The Initiation of Swallowing Can Indicate the Prognosis of Disorders of Consciousness: A Self-Controlled Study

Jianan Wang, Jing Wang, Xiaohua Hu, Lingqi Xu, Jinna Tian, Jiayin Li, Danruo Fang, Wangshan Huang, Yuxiao Sun, Minhui He, Steven Laureys, Haibo Di, Jianan Wang, Jing Wang, Xiaohua Hu, Lingqi Xu, Jinna Tian, Jiayin Li, Danruo Fang, Wangshan Huang, Yuxiao Sun, Minhui He, Steven Laureys, Haibo Di

Abstract

Objective: To detect the initiation of swallowing in patients with disorders of consciousness (DOC) as well as the relationship between the initiation of swallowing and the prognosis of DOC patients. Methods: Nineteen DOC patients were included in this study, and a self-controlled trial compared five different stimuli. The five different stimuli were as follows: (1) one command, as recommended by the Coma Recovery Scale-Revised (CRS-R), which was "open your mouth"; (2) placing a spoon in front of the patient's mouth without a command; (3) placing a spoon filled with water in front of the patient's mouth without a command; (4) one command-"there is a spoon; open your mouth"-with a spoon in front of the patient's mouth; (5) one command, "there is a spoon with water; open your mouth," with a spoon filled with water in front of the patient's mouth. All 19 patients were given these five stimuli randomly, and any one of the commands was presented four times to a patient, one at a time, at 15-s intervals. The sensitivity and specificity of the initiation of swallowing in detecting conscious awareness were determined. Results: None of the patients responded to the first four stimuli. However, six patients showed initiated swallowing toward the fifth stimulus. Among those six, five patients showed improvement in their consciousness state 6 months later. The sensitivity and specificity of the initiation of swallowing for DOC patients was 83.33% [95% CIs (36%, 100%)] and 92.31% [95% CIs (64%, 100%)], respectively. Conclusions: The initiation of swallowing can be an early indication of conscious behavior and can likely provide evidence of conscious awareness. Clinical Trial Registration: www.ClinicalTrials.gov, identifier: NCT03508336; Date of registration: 2018/4/16.

Keywords: consciousness; disorders of consciousness; minimally conscious state; prognosis; swallowing.

Copyright © 2019 Wang, Wang, Hu, Xu, Tian, Li, Fang, Huang, Sun, He, Laureys and Di.

Figures

Figure 1
Figure 1
Flow chart of patient selection in the study.
Figure 2
Figure 2
The incidence of the initiation of swallowing to different stimuli differed significantly between the fifth stimulus and the other four stimuli (Q = 24, **p < 0.01).

References

    1. Gosseries O, Di H, Laureys S, Boly M. Measuring consciousness in severely damaged brains. Ann Rev Neurosci. (2014) 37:457–78. 10.1146/annurev-neuro-062012-170339
    1. Owen AM, Coleman MR. Detecting awareness in the vegetative state. Ann N Y Acad Sci. (2008) 1129:130–8. 10.1196/annals.1417.018
    1. Giacino JT, Ashwal S, Childs N, Cranford R, Jennett B, Katz DI, et al. . The minimally conscious state: definition and diagnostic criteria. Neurology. (2002) 58:349–53. 10.1212/WNL.58.3.349
    1. Bruno MA, Vanhaudenhuyse A, Thibaut A, Moonen G, Laureys S. From unresponsive wakefulness to minimally conscious PLUS and functional locked-in syndromes: recent advances in our understanding of disorders of consciousness. J Neurol. (2011) 258:1373–84. 10.1007/s00415-011-6114-x
    1. Bruno M-A, Majerus S, Boly M, Vanhaudenhuyse A, Schnakers C, Gosseries O, et al. . Functional neuroanatomy underlying the clinical subcategorization of minimally conscious state patients. J Neurol. (2011) 259:1087–98. 10.1007/s00415-011-6303-7
    1. Andrews K. Medical decision making in the vegetative state: withdrawal of nutrition and hydration. NeuroRehabilitation. (2004) 19:299–304.
    1. Giacino JT, Schnakers C, Rodriguez-Moreno D, Kalmar K, Schiff N, Hirsch J. Behavioral assessment in patients with disorders of consciousness: gold standard or fool's gold? Progr Brain Res. (2009) 177:33–48. 10.1016/S0079-6123(09)17704-X
    1. Di H, He M, Zhang Y, Cheng L, Wang F, Nie Y, et al. . Chinese translation of the Coma Recovery Scale-Revised. Brain Injury. (2017) 31:363–5. 10.1080/02699052.2016.1255780
    1. Kalmar K, Giacino JT. The JFK coma recovery scale–revised. Neuropsychol Rehabil. (2005) 15:454–60. 10.1080/09602010443000425
    1. Andrews K, Murphy L, Munday R, Littlewood C. Misdiagnosis of the vegetative state: retrospective study in a rehabilitation unit. BMJ. (1996) 313:13–6. 10.1136/bmj.313.7048.13
    1. Gill-Thwaites H. Lotteries, loopholes and luck: misdiagnosis in the vegetative state patient. Brain Injury. (2009) 20:1321–8. 10.1080/02699050601081802
    1. Schnakers C, Vanhaudenhuyse A, Giacino J, Ventura M, Boly M, Majerus S, et al. . Diagnostic accuracy of the vegetative and minimally conscious state: clinical consensus versus standardized neurobehavioral assessment. BMC Neurol. (2009) 9:35. 10.1186/1471-2377-9-35
    1. American Congress of Rehabilitation Medicine BI-ISIGDoCTF. Seel RT, Sherer M, Whyte J, Katz DI, Giacino JT, et al. . Assessment scales for disorders of consciousness: evidence-based recommendations for clinical practice and research. Arch Phys Med Rehabil. (2010) 91:1795–813. 10.1016/j.apmr.2010.07.218
    1. Bodien YG, Carlowicz CA, Chatelle C, Giacino JT. Sensitivity and specificity of the coma recovery scale–revised total score in detection of conscious awareness. Arch Phys Med Rehabil. (2016) 97:490–2.e1. 10.1016/j.apmr.2015.08.422
    1. Schnakers C. Clinical assessment of patients with disorders of consciousness. Arch Ital Biol. (2012) 150:36–43. 10.4449/aib.v150i2.1371
    1. Xiao J, Xie Q, He Y, Yu T, Lu S, Huang N, et al. . An auditory BCI system for assisting CRS-R behavioral assessment in patients with disorders of consciousness. Sci Rep. (2016) 6:32917. 10.1038/srep32917
    1. Sun Y, Wang J, Heine L, Huang W, Wang J, Hu N, et al. . Personalized objects can optimize the diagnosis of EMCS in the assessment of functional object use in the CRS-R: a double blind, randomized clinical trial. BMC Neurol. (2018) 18:38. 10.1186/s12883-018-1040-5
    1. Bremare A, Rapin A, Veber B, Beuret-Blanquart F, Verin E. Swallowing disorders in severe brain injury in the arousal phase. Dysphagia. (2016) 31:511–20. 10.1007/s00455-016-9707-9
    1. Hansen TS, Engberg AW, Larsen K. Functional oral intake and time to reach unrestricted dieting for patients with traumatic brain injury. Arch Phys Med Rehabil. (2008) 89:1556–62. 10.1016/j.apmr.2007.11.063
    1. Ludlow CL. Central nervous system control of voice and swallowing. J Clin Neurophysiol. (2015) 32:294–303. 10.1097/WNP.0000000000000186
    1. Lowell SY, Reynolds RC, Chen G, Horwitz B, Ludlow CL. Functional connectivity and laterality of the motor and sensory components in the volitional swallowing network. Exp Brain Res. (2012) 219:85–96. 10.1007/s00221-012-3069-9
    1. Cheng L, Gosseries O, Ying L, Hu X, Yu D, Gao H, et al. . Assessment of localisation to auditory stimulation in post-comatose states: use the patient's own name. BMC Neurol. (2013) 13:27. 10.1186/1471-2377-13-27
    1. Giacino JT, Kalmar K, Whyte J. The JFK Coma Recovery Scale-Revised: measurement characteristics and diagnostic utility. Arch Phys Med Rehabil. (2004) 85:2020–9. 10.1016/j.apmr.2004.02.033
    1. Righard L, Alade MO. Effect of delivery room routines on success of first breast-feed. Lancet. (1990) 336:1105–7. 10.1016/0140-6736(90)92579-7
    1. Calabro RS, Nibali VC, Naro A, Floridia D, Pizzimenti M, Salmeri L, et al. . Is non-invasive neuromuscular electrical stimulation effective in severe chronic neurogenic dysphagia? Reporton a post-traumatic brain injury patient. NeuroRehabilitation. (2016) 38:53–7. 10.3233/NRE-151295
    1. Alhashemi HH. Dysphagia in severe traumatic brain injury. Neurosciences. (2010) 15:231–6.
    1. Buchholz DW. Dysphagia associated with neurological disorders. Acta otorhinolaryngol Belg. (1994) 48:143–55.
    1. Krakau K, Hansson A, Karlsson T, de Boussard CN, Tengvar C, Borg J. Nutritional treatment of patients with severe traumatic brain injury during the first six months after injury. Nutrition. (2007) 23:308–17. 10.1016/j.nut.2007.01.010
    1. Wieseke A, Bantz D, Siktberg L, Dillard N. Assessment and early diagnosis of dysphagia. Geriatr Nurs. (2008) 29:376–83. 10.1016/j.gerinurse.2007.12.001
    1. Sharon H, Pasternak Y, Ben Simon E, Gruberger M, Giladi N, Krimchanski B, et al. . Emotional processing of personally familiar faces in the vegetative state. PLoS ONE. (2013) 8:e74711. 10.1371/journal.pone.0074711
    1. Di HB, Yu SM, Weng XC, Laureys S, Yu D, Li JQ, et al. . Cerebral response to patient's own name in the vegetative and minimally conscious states. Neurology. (2007) 68:895–9. 10.1212/01.wnl.0000258544.79024.d0
    1. Wang F, Di H, Hu X, Jing S, Thibaut A, Di Perri C, et al. . Cerebral response to subject's own name showed high prognostic value in traumatic vegetative state. BMC Med. (2015) 13:83. 10.1186/s12916-015-0330-7
    1. Majerus S, Bruno MA, Schnakers C, Giacino JT, Laureys S. The problem of aphasia in the assessment of consciousness in brain-damaged patients. Coma Sci. (2009) 177:49–61. 10.1016/S0079-6123(09)17705-1
    1. Inatomi Y, Yonehara T, Omiya S, Hashimoto Y, Hirano T, Uchino M. Aphasia during the acute phase in ischemic stroke. Cerebrovasc Dis. (2008) 25:316–23. 10.1159/000118376
    1. Laska AC, Hellblom A, Murray V, Kahan T, Von Arbin M. Aphasia in acute stroke and relation to outcome. J Intern Med. (2001) 249:413–22. 10.1046/j.1365-2796.2001.00812.x
    1. Lhermitte F, Pillon B, Serdaru M. Human autonomy and the frontal lobes. Part I: imitation and utilization behavior: a neuropsychological study of 75 patients. Ann Neurol. (1986) 19:326–34. 10.1002/ana.410190404
    1. Terre R, Mearin F. Evolution of tracheal aspiration in severe traumatic brain injury-related oropharyngeal dysphagia: 1-year longitudinal follow-up study. Neurogastroenterol Motil. (2009) 21:361–9. 10.1111/j.1365-2982.2008.01208.x
    1. Mackay LE, Morgan AS, Bernstein BA. Swallowing disorders in severe brain injury: risk factors affecting return to oral intake. Arch Phys Med Rehabil. (1999) 80:365–71. 10.1016/S0003-9993(99)90271-X
    1. Pascarella A, Fiorenza S, Masotta O, Tibollo V, Vella D, Nardone AM, et al. . Multicentre registry of brain-injured patients with disorder of consciousness: rationale and preliminary data. Funct Neurol. (2018) 33:19–30. 10.11138/FNeur/2018.33.1.019
    1. Humbert IA, Robbins J. Normal swallowing and functional magnetic resonance imaging: a systematic review. Dysphagia. (2007) 22:266–75. 10.1007/s00455-007-9080-9
    1. Bekinschtein T, Leiguarda R, Armony J, Owen A, Carpintiero S, Niklison J, et al. . Emotion processing in the minimally conscious state. J Neurol Neurosurg Psychiatry. (2004) 75:788. 10.1136/jnnp.2003.034876

Source: PubMed

Sponsorit ja yhteistyökumppanit

Sairaudet

Huumeiden interventiot

3
Tilaa