Recording, analysis, and interpretation of spreading depolarizations in neurointensive care: Review and recommendations of the COSBID research group

Author:

Dreier Jens P123,Fabricius Martin4,Ayata Cenk56,Sakowitz Oliver W78,William Shuttleworth C9,Dohmen Christian1011,Graf Rudolf11,Vajkoczy Peter112,Helbok Raimund13,Suzuki Michiyasu14,Schiefecker Alois J13,Major Sebastian123,Winkler Maren KL1,Kang Eun-Jeung13,Milakara Denny1,Oliveira-Ferreira Ana I13,Reiffurth Clemens13,Revankar Gajanan S1,Sugimoto Kazutaka14,Dengler Nora F112,Hecht Nils112,Foreman Brandon15,Feyen Bart16,Kondziella Daniel17,Friberg Christian K4,Piilgaard Henning4,Rosenthal Eric S6,Westover M Brandon6,Maslarova Anna18,Santos Edgar8,Hertle Daniel8,Sánchez-Porras Renán8,Jewell Sharon L19,Balança Baptiste2021,Platz Johannes22,Hinzman Jason M23,Lückl Janos1,Schoknecht Karl1324,Schöll Michael825,Drenckhahn Christoph126,Feuerstein Delphine11,Eriksen Nina2728,Horst Viktor129,Bretz Julia S129,Jahnke Paul29,Scheel Michael29,Bohner Georg29,Rostrup Egill27,Pakkenberg Bente2830,Heinemann Uwe124,Claassen Jan31,Carlson Andrew P32,Kowoll Christina M1011,Lublinsky Svetlana3334,Chassidim Yoash3334,Shelef Ilan34,Friedman Alon3335,Brinker Gerrit36,Reiner Michael36,Kirov Sergei A37,Andrew R David38,Farkas Eszter39,Güresir Erdem18,Vatter Hartmut18,Chung Lee S40,Brennan KC40,Lieutaud Thomas2021,Marinesco Stephane2041,Maas Andrew IR16,Sahuquillo Juan42,Dahlem Markus A43,Richter Frank44,Herreras Oscar45,Boutelle Martyn G46,Okonkwo David O47,Bullock M Ross48,Witte Otto W49,Martus Peter50,van den Maagdenberg Arn MJM5152,Ferrari Michel D52,Dijkhuizen Rick M53,Shutter Lori A4754,Andaluz Norberto2355,Schulte André P56,MacVicar Brian57,Watanabe Tomas58,Woitzik Johannes112,Lauritzen Martin459,Strong Anthony J19,Hartings Jed A2355

Affiliation:

1. Center for Stroke Research Berlin, Charité University Medicine Berlin, Berlin, Germany

2. Department of Neurology, Charité University Medicine Berlin, Berlin, Germany

3. Department of Experimental Neurology, Charité University Medicine Berlin, Berlin, Germany

4. Department of Clinical Neurophysiology, Rigshospitalet, Copenhagen, Denmark

5. Neurovascular Research Laboratory, Department of Radiology, and Stroke Service and Neuroscience Intensive Care Unit, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

6. Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston, MA, USA

7. Department of Neurosurgery, Klinikum Ludwigsburg, Ludwigsburg, Germany

8. Department of Neurosurgery, University Hospital, Heidelberg, Germany

9. Department of Neurosciences, University of New Mexico School of Medicine, Albuquerque, NM, USA

10. Department of Neurology, University of Cologne, Cologne, Germany

11. Multimodal Imaging of Brain Metabolism, Max-Planck-Institute for Metabolism Research, Cologne, Germany

12. Department of Neurosurgery, Charité University Medicine Berlin, Berlin, Germany

13. Department of Neurology, Neurocritical Care Unit, Medical University Innsbruck, Innsbruck, Austria

14. Department of Neurosurgery, Yamaguchi University Graduate School of Medicine, Ube, Yamaguchi, Japan

15. 5Department of Neurology and Rehabilitation Medicine, Neurocritical Care Division, University of Cincinnati College of Medicine, Cincinnati, OH, USA

16. Department of Neurosurgery, Antwerp University Hospital and University of Antwerp, Edegem, Belgium

17. Department of Neurology, Rigshospitalet, Copenhagen, Denmark

18. Department of Neurosurgery, University Hospital and University of Bonn, Bonn, Germany

19. Department of Basic and Clinical Neuroscience, Institute of Psychiatry, Psychology and Neuroscience, King’s College London, London, UK

20. Inserm U10128, CNRS UMR5292, Lyon Neuroscience Research Center, Team TIGER, Lyon, France

21. Université Claude Bernard, Lyon, France

22. Department of Neurosurgery, Goethe-University, Frankfurt, Germany

23. Department of Neurosurgery, University of Cincinnati College of Medicine, Cincinnati, OH, USA

24. Neuroscience Research Center, Charité University Medicine Berlin, Berlin, Germany

25. Institute of Medical Biometry and Informatics, University of Heidelberg, Heidelberg, Germany

26. Neurological Center, Segeberger Kliniken, Bad Segeberg, Germany

27. Department of Clinical Physiology and Nuclear Medicine, Rigshospitalet, Copenhagen, Denmark

28. Research Laboratory for Stereology and Neuroscience, Bispebjerg-Frederiksberg Hospital, Rigshospitalet, Copenhagen, Denmark

29. Department of Neuroradiology, Charité University Medicine Berlin, Berlin, Germany

30. Faculty of Health and Medical Sciences, Panum Institute, University of Copenhagen, Copenhagen, Denmark

31. Neurocritical Care, Columbia University College of Physicians & Surgeons, New York, NY, USA

32. Department of Neurosurgery, University of New Mexico School of Medicine, Albuquerque, NM, USA

33. Department of Physiology and Cell Biology, Zlotowski Center for Neuroscience, Beer-Sheva, Israel

34. Department of Neuroradiology, Soroka University Medical Center and Zlotowski Center for Neuroscience, Ben-Gurion University of the Negev, Beer-Sheva, Israel

35. Department of Medical Neuroscience, Faculty of Medicine, Dalhousie University, Halifax, Canada

36. Department of Neurosurgery, University of Cologne, Cologne, Germany

37. Department of Neurosurgery and Brain and Behavior Discovery Institute, Medical College of Georgia, Augusta, GA, USA

38. Department of Biomedical & Molecular Sciences, Queen’s University, Kingston, Canada

39. Department of Medical Physics and Informatics, Faculty of Medicine, and Faculty of Science and Informatics, University of Szeged, Szeged, Hungary

40. Department of Neurology, University of Utah, Salt Lake City, UT, USA

41. AniRA-Neurochem Technological Platform, Lyon, France

42. Department of Neurosurgery, Neurotraumatology and Neurosurgery Research Unit (UNINN), Vall d’Hebron University Hospital, Universitat Autònoma de Barcelona, Barcelona, Spain

43. Department of Physics, Humboldt University, Berlin, Germany

44. Institute of Physiology I/Neurophysiology, Friedrich Schiller University Jena, Jena, Germany

45. Department of Systems Neuroscience, Cajal Institute-CSIC, Madrid, Spain

46. Department of Bioengineering, Imperial College London, London, UK

47. Department of Neurosurgery, University of Pittsburgh Medical Center, Pittsburgh, PA, USA

48. Department of Neurological Surgery, University of Miami, Miami, FL, USA

49. Hans Berger Department of Neurology, Jena University Hospital, Friedrich Schiller University Jena, Jena, Germany

50. Institute for Clinical Epidemiology and Applied Biometry, University of Tübingen, Tübingen, Germany

51. Department of Human Genetics, Leiden University Medical Center, Leiden, the Netherlands

52. Department of Neurology, Leiden University Medical Center, Leiden, the Netherlands

53. Center for Image Sciences, University Medical Center Utrecht, Utrecht, the Netherlands

54. Department of Critical Care Medicine and Neurology, University of Pittsburgh Medical Center, Pittsburgh, PA, USA

55. Mayfield Clinic, Cincinnati, OH, USA

56. Department of Spinal Surgery, St. Franziskus Hospital Cologne, Cologne, Germany

57. Department of Psychiatry, University of British Columbia, Vancouver, Canada

58. Lannister-Finn Corporation, Bryn Mawr, PA, USA

59. Department of Neuroscience and Pharmacology, Panum Institute, University of Copenhagen, Copenhagen, Denmark

Abstract

Spreading depolarizations (SD) are waves of abrupt, near-complete breakdown of neuronal transmembrane ion gradients, are the largest possible pathophysiologic disruption of viable cerebral gray matter, and are a crucial mechanism of lesion development. Spreading depolarizations are increasingly recorded during multimodal neuromonitoring in neurocritical care as a causal biomarker providing a diagnostic summary measure of metabolic failure and excitotoxic injury. Focal ischemia causes spreading depolarization within minutes. Further spreading depolarizations arise for hours to days due to energy supply-demand mismatch in viable tissue. Spreading depolarizations exacerbate neuronal injury through prolonged ionic breakdown and spreading depolarization-related hypoperfusion (spreading ischemia). Local duration of the depolarization indicates local tissue energy status and risk of injury. Regional electrocorticographic monitoring affords even remote detection of injury because spreading depolarizations propagate widely from ischemic or metabolically stressed zones; characteristic patterns, including temporal clusters of spreading depolarizations and persistent depression of spontaneous cortical activity, can be recognized and quantified. Here, we describe the experimental basis for interpreting these patterns and illustrate their translation to human disease. We further provide consensus recommendations for electrocorticographic methods to record, classify, and score spreading depolarizations and associated spreading depressions. These methods offer distinct advantages over other neuromonitoring modalities and allow for future refinement through less invasive and more automated approaches.

Publisher

SAGE Publications

Subject

Cardiology and Cardiovascular Medicine,Clinical Neurology,Neurology

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