumatic hydrocephalus: influence of craniectomy on the CSF circulation. J Neurol Neurosurg Psychiatry 68:246–248

    Article  Google Scholar 

  12. Dardenne G, Dereymaeker A, Lacheron JM (1969) Cerebrospinal fluid pressure and pulsatility. Europ Neurol 2:193–216

    Article  PubMed  CAS  Google Scholar 

  13. De Slegte RGM, Valk J, Broere G, de Waal F (1986) Further experience with ultrasound examinations in the postoperative brain. Acta Neurochir (Wien) 81:106–112

    Article  Google Scholar 

  14. Du Boulay GH, O’Connell J, Currie J, Bostick T, Verity P (1972) Further investigations on pulsatile movements in the cerebrospinal fluid pathways. Acta Radiol Diagn 13:496–523

    Google Scholar 

  15. Dujovny M, Aviles A, Agner C, Fernandez P, Charbel FT (1997) Cranioplasty: cosmetic or therapeutic? Surg Neurol 47:238–241

    Article  PubMed  CAS  Google Scholar 

  16. Dujovny M, Fernandez P, Alperin N, Betz N, Misra M, Mafee M (1997) Post-cranioplasty cerebrospinal fluid hydrodynamic changes: magnetic resonance imaging quantitative analysis. Neurol Res 19:311–316

    PubMed  CAS  Google Scholar 

  17. Enzmann DR, Murphy Irwin K, Fine M, Silverberg GM, Hanbery JW (1984) Intraoperative and outpatient echoencephalography through a burr hole. Neuroradiology 26:57–59

    Article  PubMed  CAS  Google Scholar 

  18. Erdogan E, Duz B, Kocaoglu M, Izci Y, Sirin S, Timurkaynak E (2003) The effect of cranioplasty on cerebral hemodynamics: evaluation with transcranial doppler sonography. Neurol India 51:479–481

    PubMed  CAS  Google Scholar 

  19. Ertl-Wagner BB, Lienemann A, Reith W, Reiser MF (2001) Demonstration of periventricular brain motion during a Valsalva maneuver: description of technique, evaluation in healthy volunteers and first results in hydrocephalic patients. Eur Radiol 11:1998–2003

    Article  PubMed  CAS  Google Scholar 

  20. Fields JD, Lansberg MG, Skirboll SL, Kurien PA, Wijman CAC (2006) “Paradoxical” transtentorial herniation due to CSF drainage in the presence of a hemicraniectomy. Neurology 67:1513–1514

    Article  PubMed  CAS  Google Scholar 

  21. Fodstad H, Love JA, Ekstedt J, Friden H, Liliequist B (1984) Effect of cranioplasty on cerebrospinal fluid hydrodynamics in patients with the syndrome of the trephined. Acta Neurochir (Wien) 70:21–30

    Article  CAS  Google Scholar 

  22. Friese S, Hamhaber U, Erb M, Kueker W, Klose U (2004) The influence of pulse and respiration on spinal cerebrospinal fluid pulsation. Invest Radiol 39:120–130

    Article  PubMed  Google Scholar 

  23. Gardner WJ (1945) Closure of defects of the skull with tantalum. Surg Gynecol Obstetrics 80:303–312

    Google Scholar 

  24. Gardner WJ (1965) Hydrodynamic mechanism of syringomyelia: its relationship to myelocele. J Neurol Neurosurg Psychiatry 28:247–259

    Article  PubMed  CAS  Google Scholar 

  25. Gisolf J, van Lieshout JJ, van Heusden K, Pott E, Stok WJ, Karemaker JM (2004) Human cerebral venous outflow pathway depends on posture and central venous pressure. J Physiol 560(Pt1):317–327

    Article  PubMed  CAS  Google Scholar 

  26. Gooding GAW, Boggan JE, Powers SK, Martin NA, Weinstein PR (1984) Neurosurgical sonography: intraoperative and postoperative imaging of the brain. AJNR 5:521–525

    PubMed  CAS  Google Scholar 

  27. Goodrich JT (1997) Neurosurgery in the Ancient and Medieval Worlds. In: Greenblatt SH, Dagi TF, Epstein MH (eds) A History of Neurosurgery. In its Scientific and Professional Contexts. The American Association of Neurological Surgeons, Illinois, p 54

    Google Scholar 

  28. Gottlob I, Simonsz-Tòth B, Heilbronner R (2002) Midbrain syndrome with eye movement disorder: dramatic improvement after cranioplasty. Strabismus 10:271–277

    Article  PubMed  Google Scholar 

  29. Guerci AD, Shi AY, Levin H, Tsitlik J, Weisfeldt ML, Chandra N (1985) Transmission of intrathoracic pressure to the intracranial space during cardiopulmonary resuscitation in dogs. Circ Res 56:20–30

    Article  PubMed  CAS  Google Scholar 

  30. Haller A (1936) A Dissertation on the Sensible and Irritable Parts of Animals. [London, J Nourse] Introduction by Owsei Temkin. The Johns Hopkins Press, Baltimore, p 49

    Google Scholar 

  31. Hamilton WF, Woodbury RA, Jr Harper HT (1944) Arterial, cerebrospinal and venous pressures in man during cough and strain. Am J Physiol 141:42–50

    Google Scholar 

  32. Hill DLG, Maurer CR Jr, Maciunas RJ, Barwise JA, Fitzpatrick JM, Wang MY (1998) Measurement of intraoperative brain surface deformation under a craniotomy. Neurosurgery 43:514–528

    Article  PubMed  CAS  Google Scholar 

  33. Jellinek EH (2006) The Valsalva manoeuvre and Antonio Valsalva (1666–1723). J R Soc Med 99:448–451

    Article  PubMed  CAS  Google Scholar 

  34. Kemmling A, Duning T, Lemcke L, Niederstadt T, Minnerup J, Wersching H, Marziniak M (2010) Case report of MR perfusion imaging on sinking skin flap syndrome: growing evidence for hemodynamic impairment. BMC Neurol 10:80–83

    Article  PubMed  Google Scholar 

  35. Klose U, Strik C, Kiefer C, Grodd W (2000) Detection of a relation between respiration and CSF pulsation with an echoplanar technique. J Magn Reson Imaging 11:438–444

    Article  PubMed  CAS  Google Scholar 

  36. Lee RR, Abraham RA, Quinn CB (2001) Dynamic physiologic changes in lumbar CSF volume quantitatively measured by three-dimensional fast spin-echo MRI. Spine 26:1172–1178

    Article  PubMed  CAS  Google Scholar 

  37. Maier SE, Hardy CJ, Jolesz FA (1994) Brain and cerebrospinal fluid motion: real-time quantification with M-mode MR imaging. Radiology 193:477–483

    PubMed  CAS  Google Scholar 

  38. Martins AN, Wiley JK, Myers PW (1972) Dynamics of the cerebrospinal fluid and the spinal dura mater. J Neurol Neurosurg Psychiatry 35:468–473

    Article  PubMed  CAS  Google Scholar 

  39. Nabavi A, Black PM, Gering DT, Westin CF, Mehta V, Pergolizzi RS, Ferrant M, Warfield SK, Hata N, Schwartz RB, Wells WM III, Kikinis R, Jolesz FA (2001) Serial intraoperative magnetic resonance imaging of brain shift. Neurosurgery 48:787–798

    PubMed  CAS  Google Scholar 

  40. Neuburger M (1987) The Historical Development of Experimental Brain and Spinal Cord Physiology Before Flourens. Translated and Edited by Edwin Clarke. The Johns Hopkins University Press, Baltimore

    Google Scholar 

  41. Ostrup R, Bejar R, Marshall L (1983) Real-time ultrasonography: a useful tool in the evaluation of the craniectomized, brain-injured patient. Neurosurgery 12:225–227

    Article  PubMed  CAS  Google Scholar 

  42. Prabhakar H, Bithal PK, Suri A, Rath GP, Dash HH (2007) Intracranial pressure changes during Valsalva Manoeuvre in patients undergoing a neuroendoscopic procedure. Minim Invas Neurosurg 50:98–101

    Article  CAS  Google Scholar 

  43. Quencer RM, Montalvo BM (1986) Intraoperative cranial sonography. Neuroradiology 28:528–550

    Article  PubMed  CAS  Google Scholar 

  44. Reitan H (1941) On movements of fluid inside the cerebro-spinal space. Acta Radiol 22:762–779

    Article  Google Scholar 

  45. Roberts DW, Hartov A, Kennedy FE, Miga MI, Paulsen KD (1998) Intraoperative brain shift and deformation: a quantitative analysis of cortical displacement in 28 cases. Neurosurgery 43:749–760

    Article  PubMed  CAS  Google Scholar 

  46. Rubin JM, Mirfakhraee M, Duda EE, Dohrmann GJ, Brown F (1980) Intraoperative ultrasound examination of the brain. Radiology 137:831–832

    PubMed  CAS  Google Scholar 

  47. Sakamoto S, Eguchi K, Kiura Y, Arita K, Kurisu K (2006) CT perfusion imaging in the syndrome of the sinking skin flap before and after cranioplasty. Clin Neurol Neurosurg 108:583–585

    Article  PubMed  Google Scholar 

  48. Schroth G, Klose U (1992) Cerebrospinal fluid flow II Physiology of respiration-related pulsations. Neuroradiology 35:10–15

    Article  PubMed  CAS  Google Scholar 

  49. Schiffer J, Gur R, Nisim U, Pollak L (1997) Symptomatic patients after craniectomy. Surg Neurol 47:231–237

    Article  PubMed  CAS  Google Scholar 

  50. Stiver SI (2009) Complications of decompressive craniectomy for traumatic brain injury. Neurosurg Focus 26:E7

    Article  PubMed  Google Scholar 

  51. Tabaddor K, La Morgese J (1976) Complication of a large cranial defect. Case report J Neurosurg 44:506–508

    CAS  Google Scholar 

  52. West CGH (1981) A short history of the management of penetrating missile injuries of the head. Surg Neurol 16:145–149

    Article  PubMed  CAS  Google Scholar 

  53. Williams B (1981) Simultaneous cerebral and spinal fluid pressure recordings. I. Technique, physiology, and normal results. Acta Neurochir 58:167–185

    Article  PubMed  CAS  Google Scholar 

  54. Winkler P (1994) Cerebrospinal fluid dynamics in infants evaluated with color doppler US and spectral analysis: respiratory versus arterial synchronization. Radiology 192:423–430

    PubMed  CAS  Google Scholar 

  55. Winkler PA, Stummer W, Linke R, Krishnan KG, Tatsch K (2000) Influence of cranioplasty on postural blood flow regulation, cerebrovascular reserve capacity, and cerebral glucose metabolism. J Neurosurg 93:53–61

    Article  PubMed  CAS  Google Scholar 

  56. Wostyn P (2004) Can increased intracranial pressure or exposure to repetitive intermittent intracranial pressure elevations raise your risk for Alzheimer’s disease? Med Hypotheses 62:925–930

    Article  PubMed  CAS  Google Scholar 

  57. Wostyn P, Audenaert K, De Deyn PP (2009) The Valsalva maneuver and Alzheimer’s disease: is there a link? Curr Alzheimer Res 6:59–68

    Article  PubMed  CAS  Google Scholar 

  58. Yamaura A, Makino H (1976) Neurological deficits following craniectomy. J Neurosurg 45:362

    Google Scholar 

  59. Yasargil MG, Kasdaglis K, Jain KK, Weber HP (1976) Anatomical observations of the subarachnoid cisterns of the brain during surgery. J Neurosurg 44:298–302

    Article  PubMed  CAS  Google Scholar 

  60. Yoshida K, Furuse M, Izawa A, Iizima N, Kuchiwaki H, Inao S (1996) Dynamics of cerebral blood flow and metabolism in patients with cranioplasty as evaluated by 133Xe CT and 31P magnetic resonance spectroscopy. J Neurol Neurosurg Psychiatry 61:166–171

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgements

The authors wish to thank Silvana A. Sanguinetti, M.D. for translating the original article into English.

Conflict of interest

The authors declare that they have no conflict of interest.

Author information

Authors and Affiliations

  1. Neurosurgery Unit, “Dr. Abraham Piñeyro” Hospital, Arenales 361, 6000, Junin, Argentina

    Nelson A. Picard & Carlos A. Zanardi

Authors
  1. Nelson A. Picard
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Carlos A. Zanardi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Nelson A. Picard.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Ambulatory patient No. 13. Parasagittal view. The transducer was placed on the top of the head. The thalamus is found in the centre of the image, and the brainstem can be seen toward hour 6. The skull base is seen as a hyperechoic rim at the bottom of the image. Hyperpnea. The descent of the brainstem during inspiration and its ascent during exhalation is shown. (MPG 6194 kb)

Ambulatory patient No. 19. Coronal view. Coughing. Abrupt movements can be seen at the brainstem and diencephalic levels. Towards hour 4, the fourth ventricle (hypoechoic) with its choroid plexus (hyperechoic) and the occipital foramen can be seen. The morphological changes seem to be due to parenchymal propulsion caused by CSF. No changes can be seen in the distance between the cortical surface and the ependyma of the supratentorial ventricular cavities, which could be attributed to vascular congestion. (MPG 2970 kb)

Ambulatory patient No 10. Coronal view. Valsalva manoeuvre. See Fig. 1 for descriptive text. (MPG 4682 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Picard, N.A., Zanardi, C.A. Brain motion in patients with skull defects: B-mode ultrasound observations on respiration-induced movements. Acta Neurochir 155, 2149–2157 (2013). https://doi.org/10.1007/s00701-013-1838-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00701-013-1838-2

Keywords

Search

Navigation