Functional neurodiagnostics could allow researchers and clinicians to distinguish more accurately between the unresponsive wakefulness syndrome (UWS) and the minimally conscious state (MCS). It remains unclear how it informs surrogate decision-making.
To explore how the next of kin of patients with disorders of consciousness (DOC) interpret the results of a functional neurodiagnostics measure and how/why their interpretations influence their attitudes towards medical decisions.
Methods and Sample
We conducted problem-centered interviews with seven next of kin of patients with DOC who had undergone a functional HD-EEG examination at a neurological rehabilitation center in Germany. The examination included an auditory oddball paradigm and a motor imagery task to detect hidden awareness. We analyzed the interview transcripts using structuring qualitative content analysis.
Regardless of the diagnostic results, all participants were optimistic of the patients’ meaningful recovery. We hypothesize, that participants deal with the results of examinations according to their belief system. Thus, an unfavorable evaluation of the patient’s state (e.g., a “negative” HD-EEG-result) had the potential to destabilize the participant’s belief system. To re-stabilize or to prevent the destabilization of their belief system, participants used different strategies. Participants accepted a “positive” HD-EEG result since it stabilized their belief system.
We hypothesize, that a group of next of kin of patients with DOC deals with functional neurodiagnostics results on the basis of the result’s value and their high hope that the patient will recover meaningfully. A psychological mechanism seems to moderate the impact of functional neurodiagnostics on surrogate treatment decisions.
This is a preview of subscription content, log in to check access.
Buy single article
Instant unlimited access to the full article PDF.
Price includes VAT for USA
Subscribe to journal
Immediate online access to all issues from 2019. Subscription will auto renew annually.
This is the net price. Taxes to be calculated in checkout.
Giacino, J.T., S. Ashwal, N. Childs, R. Cranford, B. Jennett, D.I. Katz, J.P. Kelly, J.H. Rosenberg, J. Whyte, R.D. Zafonte, and N.D. Zasler. 2002. The minimally conscious state: Definition and diagnostic criteria. Neurology 58 (3): 349–353.
Jennett, B., and F. Plum. 1972. Persistent vegetative state after brain damage. RN 35 (10): ICU1–ICU4.
Laureys, S., et al. 2010. Unresponsive wakefulness syndrome: A new name for the vegetative state or apallic syndrome. BMC Medicine 8: 68.
Multi-Society Task Force on PVS. 1994. Medical aspects of the persistent vegetative state (1). The New England Journal of Medicine 330 (21): 1499–1508.
Bernat, J.L. 2010. Current controversies in states of chronic unconsciousness. Neurology 75 (18 Suppl 1): S33–S38.
Luaute, J., et al. 2010. Long-term outcomes of chronic minimally conscious and vegetative states. Neurology 75 (3): 246–252.
Bernat, J.L., and D.A. Rottenberg. 2007. Conscious awareness in PVS and MCS: The borderlands of neurology. Neurology 68 (12): 885–886.
Bender, A., et al. S1-Leitlinie Hypoxisch-ischämische Enzephalopathie im Erwachsenenalter. Leitlinien für Diagnostik und Therapie in der Neurologie 2018 [cited 2019 30 March]; Available from: www.dgn.org/leitlinien.
Giacino, J.T., C. Schnakers, D. Rodriguez-Moreno, K. Kalmar, N. Schiff, and J. Hirsch. 2009. Behavioral assessment in patients with disorders of consciousness: Gold standard or fool’s gold? Progress in Brain Research 177: 33–48.
Owen, A.M., N.D. Schiff, and S. Laureys. 2009. The assessement of conscious awareness in the vegetative state. In The neurology of consciousness: Cognitive neuroscience and neurpathology. London/Burlington/San Diego: Academic (Elsevier).
Schnakers, C., et al. 2009. Diagnostic accuracy of the vegetative and minimally conscious state: Clinical consensus versus standardized neurobehavioral assessment. BMC Neurology 9: 35.
Jox, R.J., J.L. Bernat, S. Laureys, and E. Racine. 2012. Disorders of consciousness: Responding to requests for novel diagnostic and therapeutic interventions. Lancet Neurology 11 (8): 732–738.
Aguirre, G.K. 2014. Functional neuroimaging: Technical, logical, and social perspectives. The Hastings Center Report Spec No: p. S8–18.
Fernandez-Espejo, D., and A.M. Owen. 2013. Detecting awareness after severe brain injury. Nature Reviews Neuroscience 14 (11): 801–809.
Laureys, S., and N.D. Schiff. 2012. Coma and consciousness: Paradigms (re)framed by neuroimaging. Neuroimage 61 (2): 478–491.
Owen, A.M., M.R. Coleman, M. Boly, M.H. Davis, S. Laureys, and J.D. Pickard. 2006. Detecting awareness in the vegetative state. Science 313 (5792): 1402.
Boly, M., M.R. Coleman, M.H. Davis, A. Hampshire, D. Bor, G. Moonen, P.A. Maquet, J.D. Pickard, S. Laureys, and A.M. Owen. 2007. When thoughts become action: An fMRI paradigm to study volitional brain activity in non-communicative brain injured patients. Neuroimage 36 (3): 979–992.
Monti, M.M., et al. 2010. Willful modulation of brain activity in disorders of consciousness. The New England Journal of Medicine 362 (7): 579–589.
Peterson, A., et al. 2015. Risk, diagnostic error, and the clinical science of consciousness. NeuroImage Clinical 7: 588–597.
Horki, P., et al. 2014. Detection of mental imagery and attempted movements in patients with disorders of consciousness using EEG. Frontiers in Human Neuroscience 8: 1009.
Cruse, D., S. Chennu, C. Chatelle, T.A. Bekinschtein, D. Fernández-Espejo, J.D. Pickard, S. Laureys, and A.M. Owen. 2011. Bedside detection of awareness in the vegetative state: A cohort study. Lancet 378 (9809): 2088–2094.
Cruse, D., S. Chennu, D. Fernández-Espejo, W.L. Payne, G.B. Young, and A.M. Owen. 2012. Detecting awareness in the vegetative state: Electroencephalographic evidence for attempted movements to command. PLoS One 7 (11): e49933.
Gibson, R.M., et al. 2014. Multiple tasks and neuroimaging modalities increase the likelihood of detecting covert awareness in patients with disorders of consciousness. Frontiers in Human Neuroscience 8: 950.
Goldfine, A.M., J.D. Victor, M.M. Conte, J.C. Bardin, and N.D. Schiff. 2011. Determination of awareness in patients with severe brain injury using EEG power spectral analysis. Clinical Neurophysiology 122 (11): 2157–2168.
Sergent, C., F. Faugeras, B. Rohaut, F. Perrin, M. Valente, C. Tallon-Baudry, L. Cohen, and L. Naccache. 2017. Multidimensional cognitive evaluation of patients with disorders of consciousness using EEG: A proof of concept study. NeuroImage Clinical 13: 455–469.
Laureys, S., F. Pellas, P. van Eeckhout, S. Ghorbel, C. Schnakers, F. Perrin, J. Berré, M.E. Faymonville, K.H. Pantke, F. Damas, M. Lamy, G. Moonen, and S. Goldman. 2005. The locked-in syndrome: What is it like to be conscious but paralyzed and voiceless? Progress in Brain Research 150: 495–511.
Bruno, M.A., A. Vanhaudenhuyse, A. Thibaut, G. Moonen, and S. Laureys. 2011. From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: Recent advances in our understanding of disorders of consciousness. Journal of Neurology 258 (7): 1373–1384.
Schiff, N.D. 2015. Cognitive motor dissociation following severe brain injuries. JAMA Neurology 72 (12): 1413–1415.
Bernat, J.L. 2004. Ethical aspects of determining and communicating prognosis in critical care. Neurocritical Care 1 (1): 107–117.
Estraneo, A., P. Moretta, V. Loreto, B. Lanzillo, L. Santoro, and L. Trojano. 2010. Late recovery after traumatic, anoxic, or hemorrhagic long-lasting vegetative state. Neurology 75 (3): 239–245.
Kuehlmeyer, K., et al. 2013. Single case reports on late recovery from chronic disorders of consciousness: A systematic review and ethical appraisal. Bioethica Forum 6 (4).
Johnson, L.S.M., and C. Lazaridis. 2018. The sources of uncertainty in disorders of consciousness. AJOB Neuroscience 9 (2): 76–82.
Smart, C.M., and J.T. Giacino. 2015. Exploring caregivers' knowledge of and receptivity toward novel diagnostic tests and treatments for persons with post-traumatic disorders of consciousness. NeuroRehabilitation 37 (1): 117–130.
Kitzinger, J. 2013. Reporting consciousness in coma: Media framing of neuro-scientific research, hope, and the response of families with relatives in vegetative and minimally conscious states. JOMEC Journal 3: 1–15.
Weijer, C., et al. 2014. Ethics of neuroimaging after serious brain injury. BMC Medical Ethics 15: 41.
Centre Hospitalier Universitaire de Besancon. Families expectations and hope raised by an evaluation of consciousness in patients in a vegetative state (REVE). 2016 [cited 2019 30 March]; Available from: https://clinicaltrials.gov/show/NCT02879565.
Tong, A., P. Sainsbury, and J. Craig. 2007. Consolidated criteria for reporting qualitative research (COREQ): A 32-item checklist for interviews and focus groups. International Journal for Quality in Health Care 19 (6): 349–357.
Schreier, M. 2012. Qualitative content analysis in practice. Sage Publications Ltd.
Stamann, C., M. Janssen, and M. Schreier. 2016. Qualitative Inhaltsanalyse – Versuch einer Begriffsbestimmung und Systematisierung. Forum Qualitative Sozialforschung/Forum: Qualitative Social Research 17 (3): 16.
Mayring, P. 2000. Qualitative content analysis. Forum Qualitative Social Research 1 (2).
Mayring, P. 2014. Qualitative content analysis: Theoretical foundation, basic procedures and software solution. Klagenfurt.
Helfferich, C. 2010. Die Qualität qualitativer Daten: Manual für die Durchführung qualitativer Interviews. Vol. 4. VS Verlag für Sozialwissenschaften.
Jox, R.J., K. Kuehlmeyer, A.M. Klein, J. Herzog, M. Schaupp, D.A. Nowak, E. Koenig, F. Müller, and A. Bender. 2015. Diagnosis and decision making for patients with disorders of consciousness: A survey among family members. Archives of Physical Medicine and Rehabilitation 96 (2): 323–330.
Kuehlmeyer, K., G.D. Borasio, and R.J. Jox. 2012. How family caregivers' medical and moral assumptions influence decision making for patients in the vegetative state: A qualitative interview study. Journal of Medical Ethics 38 (6): 332–337.
Dresing, T., T. Pehl, and C. Schmieder, Manual (on) transcription. Transcription conventions, software guides and practical hints for qualitative researchers. 2015, Marburg.
VERBI Software. Consult. Sozialforschung GmbH, B., Deutschland, MAXQDA, Software für qualitative Datenanalyse. 1989–2018.
Saldana, J. 2013. The coding manual for qualitative researchers. Vol. 2. Sage.
Flick, U., E. von Kardorff, and I. Steinke. 2008. Was ist qualitative Forschung? Einleitung und Überblick. In Qualitative Forschung: Ein Handbuch, ed. E. von Kardorff, U. Flick, and I. Steinke, 13–29. Reinbek bei Hamburg: Rowohlt.
Hopf, C. and C. Schmidt, Zum Verhältnis von innerfamilialen sozialen Erfahrungen, Persönlichkeitsentwicklung und politischen Orientierungen: Dokumentation und Erörterung des methodischen Vorgehens in einer Studie zu diesem Thema. 1993, Hildesheim.
Synder, C.R. 2000. Handbook of hope: Theory, measures, and applications. San Diego: Academic.
Phipps, E.J., et al. 1997. Interpreting responsiveness in persons with severe traumatic brain injury: Beliefs in families and quantitative evaluations. The Journal of Head Trauma Rehabilitation 12 (4): 52–69.
Crawford, S., and J.G. Beaumont. 2005. Psychological needs of patients in low awareness states, their families, and health professionals. Neuropsychological Rehabilitation 15 (3–4): 548–555.
Løvstad, M., K.N. Solbrække, M. Kirkevold, A. Geard, S.L. Hauger, and A.K. Schanke. 2018. “It gets better. It can’t be worse than what we have been through.” Family accounts of the minimally conscious state. Brain Injury 32 (13–14): 1659–1669.
Edgar, A., C. Kitzinger, and J. Kitzinger. 2015. Interpreting chronic disorders of consciousness: Medical science and family experience. Journal of Evaluation in Clinical Practice 21: 374–379.
Verhaeghe, S.T., F. van Zuuren, T. Defloor, M.S. Duijnstee, and M.H. Grypdonck. 2007. The process and the meaning of hope for family members of traumatic coma patients in intensive care. Qualitative Health Research 17 (6): 730–743.
Crispi, F., and C. Crisci. 2000. Patients in persistent vegetative state … and what of their relatives? Nursing Ethics 7 (6): 533–535.
Boyd, E.A., B. Lo, L.R. Evans, G. Malvar, L. Apatira, J.M. Luce, and D.B. White. 2010. "It's not just what the doctor tells me:" Factors that influence surrogate decision-makers' perceptions of prognosis. Critical Care Medicine 38 (5): 1270–1275.
Musschenga, B. 2019. Is there a problem with false Hope? The Journal of Medicine and Philosophy: A Forum for Bioethics and Philosophy of Medicine 44 (4): 423–441.
Tresch, D.D., F.H. Sims, Duthie EH Jr, and M.D. Goldstein. 1991. Patients in a persistent vegetative state attitudes and reactions of family members. Journal of the American Geriatrics Society 39 (1): 17–21.
Mwaria, C.B. 1990. The concept of self in the context of crisis: A study of families of the severely brain-injured. Social Science & Medicine 30 (8): 889–893.
Gray, K., T.A. Knickman, and D.M. Wegner. 2011. More dead than dead: Perceptions of persons in the persistent vegetative state. Cognition 121 (2): 275–280.
Ditto, P.H. 2006. What would Terri want? On the psychological challenges of surrogate decision making. Death Studies 30 (2): 135–148.
Racine, E., R. Amaram, M. Seidler, M. Karczewska, and J. Illes. 2008. Media coverage of the persistent vegetative state and end-of-life decision-making. Neurology 71 (13): 1027–1032.
Festinger, L. 1957. A theory of cognitive dissonance. Stanford University Press.
Festinger, L., H. Riecken, and S. Schachter. 1956. When prophecy fails. Harper-Torchbooks.
Harmon-Jones, E., and C. Harmon-Jones. 2007. Cognitive dissonance theory after 50 years of development. Zeitschrift für Sozialpsychologie 38 (1): 7–16.
Ong, A.S., L. Frewer, and M.Y. Chan. 2017. Cognitive dissonance in food and nutrition–a review. Critical Reviews in Food Science and Nutrition 57 (11): 2330–2342.
Steckelberg, A., J. Kasper, and I. Muhlhauser. 2005. Selective information seeking: Can consumers' avoidance of evidence-based information on colorectal cancer screening be explained by the theory of cognitive dissonance? German Medical Science 5.
Schembs, L., R.J. Jox, and K. Kuehlmeyer. 2018. Social uncertainty in disorders of consciousness: Shedding light on the various perspectives of family caregivers and surrogates. AJOB Neuroscience 9 (2): 85–87.
Macdonald, M.E., S. Liben, F.A. Carnevale, and S.R. Cohen. 2008. Signs of life and signs of death: Brain death and other mixed messages at the end of life. Journal of Child Health Care 12 (2): 92–105.
Racine, E., S. Sattler, and A. Escande. 2017. Free will and the brain disease model of addiction: The not so seductive allure of neuroscience and its modest impact on the attribution of free will to people with an addiction. Frontiers in Psychology 8: 1850.
Kuehlmeyer, K., et al. 2014. Physicians' attitudes toward medical and ethical challenges for patients in the vegetative state: Comparing Canadian and German perspectives in a vignette survey. BMC Neurology 14: 119.
Racine, E. 2010. Pragmatic neuroethics: Improving treatment and understanding of the mind-brain, 174–176. Cambridge: MIT Press.
Kuehlmeyer, K., E. Racine, N. Palmour, E. Hoster, G.D. Borasio, and R.J. Jox. 2012. Diagnostic and ethical challenges in disorders of consciousness and locked-in syndrome: A survey of German neurologists. Journal of Neurology 259 (10): 2076–2089.
McCabe, D.P., and A.D. Castel. 2008. Seeing is believing: The effect of brain images on judgments of scientific reasoning. Cognition 107 (1): 343–352.
Michael, R.B., E.J. Newman, M. Vuorre, G. Cumming, and M. Garry. 2013. On the (non)persuasive power of a brain image. Psychonomic Bulletin & Review 20 (4): 720–725.
Feigenson, N. 2006. Brain imaging and courtroom evidence: On the admissibility and persuasiveness of fMRI. International Journal of Law in Context 2 (3): 233–255.
Jox, R.J., E. Denke, J. Hamann, R. Mendel, H. Förstl, and G.D. Borasio. 2012. Surrogate decision making for patients with end-stage dementia. International Journal of Geriatric Psychiatry 27 (10): 1045–1052.
Suppes, A., and J.J. Fins. 2013. Surrogate expectations in severe brain injury. Brain Injury 27 (10): 1141–1147.
French, K.B. 2017. Care of extremely small premature infants in the neonatal intensive care unit: A parent's perspective. Clinics in Perinatology 44 (2): 275–282.
Lariviere-Bastien, D., et al. 2011. Perspectives of adolescents and young adults with cerebral palsy on the ethical and social challenges encountered in healthcare services. Narrative Inquiry in Bioethics 1 (1): 43–54.
Mruck, K., and F. Breuer. 2003. Subjectivity and reflexivity in qualitative research – The FQS issues. Forum Qualitative Sozialforschung/Forum: Qualitative Social Research 2 (4).
Schorr, B., W. Schlee, M. Arndt, D. Lulé, I.T. Kolassa, A. Lopez-Rolon, and A. Bender. 2015. Stability of auditory event-related potentials in coma research. Journal of Neurology 262 (2): 307–315.
Kalmar, K., and J.T. Giacino. 2005. The JFK coma recovery scale—Revised. Neuropsychological Rehabilitation 15 (3–4): 454–460.
This article is part of LS’s cumulative dissertation (Dr. med.) at the Medical Faculty of LMU Munich. The assistance provided by Marion Arndt in approaching the participants and ensuring their informed consent, by Silke Ohlmeier for transcribing interviews and sharing her insights during early stages of the analysis with us, by Lukas Martinez who translated some of the interview quotes from German into English and by Lars Schrodberger who finalized the layout of the figure is very much appreciated. We are grateful to participants of different research meetings where we were able to discuss our study, foremost in Germany at the rehabilitation center where the examinations of the patients were conducted, the Qualitative Workshop [Qualitative Werkstatt] at LMU Munich, the Institute for Ethics, History and Theory of Medicine at LMU Munich, the Palliative Medicine Research Network under the lead of Prof. Dr. Gian Domenico Borasio in Munich and in Canada a meeting with the Montréal Neuroethics Network and a Journal Club at the Neuroethics Research Unit at the IRCM and a poster presentation at the 21st International Congress on Palliative Care. Last but not least, we would like to express our great appreciation to the participants of this study who shared their personal experiences with us. We also express our gratitude to the Friedrich-Baur-Stiftung who funded our study (Grant Number: 12/14, funding period 8/2014 to 07/2016) and the Max Weber Program who funded LS’s research stay at the IRCM, Montréal, Canada and her visit to the 21st International Congress on Palliative Care. Furthermore, ER receives a career award from the Fonds de recherche du Québec – Santé (FRQ-S).
Research involving Human Participants: All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards.
Informed consent was obtained from all individual participants included in the study.
Disclosure of potential conflicts of interest
All authors declare no conflict of interest.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Functional HD-EEG-Examination to Detect Residual Conscious Awareness
The functional HD-EEG examination consisted of a protocol with two sections. The researchers performed both examinations with each patient. The first part was an auditory oddball paradigm using 4 blocks of standard and target stimuli with 10 target and 40 standard stimuli per block, which were presented randomized within each block. Stimuli consisted of 1500 Hz and 1000 Hz tones, respectively, with 500 ms duration and a 500 ms inter-stimulus interval. The main experiment was preceded by the presentation of 2 target and 8 standard tones as demonstration. Patients were instructed to listen to the target tones attentively. The experimental procedure was identical to the one described in a prior publication by one of the authors of this study and colleagues .
The second part involved a command-following paradigm. Using a randomized block-structure, a resting condition and a mental motor imagery condition were tested in 6 blocks per condition with 15 trials per block. Each block was preceded by a verbal instruction and each trial was announced by an auditory trigger signal. The method was based on the experiment by Cruse et al. (2011) . It tested command-following using an ERP-based mental motor imagery, instructing participants to either squeeze their right hand or to wiggle the toes. Yet, the paradigm, which was used in the rehabilitation clinic, entailed different movements than in the experiment of Cruse et al. (2011), in order to achieve a higher activation of the motor cortex following the instruction: For the motor imagery task, the patient received the instruction to imagine raising his/her arms and lowering them again when an auditive trigger-sound appeared. This condition was statistically compared to the findings obtained during a resting period, which was also indicated by auditive trigger-sounds. For the resting periods, patients were instructed to listen to the auditive trigger-sounds. The examination was repeated on a second day to reduce the influence of possibly confounding factors like tiredness. All exams were conducted by research personnel (a psychologist and a study nurse) specifically trained in conducting HD-EEG exams and data analyses. The mental motor imagery condition was statistically compared to the resting condition. The examination was repeated on a second day to reduce the influence of possibly confounding factors like alertness or tiredness. All exams were conducted by research personnel specifically trained in neurodiagnostics measures.
Standardized Written Report of the Findings of the HD-EEG Examination
In addition to the scientific purpose of the study, the results of the HD-EEG exams were always communicated in a standardized way using a written report. The reports were prepared by the researchers and revised by physicians experienced in the field of neuro-rehabilitation and trained in the interpretation of the functional HD-EEG paradigm by one of the head physicians. The HD-EEG report included a detailed description of the examinations, the individual patient’s results and a discussion of these results in comparison with a population of healthy individuals. In respect to the auditory oddball paradigm (p300), the report included the extracted waveforms and topographies of the stimulus groups (standards and targets). Based on the waveform (amplitude and latency) as well as the topographical distribution of the p300 component, the quality of the brain response to the presented stimuli was rated. In respect to the mental motor imagery paradigm, the accuracy of the machine learning classifier was reported, expressing the performance of the patient to follow the instructions. Additionally, the statistical difference between the resting and the mental motor imagery condition was reported. The report then stated if and how well the patient was able to follow the instructions and compared the performance to a control group of healthy controls. The report concluded with an overall evaluation of the patient’s level of consciousness. Here it compared the results of the HD EEG with the results of the structured clinical examinations with the Coma Recovery Scale Revised (CRS-R) . In case that the results of both measures were at odds with each other, this was stated and explained with regard to a variability of a patient’s arousal during the exams. Reports described the HD-EEG as an experimental scientific measure and stated that results would never be used alone to guide medical decisions. Doctors attached the HD-EEG-reports to the patient’s medical chart and sent them out to the patient’s general physician as well as to his/her legal representative within one to two weeks after the patient’s discharge. The process of oral disclosure of the results was not standardized. Usually, the results of the examinations were mentioned in the medical discharge conversations between doctors and patients’ next of kin, embedded in a more general evaluation of the patient’s condition and prognosis.
About this article
Cite this article
Schembs, L., Ruhfass, M., Racine, E. et al. How Does Functional Neurodiagnostics Inform Surrogate Decision-Making for Patients with Disorders of Consciousness? A Qualitative Interview Study with Patients’ Next of Kin. Neuroethics (2020) doi:10.1007/s12152-019-09425-4
- Unresponsive wakefulness syndrome (UWS)
- Persistent vegetative state (PVS)
- Minimally conscious state (MCS)
- Functional neuroimaging
- Electroencephalography (EEG)
- Family care givers