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Towards consensus on visual pursuit and visual fixation in patients with disorders of consciousness. A Delphi study

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Abstract

Background

The aim of this Delphi study was to reach consensus about definition, operationalization and assessment of visual pursuit (VP) and visual fixation (VF).

Methods

In a three-round international Delphi study, clinical and research experts on disorders of consciousness indicated their level of agreement on 87 statements using a 5-point Likert scale. Consensus for agreement was defined by a median of 5, an interquartile range (IQR) ≤ 1, and ≥ 80% indicating moderate or strong agreement.

Results

Forty-three experts from three continents participated, 32 completed all three rounds. For VP, the consensus statements with the highest levels of agreement were on the term ‘pursuit of a visual stimulus’, the description ‘ability to follow visually in horizontal and/or vertical plane’, a duration > 2 s, tracking in horizontal and vertical planes, and a frequency of more than 2 times per assessment. For VF, consensus statements with the highest levels of agreement were on the term ‘sustained VF’, the description ‘sustained fixation in response to a salient stimulus’, a duration of > 2 s and a frequency of 2 or more times per assessment. The assessment factors with the highest levels of agreement were personalized stimuli, the use of eye tracking technology, a patient dependent time of assessment, sufficient environmental light, upright posture, and the necessity to exclude ocular/oculomotor problems.

Conclusion

This first international Delphi study on VP and VF in patients with disorders of consciousness provides provisional operational definitions and an overview of the most relevant assessment factors.

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Data availability

Anonymized data will be shared upon reasonable request.

References

  1. Laureys S, Celesia G, Cohadon F, Lavrijsen J, León-Carrión J, Sannita W, Sazbon L, Schmutzhard E, von Wild K, Zeman A, Dolce G (2010) Unresponsive wakefulness syndrome: a new name for the vegetative state or apallic syndrome. BMC Med 8:68. https://doi.org/10.1186/1741-7015-8-68

    Article  PubMed  PubMed Central  Google Scholar 

  2. Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, Kelly JP, Rosenberg JH, Whyte J, Zafonte RD, Zasler ND (2002) The minimally conscious state: definition and diagnostic criteria. Neurology 58:349–353. https://doi.org/10.1212/wnl.58.3.349

    Article  PubMed  Google Scholar 

  3. Multi-Society Task Force on PVS (1994) Medical aspects of the persistent vegetative state (1). N Engl J Med 330:1499–1508. https://doi.org/10.1056/NEJM199405263302107

    Article  Google Scholar 

  4. Giacino JT, Kalmar K, Whyte J (2004) The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil 85:2020–2029. https://doi.org/10.1016/j.apmr.2004.02.033

    Article  PubMed  Google Scholar 

  5. Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly M, Majerus S, Moonen G, Laureys S (2009) Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol 9:35. https://doi.org/10.1186/1471-2377-9-35

    Article  PubMed  PubMed Central  Google Scholar 

  6. van Erp WS, Lavrijsen JC, Vos PE, Bor H, Laureys S, Koopmans RT (2015) The vegetative state: prevalence, misdiagnosis, and treatment limitations. J Am Med Dir Assoc 16:85 e89-85 e14. https://doi.org/10.1016/j.jamda.2014.10.014

    Article  Google Scholar 

  7. Luaute J, Maucort-Boulch D, Tell L, Quelard F, Sarraf T, Iwaz J, Boisson D, Fischer C (2010) Long-term outcomes of chronic minimally conscious and vegetative states. Neurology 75:246–252. https://doi.org/10.1212/WNL.0b013e3181e8e8df

    Article  CAS  PubMed  Google Scholar 

  8. Boly M, Faymonville ME, Schnakers C, Peigneux P, Lambermont B, Phillips C, Lancellotti P, Luxen A, Lamy M, Moonen G, Maquet P, Laureys S (2008) Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol 7:1013–1020. https://doi.org/10.1016/S1474-4422(08)70219-9

    Article  PubMed  Google Scholar 

  9. Eilander HJ, Wijnen VJ, Scheirs JG, de Kort PL, Prevo AJ (2005) Children and young adults in a prolonged unconscious state due to severe brain injury: outcome after an early intensive neurorehabilitation programme. Brain Inj 19:425–436. https://doi.org/10.1080/02699050400025299

    Article  CAS  PubMed  Google Scholar 

  10. Seel RT, Douglas J, Dennison AC, Heaner S, Farris K, Rogers C (2013) Specialized early treatment for persons with disorders of consciousness: program components and outcomes. Arch Phys Med Rehabil 94:1908–1923. https://doi.org/10.1016/j.apmr.2012.11.052

    Article  PubMed  Google Scholar 

  11. Giacino JT, Whyte J, Bagiella E, Kalmar K, Childs N, Khademi A, Eifert B, Long D, Katz DI, Cho S, Yablon SA, Luther M, Hammond FM, Nordenbo A, Novak P, Mercer W, Maurer-Karattup P, Sherer M (2012) Placebo-controlled trial of amantadine for severe traumatic brain injury. N Engl J Med 366:819–826. https://doi.org/10.1056/NEJMoa1102609

    Article  CAS  PubMed  Google Scholar 

  12. Singh R, McDonald C, Dawson K, Lewis S, Pringle AM, Smith S, Pentland B (2008) Zolpidem in a minimally conscious state. Brain Inj 22:103–106. https://doi.org/10.1080/02699050701829704

    Article  PubMed  Google Scholar 

  13. Thibaut A, Bruno MA, Ledoux D, Demertzi A, Laureys S (2014) tDCS in patients with disorders of consciousness: sham-controlled randomized double-blind study. Neurology 82:1112–1118. https://doi.org/10.1212/WNL.0000000000000260

    Article  PubMed  Google Scholar 

  14. Schiff ND, Giacino JT, Kalmar K, Victor JD, Baker K, Gerber M, Fritz B, Eisenberg B, Biondi T, O’Connor J, Kobylarz EJ, Farris S, Machado A, McCagg C, Plum F, Fins JJ, Rezai AR (2007) Behavioural improvements with thalamic stimulation after severe traumatic brain injury. Nature 448:600–603. https://doi.org/10.1038/nature06041

    Article  CAS  PubMed  Google Scholar 

  15. Wilkinson D, Savulescu J (2013) Is it better to be minimally conscious than vegetative? J Med Ethics 39:557–558. https://doi.org/10.1136/medethics-2012-100954

    Article  PubMed  Google Scholar 

  16. Cranford RE (1998) The vegetative and minimally conscious states: ethical implications. Geriatrics 53(Suppl 1):S70-73

    PubMed  Google Scholar 

  17. Fins JJ, Bernat JL (2018) Ethical, palliative, and policy considerations in disorders of consciousness. Neurology 91:471–475. https://doi.org/10.1212/WNL.0000000000005927

    Article  PubMed  Google Scholar 

  18. Giacino JT, Kalmar K (2005) Diagnostic and prognostic guidelines for the vegetative and minimally conscious states. Neuropsychol Rehabil 15:166–174. https://doi.org/10.1080/09602010443000498

    Article  PubMed  Google Scholar 

  19. Giacino JT, Kalmar K (1997) The vegetative and minimally conscious states: a comparison of clinical features and functional outcome. J Head Trauma Rehabil 12:36–51. https://doi.org/10.1097/00001199-199708000-00005

    Article  Google Scholar 

  20. Shiel A, Horn SA, Wilson BA, Watson MJ, Campbell MJ, McLellan DL (2000) The Wessex Head Injury Matrix (WHIM) main scale: a preliminary report on a scale to assess and monitor patient recovery after severe head injury. Clin Rehabil 14:408–416. https://doi.org/10.1191/0269215500cr326oa

    Article  CAS  PubMed  Google Scholar 

  21. Ansell BJ, Keenan JE (1989) The Western Neuro Sensory Stimulation Profile: a tool for assessing slow-to-recover head-injured patients. Arch Phys Med Rehabil 70:104–108

    CAS  PubMed  Google Scholar 

  22. Noe E, Olaya J, Navarro MD, Noguera P, Colomer C, Garcia-Panach J, Rivero S, Moliner B, Ferri J (2012) Behavioral recovery in disorders of consciousness: a prospective study with the Spanish version of the Coma Recovery Scale-Revised. Arch Phys Med Rehabil 93(428–433):e412. https://doi.org/10.1016/j.apmr.2011.08.048

    Article  Google Scholar 

  23. Estraneo A, Moretta P, Cardinale V, De Tanti A, Gatta G, Giacino JT, Trojano L (2015) A multicentre study of intentional behavioural responses measured using the Coma Recovery Scale-Revised in patients with minimally conscious state. Clin Rehabil 29:803–808. https://doi.org/10.1177/0269215514556002

    Article  PubMed  Google Scholar 

  24. Wannez S, Gosseries O, Azzolini D, Martial C, Cassol H, Aubinet C, Annen J, Martens G, Bodart O, Heine L, Charland-Verville V, Thibaut A, Chatelle C, Vanhaudenhuyse A, Demertzi A, Schnakers C, Donneau AF, Laureys S (2018) Prevalence of coma-recovery scale-revised signs of consciousness in patients in minimally conscious state. Neuropsychol Rehabil 28:1350–1359. https://doi.org/10.1080/09602011.2017.1310656

    Article  PubMed  Google Scholar 

  25. Bagnato S, Boccagni C, Sant’Angelo A, Fingelkurts AA, Fingelkurts AA, Galardi G (2017) Longitudinal assessment of clinical signs of recovery in patients with unresponsive wakefulness syndrome after traumatic or nontraumatic brain injury. J Neurotrauma 34:535–539. https://doi.org/10.1089/neu.2016.4418

    Article  PubMed  Google Scholar 

  26. Martens G, Bodien Y, Sheau K, Christoforou A, Giacino JT (2020) Which behaviours are first to emerge during recovery of consciousness after severe brain injury? Ann Phys Rehabil Med 63:263–269. https://doi.org/10.1016/j.rehab.2019.10.004

    Article  PubMed  Google Scholar 

  27. American Congress of Rehabilitation Medicine BI-ISIGDoCTF, Seel RT, Sherer M, Whyte J, Katz DI, Giacino JT, Rosenbaum AM, Hammond FM, Kalmar K, Pape TL, Zafonte R, Biester RC, Kaelin D, Kean J, Zasler N (2010) Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Arch Phys Med Rehabil 91:1795–1813. https://doi.org/10.1016/j.apmr.2010.07.218

    Article  Google Scholar 

  28. Kondziella D, Bender A, Diserens K, van Erp W, Estraneo A, Formisano R, Laureys S, Naccache L, Ozturk S, Rohaut B, Sitt JD, Stender J, Tiainen M, Rossetti AO, Gosseries O, Chatelle C, Ean Panel on Coma DoC (2020) European Academy of Neurology guideline on the diagnosis of coma and other disorders of consciousness. Eur J Neurol 27:741–756. https://doi.org/10.1111/ene.14151

    Article  CAS  PubMed  Google Scholar 

  29. Giacino JT, Katz DI, Schiff ND, Whyte J, Ashman EJ, Ashwal S, Barbano R, Hammond FM, Laureys S, Ling GSF, Nakase-Richardson R, Seel RT, Yablon S, Getchius TSD, Gronseth GS, Armstrong MJ (2018) Practice guideline update recommendations 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 91:450–460. https://doi.org/10.1212/WNL.0000000000005926

    Article  PubMed  PubMed Central  Google Scholar 

  30. Overbeek BUH, Eilander HJ, Lavrijsen JCM, Koopmans R (2018) Are visual functions diagnostic signs of the minimally conscious state? an integrative review. J Neurol 265:1957–1975. https://doi.org/10.1007/s00415-018-8788-9

    Article  PubMed  PubMed Central  Google Scholar 

  31. Keeney S, Hasson F, McKenna HP (2011) The Delphi technique in nursing and health research. Wiley-Blackwell, Oxford

    Book  Google Scholar 

  32. Junger S, Payne SA, Brine J, Radbruch L, Brearley SG (2017) Guidance on Conducting and REporting DElphi Studies (CREDES) in palliative care: recommendations based on a methodological systematic review. Palliat Med 31:684–706. https://doi.org/10.1177/0269216317690685

    Article  PubMed  Google Scholar 

  33. Giacino JT, Whyte J, Nakase-Richardson R, Katz DI, Arciniegas DB, Blum S, Day K, Greenwald BD, Hammond FM, Pape TB, Rosenbaum A, Seel RT, Weintraub A, Yablon S, Zafonte RD, Zasler N (2020) Minimum competency recommendations for programs that provide rehabilitation services for persons with disorders of consciousness: a position statement of the american congress of rehabilitation medicine and the national institute on disability, independent living and rehabilitation research traumatic brain injury model systems. Arch Phys Med Rehabil 101:1072–1089. https://doi.org/10.1016/j.apmr.2020.01.013

    Article  PubMed  Google Scholar 

  34. Diamond IR, Grant RC, Feldman BM, Pencharz PB, Ling SC, Moore AM, Wales PW (2014) Defining consensus: a systematic review recommends methodologic criteria for reporting of Delphi studies. J Clin Epidemiol 67:401–409. https://doi.org/10.1016/j.jclinepi.2013.12.002

    Article  PubMed  Google Scholar 

  35. Koopmans RT, Lavrijsen JC, Hoek F (2013) Concrete steps toward academic medicine in long term care. J Am Med Dir Assoc 14:781–783. https://doi.org/10.1016/j.jamda.2013.08.004

    Article  PubMed  Google Scholar 

  36. Leigh RJ, Zee DS (2015) The neurology of eye movements. Oxford University Press, New York

    Book  Google Scholar 

  37. Giacino JT (1997) Disorders of consciousness: differential diagnosis and neuropathologic features. Semin Neurol 17:105–111. https://doi.org/10.1055/s-2008-1040919

    Article  CAS  PubMed  Google Scholar 

  38. Magliacano A, De Bellis F, Galvao-Carmona A, Estraneo A, Trojano L (2019) Can salient stimuli enhance responses in disorders of consciousness? A systematic review. Curr Neurol Neurosci Rep 19:98. https://doi.org/10.1007/s11910-019-1018-8

    Article  PubMed  Google Scholar 

  39. Blume C, Lechinger J, Santhi N, del Giudice R, Gnjezda MT, Pichler G, Scarpatetti M, Donis J, Michitsch G, Schabus M (2017) Significance of circadian rhythms in severely brain-injured patients: a clue to consciousness? Neurology 88:1933–1941. https://doi.org/10.1212/WNL.0000000000003942

    Article  PubMed  PubMed Central  Google Scholar 

  40. Wilson BA, Dhamapurkar S, Tunnard C, Watson P, Florschutz G (2013) The effect of positioning on the level of arousal and awareness in patients in the vegetative state or the minimally conscious state: a replication and extension of a previous finding. Brain Impairment 14:475–479. https://doi.org/10.1017/BrImp.2013.34

    Article  Google Scholar 

  41. Chatelle C, Bodien YG, Carlowicz C, Wannez S, Charland-Verville V, Gosseries O, Laureys S, Seel RT, Giacino JT (2016) Detection and interpretation of impossible and improbable coma recovery scale-revised scores. Arch Phys Med Rehabil 97(1295–1300):e1294. https://doi.org/10.1016/j.apmr.2016.02.009

    Article  Google Scholar 

  42. Trojano L, Moretta P, Masotta O, Loreto V, Estraneo A (2018) Visual pursuit of one’s own face in disorders of consciousness: a quantitative analysis. Brain Inj 32:1549–1555. https://doi.org/10.1080/02699052.2018.1504117

    Article  PubMed  Google Scholar 

  43. Ting WK, Perez Velazquez JL, Cusimano MD (2014) Eye movement measurement in diagnostic assessment of disorders of consciousness. Front Neurol 5:137. https://doi.org/10.3389/fneur.2014.00137

    Article  PubMed  PubMed Central  Google Scholar 

  44. Spering M, Carrasco M (2015) Acting without seeing: eye movements reveal visual processing without awareness. Trends Neurosci 38:247–258. https://doi.org/10.1016/j.tins.2015.02.002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Schnakers C (2020) Update on diagnosis in disorders of consciousness. Expert Rev Neurother 20:997–1004. https://doi.org/10.1080/14737175.2020.1796641

    Article  CAS  PubMed  Google Scholar 

  46. Royal College of Physicians (2020) Prolonged disorders of consciousness following sudden onset brain injury: National clinical guidelines. RCP, London

    Google Scholar 

  47. Giacino JT, Kalmar K (2004) Coma Recovery Scale-Revised. Administration and Scoring Guidelines. In: Injuries CfH (ed), Edison, New Jersey. http://www.tbims.org/combi/crs/CRS%20Syllabus.pdf

  48. Fitzpatrick-DeSalme E, Long A, Patel F, Whyte J (2021) Behavioral assessment of patients with disorders of consciousness. J Clin Neurophysiol. https://doi.org/10.1097/WNP.0000000000000666

    Article  Google Scholar 

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Acknowledgements

We thank all the experts for participating in this study. We thank the IBIA special interest group on diagnosis/prognosis of DoC for their help in recuitment of experts and discussing the study. We thank ‘Stichting St. Joannes de Deo’ and ‘Het Coma-Hospitium’ for funding this study. We thank Anita Oude Bos, research assistant of the Radboud University Medical Center for developing and processing the online survey and calculating the results. We thank Camille Chatelle PhD and Theresa Bender-Pape PhD for reviewing the survey.

Funding

This study was funded by ‘Het Coma-Hospitium’ and ‘Stichting St. Joannes de Deo’.

Author information

Authors and Affiliations

  1. Department of Primary and Community Care, Radboud Institute of Health Sciences, Radboud University Medical Center, Nijmegen, The Netherlands

    Berno U. H. Overbeek, Jan C. M. Lavrijsen, Henk J. Eilander & Raymond T. C. M. Koopmans

  2. Kalorama, Beek Ubbergen, The Netherlands

    Berno U. H. Overbeek

  3. Azora, Terborg, The Netherlands

    Berno U. H. Overbeek

  4. Faculty of Social and Behavioural Sciences, Department of Psychology, University of Amsterdam, Amsterdam, The Netherlands

    Simon van Gaal

  5. Department of Neurology, Rigshospitalet, Copenhagen University Hospital, Copenhagen, Denmark

    Daniel Kondziella

  6. Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark

    Daniel Kondziella

  7. Center for Specialized Geriatric Care, Joachim en Anna, Nijmegen, The Netherlands

    Raymond T. C. M. Koopmans

Authors
  1. Berno U. H. Overbeek
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  2. Jan C. M. Lavrijsen
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  3. Simon van Gaal
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  4. Daniel Kondziella
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  5. Henk J. Eilander
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  6. Raymond T. C. M. Koopmans
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Contributions

BO contributed to the design of the study protocol, acquisition and analysis of the data and drafted the manuscript. JL contributed to the design of the study protocol, analysis of the data and drafted a significant proportion of the manuscript. SvG contributed to the review of the study protocol, interpretatation of the data and revision of the manuscript. DK contributed to the review of the study protocol, interpretatation of the data and revision of the manuscript. HE contributed to the design of the study protocol, analysis of the data and drafted a significant proportion of the manuscript. RK contributed to the design of the study protocol, analysis of the data and drafted a significant proportion of the manuscript.

Corresponding author

Correspondence to Berno U. H. Overbeek.

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Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

The study was performed in accordance with the ethical standards as laid down in the 1964 Declaration of Helsinki and its later amendsments or comparable ethical standards.

Informed consent

Informed consent was obtained from the participating experts prior to the start of the study.

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Overbeek, B.U.H., Lavrijsen, J.C.M., van Gaal, S. et al. Towards consensus on visual pursuit and visual fixation in patients with disorders of consciousness. A Delphi study. J Neurol 269, 3204–3215 (2022). https://doi.org/10.1007/s00415-021-10905-y

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  • DOI: https://doi.org/10.1007/s00415-021-10905-y

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