NeuroRehabilitation AIIlntenllocipiinary JoulIIIl
ELSEVIER
NeuroRehabilitation 6 (1996) 3-8
Nomenclature: evolving trends Nathan D. Zasler 1 NNRC, Inc., 4198 Innslake Drive, GlennAllen, VA 23060, USA
Abstract In the past few years, there has been a burgeoning of interest in reassessing the appropriateness and applicability of historically well entrenched nomenclature germane to persons in low level neurological states following brain injury. Surprisingly, the effort to develop a cross-disciplinary uniform set of clinical definitions for low level states has only been a very recent endeavor within the neuroscience community. The intent of this review is to provide clinicians with a better understanding of some of the history and ongoing issues pertinent to appropriate diagnostic labeling and the ultimate rationale of a uniform terminology for this special population of neurologic patients.
Keywords: Nomenclature; Coma; Vegetative state
1. Introduction
Although coma and vegetative states have occurred since the beginning of time, it is only recently that cases of prolonged unconsciousness were documented in the medical literature. Probably, the first such documentation was made by Rosenblath in 1899. The patient was a young acrobat who incurred a severe traumatic brain injury (TBI) in a fall leaving him 'as if asleep.' He apparently died after nearly 1 year of tube feedings [1].
1 Director, Concussion Care Centres of America, Inc.; Director, Brain Injury Rehabilitation, Sheltering Arms Hospital; Consultant, NeuroRecovery Center, Stuart Circle Hospital; Director, Transitional Rehabilitation Services Richmond, Virginia
There was hardly any mention of states of protracted unconsciousness and unawareness following brain injury in the medical literature through the early part of this century. This is somewhat surprising given the large amount of literature published on neuropathology following severe traumatic brain injury in the earlier part of this century. After the 1940s, more literature was published, mostly in the form of case reports, of patients with uncommonly long periods of unconsciousness following TBI. Most authors described their patients based on clinical observations. Although a variety of 'terms' were coined to label such patients, there was no consistency across publications regarding the nomenclature used. Many of the terms used persisted in the literature for some time, others were as transient as the one publication that they appeared in. What became
1053-8135/96/$15.00 © 1996 Elsevier Science Ireland Ltd. All rights reserved. SSDI1053-8135(95)00143-V
4
N.D. Zasler / NeuroRehabilitation 6 (1996) 3-8
clearer, as we entered the latter part of the 20th century, was that there were serious problems with the terminology being utilized, as well as, a lack of consistency within and outside the field of neuromedical specialties relative to understanding the nomenclature being utilized and the conditions being described. Jennett and Plum [2] attempted to correct this problem with the introduction of the term persistent vegetative state in 1972. Since that time further advances have been made in trying to formulate the most appropriate nomenclature to describe persons in low level neurologic states following severe TBL Clinicians should have an understanding of the nomenclature evolution given the ongoing controversies and discussions in this area. Additionally, misperceptions continue to abound among the lay and professional community regarding many of the terms i.e. vegetative state being thought by many to imply that the patient is a 'vegetable'; clearly, a far cry from the original intent of the term. This paper will review the historical perspectives germane to 'low level' nomenclature, as well as, provide insights regarding the current evolving trends and controversies in the neuroscience community regarding terminology issues in this special population. 2. Nomenclature history One of the earliest terms utilized to described patients who were aroused but unaware was 'apallic syndrome'. This term, which in German is 'das apallische syndrome', was first coined by Kretschmer in 1940 [3] in a psychiatric publication. In the original paper, Kretschmer described the condition in two patients who lacked outward evidence of awareness and/or motivation but had periods of 'wakefulness'. He theorized that to be in such a state one would have to lose bihemispheric function with concurrent preservation of brain stem function. The term was used to describe parallel neurobehavioral states after a variety of central nervous system insults including trauma. One year after Kretschmer's report, Hugh Cairns [4] and his staff introduced the term 'akinetic mutism' to describe the behavior of a
young female with a third ventricle cystic tumor. The key neurobehavioral observations were the marked lack of movement and speech in a patient that was otherwise alert and visually tracking. Many English authors latched onto this phrase and often used it inappropriately to describe patient's who really did not fit the clinical picture originally described by Cairns and his co-workers, nor was there any consistency relative to the neuropathologic underpinnings. This phenomena is seen today in the neuroscience health care community as germane to the usage of the labels 'vegetative' and 'persistent vegetative state' in patients who are neither, that is, they do demonstrate some level of awareness, albeit at times intermittent and minimal. Subsequently, in 1968, Skultety [5] attempted to correlate and classify neuropathologic changes in persons who were akinetically mute. The diagnosis of akinetic mutism as a distinct clinical entity remains somewhat controversial as does the existence of specific neuropathologic correlates. Some professionals do believe that it is a distinct neurobehavioral entity with neuropathologic correlates [6,7]. Many within the field of neurorehabilitation believe that akinetic mutism is actually one subset of the minimally responsive sub-group of 'low level' or 'low responsiveness' patients. Geoffrey Jefferson [8] coined the term 'parasomnia' to describe a state of pathological sleep that was observed following traumatic brain injury. This term was specifically used in reference to those patients with rostral brain stem injury. In the late 1940s, Duensing [9] coined the phrase 'anoetischer symptomenkomplex' (translated: anoetic syndrome) to refer to the neurobehavioral condition of wakefulness and non-communication noted in patients with significant frontal lobe injuries. The term 'coma prolonge' (translated: prolonged unconsciousness) was defined by Le Beau [10] and co-workers in 1958 to denote a group of five patients with normal vegetative functions who survived for 4-9 months in unresponsive states of one sort or another. Neuropathologic· correlates were variable within this small group. Multiple synonyms have been noted in the scientific literature including: protracted unconsciousness [11],
N.D. Zasler / NeuroRehabilitation 6 (1996) 3-8
chronic consciousness disturbances [12], persistent coma [13], long-lasting unconsciousness [14], protracted comatose states [15], prolonged disorders of responsiveness [16], prolonged posttraumatic unawareness (PPTU) [17] and postcoma unawareness [18]. The French also utilized the term 'hypersomnies continues ou prolongees' (translated to mean: continuous or prolonged hypersomnia) during the 1950s and 1960s [19-21]. This phrase was used to describe both qualitative and quantitative alterations of sleep following potentially very different etiologies of brain injury and/or dysfunction. Another French term, coined by Fischgold and Mathis [22] in 1959, was 'stupeur hypertonique post-comateuse' (translated: hypertonic post-comatose stupor'). This phraseology was used to describe a group of patients who all eventually died after prolonged (6-8 months) periods of post-traumatic unconsciousness. Strich wrote about 'severe post-traumatic dementia' to describe patients following TBI who remained decerebrate and 'minimally responsive' (current terminology) until their demise [23]. Others have coined terms that emphasize the disordered motor control typically seen in this patient population. Such terms as 'decortication' [24], decerebrate rigidity [25], decerebrate state [26] and chronic brain stem syndrome (originator unknown) have all been utilized to express the abnormal tonal patterns in this population. Apallic syndrome continued to be 'in' phraseology through the early 1970s, in part due to a monograph published in 1967 by F. Gerstenbrand [27] on the same topic detailing over 70 cases of post-traumatic apallic state. Multiple interpretations of the condition and underlying neuropathology stemmed from Gerstenbrand's work including the tendency to group patients who had apallic syndrome features under this label, even if they were 'minimally responsive'. This tendency to 'lump' patients inappropriately again brings to light the point of the inherent dangers in having overly broad categories and/or a poor understanding of behavioral assessment in this patient population. In part, the aforementioned concern eventually stimulated professionals to develop alternative behavioral categories such as minimally
5
responsive states which has in and of itself both clinical practice and research implications [28]. Ingvar and Brun [29] proposed the terms dyspallic or incomplete apallic syndrome for patients whose neurobehavioral condition fall outside of the strict traditional definition. They proposed that the term 'complete apallic syndrome' be used only when there was: (1) no telencephalic function; (2) an isoelectric electroencephalogram; and (3) significantly reduced hemispheric cerebral blood flow and metabolism. Other investigators proposed alternative terms for patients who were arousable but not aware. Alajouanine [30] introduced a term which was used quite extensively in France; specifically, 'coma vigil' (translated: vigilant coma). Arnaud [31] coined the phrase 'vie vegetative' (translated: vegetative life) in 1963. This is the first reference to 'vegetative' that this author is aware of in the literature. The phrase 'vegetative survival' was suggested by Vapalahti and Troupp in 1971 [32]. Following this, Jennett and Plum [2] coined the now well accepted and seemingly well entrenched term 'persistent vegetative state'. The authors attempted to define this condition with fairly specific behavioral parameters and without an attempt to correlate neuropathology. They also were astute to point out that there was not adequate data, at that time, to determine absolute irreversibility of the condition. Clearly, however, there were problems with this terminology as many patients did indeed not 'persist' in this state and went on to make further neurological improvement. As a matter of fact, PVS became the most widely misused term relevant to the clinical diagnosis and care of the severely impaired patient following brain injury. The consequences of such misuse have many times been profound; including, but not limited to, withdrawal and withholding of care, failure to refer for rehabilitation services, discontinuation of rehabilitation efforts, and tendencies towards less aggressive management of comorbidity factors. Since the 1970s, there was not much of a demonstrated need on the part of the neuroscience community to develop new nomenclature until quite recently. Clinicians seemed satisfied with 'PVS' to describe patients following trauma and
6
N.D. Zasler / NeuroRehabilitation 6 (J996) 3-8
other conditions who had protracted periods of wakeful unconsciousness. Israeli investigators have introduced two alternative phrases into the literature on this topic. Sazbon and Groswasser coined the phrases 'prolonged post-traumatic unawareness' (PPTU), as well as, 'post-coma unawareness' (PC-U) [17,18]. Neither of these phrases really ever caught on in the U.S. health care community. Most recently, there has been further introspection regarding nomenclature issues in this population [33]. This effort has been further spearheaded by several 'special interest groups' within the neuroscience community. These groups initially work within their own camps but more recently joining forces to produce an ongoing collaborative effort. Recent meetings in London, England and Aspen, Colorado have brought together some of the leaders in the field of brain injury care to discuss this topic, as well as, other issues germane to the diagnosis and treatment of 'low level' neurologic states following TBI. To date, it appears that many influential clinicians, including B. Jennett, co-author of the original Lancet article first proposing the term [34], are advocating for dispensing with the use of the modifier 'persistent' due to the fact that it adds little if anything to the neurologic and/or neurobehavioral diagnostic or prognostic accuracy. At the same time, however there has been general agreement to endorse the phrases 'vegetative state' and 'permanent vegetative state'. Specifically, patients in the vegetative state (VS) demonstrate arousal without behavioral evidence of the capacity to interact with the environment. Neurobehaviorally, there are periods of eye opening, either spontaneously or following stimulation; subcortical responses to external stimulation including generalized physiologic responses to pain such as posturing, tachycardia" and diaphoresis, as well as subcortical motor responses such as a grasp reflex; return of so-called vegetative (autonomic) functions including sleep wake cycles, and normalization of respiratory and digestive system functions; and there may be roving eye movements without concomitant visual tracking ability [28]. Patients in permanent vegetative states (PVS)
meet all the criteria behaviorally that patients in vegetative state do. This prognostic label should only be utilized when there has been an adequate period of extended patient observation and adequate medical assessment to rule-out conditions potentially adversely affecting ongoing recovery and/or behavioral assessment. Clinicians should adhere to a time frame of I year for traumatic and 3 months following hypoxic-ischemic brain injury before adding the modifier 'permanent' to the diagnosis of vegetative state [33]. One concern with the modifier 'permanent' is that many clinicians do not believe that the vegetative state can be definitively (implying with 100% certainty) termed 'permanent' given the number, albeit small, of documented cases of recovery that exceed this time frame [7]. Furthermore, there has been little methodologically sound research examining long-term (1-15 years) recovery and/or treatment methodologies for this population. Some clinicians, including this author, have concerns that introduction of the term 'permanent vegetative state' only serves to create a selfprophesizing environment which surely does not encourage clinicians and scientists to pursue treatments which may ameliorate if not cure the condition [35]. Lastly, clinicians have recently introduced the term 'minimally responsive state' to describe those individuals following trauma or hypoxic ischemic brain injury who are severely disabled but demonstrating some level of demonstrable internal or external awareness [28]. This group of patients has historically been ignored by the neurological community relative to being identified as a discrete or quasidiscrete patient population. In actuality, little to no literature exists relative to either clinical diagnosis and/or assessment of this sub-group of 'low level' patients. Neither does there exist a historical literature germane to assignation of viable neurobehavioral descriptors. There are clear implications for clinical practice in terms of the ramifications of such a behavioral sub-categorization relative to initial assessment strategies, outcome prognostication, and clinical treatment that are profoundly disparate from those germane to patients in vegetative or permanent vegetative state. Further discussion and re-
N.D. Zasler / NeuroRehabilitation 6 (J996) 3-8
search is absolutely necessary to more specifically define the incidence, prevalence, outcome and treatment strategies for this sub-group of patients before any practice guidelines can be proposed, even on a preliminary basis. 3. Nomenclature rationale A concerted effort is needed to reach consensus opinion across all neuroscience disciplines as to the appropriate nomenclature germane to this special patient population. The rationale for coming to 'terms' with this nomenclature is several fold: (1) to classify patients for research purposes; (2) to insure that we are comparing 'apples with apples'; (3) to better identify early markers of good versus bad neurologic prognosis; (4) to allow for appropriate ethical and legal decisions; and (5) to guide efforts at maintenance, prevention as well as rehabilitation including potential discontinuance of care (withdrawal and/or withholding). Some researches have tried to summarize what any term or phrase should provide to be considered 'good' nomenclature. A summary of these criteria include: (1) the term should be descriptive; (2) the full spectrum of the 'syndrome' should be encompassed; (3) implications regarding unknowns should be included; (4) the nomenclature should be accurate pathophysiologically; (5) the terminology should be respectful and 'user friendly'; (6) survivors, families, payors and clinicians alike should understand it; (7) avoidance of eponymous names i.e. call it what it is not what it's not; (8) everyone should agree to use it.
References [1] [2] [3] [4] [5] [6] [7]
[8] [9] [10] [11] [12]
[13]
[14]
4. Conclusions The contemplation, consternation, and collaboration continue. We ultimately must continue to strive towards a uniform nomenclature defining the spectrum of neurobehavioral conditions noted following severe traumatic brain injury. This effort must be multidisciplinary as well as interdisciplinary if it is expected to effectuate any tangible changes in the way these patients are diagnosed and managed, both in the acute as well as post-acute arena.
7
[15)
[16] [17]
Rosenblath W. Uber einen bemerkenswerten Fall von Hirnerschutterung (aus dem Landkrankenhaus Kassel). Arch K1in Med 1899;64:406-424. Jennett B, Plum F. Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet 1972;1:734-737. Kretschmer E. Das appalli8sche Syndrom Zbl. ges. Neurol. Psychiatrist 1940;169:576-579. Cairns H, Oldfield RC, Pennybacker JB et al. Akinetic mutism with an epidermoid cyst of the third ventricle. Brain 1941;64:273-290. Skultety FM. Clinical and experimental aspects of akinetic mutism. Arch NeuroI1968;19:1-14. Nemeth G, Hegedus K, Monar L. Akinetic mutism and locked-in syndrome: The functional anatomical basis for their differentiation. Funct Neurol 1986;1(2):128-139. Giacino JT, Zasler ND, Whyte J et al. Recommendations for Use of Uniform Nomenclature Pertinent to Patients with Severe Alterations in Consciousness. Arch Phys Med Rehabil 1995;76:205-209. Jefferson G. The nature of concussion. Sr Med J 1994;1:1-5. Duensing F. Das Elektroenzephalogramm bei Storungen der BewuBtseinslage. Arch Psychiatr Nervenkr 1949;183:71-115. Le Beau J, Funck-Brentano JL, Castaigne P. Le traitement des comas prolonges. Presse Med 1958;66:829-833. Jacobson SA. Protracted unconscousness due to closed head injury. Neurology 1956;6:281-287. Jouvet M, Pellin S, Mounier, D. Etude Polygraphique des differentes phases du sommeil au cours des troubles de conscience chroniques (comas prolonges). Rev Neurol 1961;105:181-186. Carlsson CA, Von Essen C, Lofgren J. Factors affecting the clinical course of patients with severe head injuries. Part 1: Influence of biological factors. Part 2: Significance of post-traumatic coma. J Neurosurg 1968;29:242-251. Bricolo A, Gentilomo, Rosadine R, Rossi GR. Long lasting post-traumatic unconsciousness. A study based on nocturnal EEG and polygraphic recording. Acta Neurol Scan 1968b;4:512-532. Wieck H, Rottelbach R, Heerklotz B, Flugel K. Courses of protracted states of coma. In: The Apallic Syndrom, Proc. Conferenza Veronese sulla Sindrome Apallica, Valeggio sui Mincio. Heidelberg, Springer: Monographien aus dem Gesamtgebiete der Psychiatrie, 1970. Jellinger K. Nervous system lesions in prolonged disorders of responsiveness. Communicat. Danube Symposium of Neurology and Neuropathology, Warsaw, 1972. Sazbon L, Groswasser Z. Outcome in 134 patients with prolonged post-traumatic unawareness. Part 1: Parameters determining late recovery of consciousness. J Neurosurg 1990;72:75-80.
8 [18]
[19]
[20]
[21]
[22] [23]
[24] [25]
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Sazbon L, Groswasser Z. Prolonged coma, vegetative state, post-comatose unawareness: Semantics or better understandings? Brain Injury, 1995;(5)1:1-2. Facon R, Steriade M, Wertheim N. Hypersomnie prolongee engendree par des lesions bilaterales du systeme activateru medial. Le syndrome thrombotique de la bifurcation du tronc basilaire. Rev Neurol 1958;98:117-133. Castaigne P, Buge A, Escourolle R, Masson M. Ramollissement pedunculaire median tegmentothalamique avec ophtalmoplegie et hypersomnie (Etude ana tomeclinique). Rev Neurol 1962;106:357-367. Thiebaut F, Rohner F, Kurtz D. Les hypersomnies symptomatiques continues (Etude clinique et electroencephalographique). Rev Neurol 1967;116:491-546. Fischgold H, Mathis P. Obnubilations, comas et stupeurs. Paris: Masson et Cie, 1959;125. Strich S]. Diffuse degeneration of cerebral while matter in severe dementia following head injury. ] Neurol Neurosurg Psychiatr 1956;19:163-185. Nystrom S. A case of decortication following a severe head injury. Acta Psychiat Scand 1960;35:101-112. Scarcella AG, Fiels W. Recovery from coma and ecerebrated rigidity of young patients following head injury. Acta Neurochir (Wein) 1962;10:134-144.
[26]
[27] [28]
[29] [30]
[31]
[32] [33]
[34] [35]
Freedman H. Recovery from the decerebrate state associated with supratentorial space-taking lesions. J Neurosurg 1952;9:52-58. Gerstenbrand F. Das traumatisch appalische Syndrome. New York: Springer, 1967. Giacino JT, Zasler ND. Outcome following severe brain injury: The comatose, vegetative and minimally responsive patient. J Head Trauma Rehabil 1995;10(1):40-56. Ingvar DH, Brun A. Das komplette apailische Syndrom. Arch. Psvchiat. Nervenkr 1972;215:219-239. Alajouanine T. Les alterations des etats de conscience causes par les desordres neurologiques. Bruxelles, I Congress International Science Neurology Acta Medical Belgium 1957;2:19-41. Arnaud M, Vigouroux R, Vigouroux M. Etats frontiers entre la vie et la mort en nero-traumatologie Neurochiriurgia (Stuttg.) 1963;6:1-21. Vapalahti M, Troupp H. Prognosis for patients with severe brain injuries. Br Med J 1971;404-407. Multi-society task force on PVS Medical aspects of the persistent vegetative state: Statement of a multi-society task force. New Engl J Med 330, 1994;21:1499-1508. Jennett B. Personal communication, 1995. Young W. Personal communication, 1994.
ELSEVIER
NeuroRehabilitation 6 (1996) 3-8
Nomenclature: evolving trends Nathan D. Zasler 1 NNRC, Inc., 4198 Innslake Drive, GlennAllen, VA 23060, USA
Abstract In the past few years, there has been a burgeoning of interest in reassessing the appropriateness and applicability of historically well entrenched nomenclature germane to persons in low level neurological states following brain injury. Surprisingly, the effort to develop a cross-disciplinary uniform set of clinical definitions for low level states has only been a very recent endeavor within the neuroscience community. The intent of this review is to provide clinicians with a better understanding of some of the history and ongoing issues pertinent to appropriate diagnostic labeling and the ultimate rationale of a uniform terminology for this special population of neurologic patients.
Keywords: Nomenclature; Coma; Vegetative state
1. Introduction
Although coma and vegetative states have occurred since the beginning of time, it is only recently that cases of prolonged unconsciousness were documented in the medical literature. Probably, the first such documentation was made by Rosenblath in 1899. The patient was a young acrobat who incurred a severe traumatic brain injury (TBI) in a fall leaving him 'as if asleep.' He apparently died after nearly 1 year of tube feedings [1].
1 Director, Concussion Care Centres of America, Inc.; Director, Brain Injury Rehabilitation, Sheltering Arms Hospital; Consultant, NeuroRecovery Center, Stuart Circle Hospital; Director, Transitional Rehabilitation Services Richmond, Virginia
There was hardly any mention of states of protracted unconsciousness and unawareness following brain injury in the medical literature through the early part of this century. This is somewhat surprising given the large amount of literature published on neuropathology following severe traumatic brain injury in the earlier part of this century. After the 1940s, more literature was published, mostly in the form of case reports, of patients with uncommonly long periods of unconsciousness following TBI. Most authors described their patients based on clinical observations. Although a variety of 'terms' were coined to label such patients, there was no consistency across publications regarding the nomenclature used. Many of the terms used persisted in the literature for some time, others were as transient as the one publication that they appeared in. What became
1053-8135/96/$15.00 © 1996 Elsevier Science Ireland Ltd. All rights reserved. SSDI1053-8135(95)00143-V
4
N.D. Zasler / NeuroRehabilitation 6 (1996) 3-8
clearer, as we entered the latter part of the 20th century, was that there were serious problems with the terminology being utilized, as well as, a lack of consistency within and outside the field of neuromedical specialties relative to understanding the nomenclature being utilized and the conditions being described. Jennett and Plum [2] attempted to correct this problem with the introduction of the term persistent vegetative state in 1972. Since that time further advances have been made in trying to formulate the most appropriate nomenclature to describe persons in low level neurologic states following severe TBL Clinicians should have an understanding of the nomenclature evolution given the ongoing controversies and discussions in this area. Additionally, misperceptions continue to abound among the lay and professional community regarding many of the terms i.e. vegetative state being thought by many to imply that the patient is a 'vegetable'; clearly, a far cry from the original intent of the term. This paper will review the historical perspectives germane to 'low level' nomenclature, as well as, provide insights regarding the current evolving trends and controversies in the neuroscience community regarding terminology issues in this special population. 2. Nomenclature history One of the earliest terms utilized to described patients who were aroused but unaware was 'apallic syndrome'. This term, which in German is 'das apallische syndrome', was first coined by Kretschmer in 1940 [3] in a psychiatric publication. In the original paper, Kretschmer described the condition in two patients who lacked outward evidence of awareness and/or motivation but had periods of 'wakefulness'. He theorized that to be in such a state one would have to lose bihemispheric function with concurrent preservation of brain stem function. The term was used to describe parallel neurobehavioral states after a variety of central nervous system insults including trauma. One year after Kretschmer's report, Hugh Cairns [4] and his staff introduced the term 'akinetic mutism' to describe the behavior of a
young female with a third ventricle cystic tumor. The key neurobehavioral observations were the marked lack of movement and speech in a patient that was otherwise alert and visually tracking. Many English authors latched onto this phrase and often used it inappropriately to describe patient's who really did not fit the clinical picture originally described by Cairns and his co-workers, nor was there any consistency relative to the neuropathologic underpinnings. This phenomena is seen today in the neuroscience health care community as germane to the usage of the labels 'vegetative' and 'persistent vegetative state' in patients who are neither, that is, they do demonstrate some level of awareness, albeit at times intermittent and minimal. Subsequently, in 1968, Skultety [5] attempted to correlate and classify neuropathologic changes in persons who were akinetically mute. The diagnosis of akinetic mutism as a distinct clinical entity remains somewhat controversial as does the existence of specific neuropathologic correlates. Some professionals do believe that it is a distinct neurobehavioral entity with neuropathologic correlates [6,7]. Many within the field of neurorehabilitation believe that akinetic mutism is actually one subset of the minimally responsive sub-group of 'low level' or 'low responsiveness' patients. Geoffrey Jefferson [8] coined the term 'parasomnia' to describe a state of pathological sleep that was observed following traumatic brain injury. This term was specifically used in reference to those patients with rostral brain stem injury. In the late 1940s, Duensing [9] coined the phrase 'anoetischer symptomenkomplex' (translated: anoetic syndrome) to refer to the neurobehavioral condition of wakefulness and non-communication noted in patients with significant frontal lobe injuries. The term 'coma prolonge' (translated: prolonged unconsciousness) was defined by Le Beau [10] and co-workers in 1958 to denote a group of five patients with normal vegetative functions who survived for 4-9 months in unresponsive states of one sort or another. Neuropathologic· correlates were variable within this small group. Multiple synonyms have been noted in the scientific literature including: protracted unconsciousness [11],
N.D. Zasler / NeuroRehabilitation 6 (1996) 3-8
chronic consciousness disturbances [12], persistent coma [13], long-lasting unconsciousness [14], protracted comatose states [15], prolonged disorders of responsiveness [16], prolonged posttraumatic unawareness (PPTU) [17] and postcoma unawareness [18]. The French also utilized the term 'hypersomnies continues ou prolongees' (translated to mean: continuous or prolonged hypersomnia) during the 1950s and 1960s [19-21]. This phrase was used to describe both qualitative and quantitative alterations of sleep following potentially very different etiologies of brain injury and/or dysfunction. Another French term, coined by Fischgold and Mathis [22] in 1959, was 'stupeur hypertonique post-comateuse' (translated: hypertonic post-comatose stupor'). This phraseology was used to describe a group of patients who all eventually died after prolonged (6-8 months) periods of post-traumatic unconsciousness. Strich wrote about 'severe post-traumatic dementia' to describe patients following TBI who remained decerebrate and 'minimally responsive' (current terminology) until their demise [23]. Others have coined terms that emphasize the disordered motor control typically seen in this patient population. Such terms as 'decortication' [24], decerebrate rigidity [25], decerebrate state [26] and chronic brain stem syndrome (originator unknown) have all been utilized to express the abnormal tonal patterns in this population. Apallic syndrome continued to be 'in' phraseology through the early 1970s, in part due to a monograph published in 1967 by F. Gerstenbrand [27] on the same topic detailing over 70 cases of post-traumatic apallic state. Multiple interpretations of the condition and underlying neuropathology stemmed from Gerstenbrand's work including the tendency to group patients who had apallic syndrome features under this label, even if they were 'minimally responsive'. This tendency to 'lump' patients inappropriately again brings to light the point of the inherent dangers in having overly broad categories and/or a poor understanding of behavioral assessment in this patient population. In part, the aforementioned concern eventually stimulated professionals to develop alternative behavioral categories such as minimally
5
responsive states which has in and of itself both clinical practice and research implications [28]. Ingvar and Brun [29] proposed the terms dyspallic or incomplete apallic syndrome for patients whose neurobehavioral condition fall outside of the strict traditional definition. They proposed that the term 'complete apallic syndrome' be used only when there was: (1) no telencephalic function; (2) an isoelectric electroencephalogram; and (3) significantly reduced hemispheric cerebral blood flow and metabolism. Other investigators proposed alternative terms for patients who were arousable but not aware. Alajouanine [30] introduced a term which was used quite extensively in France; specifically, 'coma vigil' (translated: vigilant coma). Arnaud [31] coined the phrase 'vie vegetative' (translated: vegetative life) in 1963. This is the first reference to 'vegetative' that this author is aware of in the literature. The phrase 'vegetative survival' was suggested by Vapalahti and Troupp in 1971 [32]. Following this, Jennett and Plum [2] coined the now well accepted and seemingly well entrenched term 'persistent vegetative state'. The authors attempted to define this condition with fairly specific behavioral parameters and without an attempt to correlate neuropathology. They also were astute to point out that there was not adequate data, at that time, to determine absolute irreversibility of the condition. Clearly, however, there were problems with this terminology as many patients did indeed not 'persist' in this state and went on to make further neurological improvement. As a matter of fact, PVS became the most widely misused term relevant to the clinical diagnosis and care of the severely impaired patient following brain injury. The consequences of such misuse have many times been profound; including, but not limited to, withdrawal and withholding of care, failure to refer for rehabilitation services, discontinuation of rehabilitation efforts, and tendencies towards less aggressive management of comorbidity factors. Since the 1970s, there was not much of a demonstrated need on the part of the neuroscience community to develop new nomenclature until quite recently. Clinicians seemed satisfied with 'PVS' to describe patients following trauma and
6
N.D. Zasler / NeuroRehabilitation 6 (J996) 3-8
other conditions who had protracted periods of wakeful unconsciousness. Israeli investigators have introduced two alternative phrases into the literature on this topic. Sazbon and Groswasser coined the phrases 'prolonged post-traumatic unawareness' (PPTU), as well as, 'post-coma unawareness' (PC-U) [17,18]. Neither of these phrases really ever caught on in the U.S. health care community. Most recently, there has been further introspection regarding nomenclature issues in this population [33]. This effort has been further spearheaded by several 'special interest groups' within the neuroscience community. These groups initially work within their own camps but more recently joining forces to produce an ongoing collaborative effort. Recent meetings in London, England and Aspen, Colorado have brought together some of the leaders in the field of brain injury care to discuss this topic, as well as, other issues germane to the diagnosis and treatment of 'low level' neurologic states following TBI. To date, it appears that many influential clinicians, including B. Jennett, co-author of the original Lancet article first proposing the term [34], are advocating for dispensing with the use of the modifier 'persistent' due to the fact that it adds little if anything to the neurologic and/or neurobehavioral diagnostic or prognostic accuracy. At the same time, however there has been general agreement to endorse the phrases 'vegetative state' and 'permanent vegetative state'. Specifically, patients in the vegetative state (VS) demonstrate arousal without behavioral evidence of the capacity to interact with the environment. Neurobehaviorally, there are periods of eye opening, either spontaneously or following stimulation; subcortical responses to external stimulation including generalized physiologic responses to pain such as posturing, tachycardia" and diaphoresis, as well as subcortical motor responses such as a grasp reflex; return of so-called vegetative (autonomic) functions including sleep wake cycles, and normalization of respiratory and digestive system functions; and there may be roving eye movements without concomitant visual tracking ability [28]. Patients in permanent vegetative states (PVS)
meet all the criteria behaviorally that patients in vegetative state do. This prognostic label should only be utilized when there has been an adequate period of extended patient observation and adequate medical assessment to rule-out conditions potentially adversely affecting ongoing recovery and/or behavioral assessment. Clinicians should adhere to a time frame of I year for traumatic and 3 months following hypoxic-ischemic brain injury before adding the modifier 'permanent' to the diagnosis of vegetative state [33]. One concern with the modifier 'permanent' is that many clinicians do not believe that the vegetative state can be definitively (implying with 100% certainty) termed 'permanent' given the number, albeit small, of documented cases of recovery that exceed this time frame [7]. Furthermore, there has been little methodologically sound research examining long-term (1-15 years) recovery and/or treatment methodologies for this population. Some clinicians, including this author, have concerns that introduction of the term 'permanent vegetative state' only serves to create a selfprophesizing environment which surely does not encourage clinicians and scientists to pursue treatments which may ameliorate if not cure the condition [35]. Lastly, clinicians have recently introduced the term 'minimally responsive state' to describe those individuals following trauma or hypoxic ischemic brain injury who are severely disabled but demonstrating some level of demonstrable internal or external awareness [28]. This group of patients has historically been ignored by the neurological community relative to being identified as a discrete or quasidiscrete patient population. In actuality, little to no literature exists relative to either clinical diagnosis and/or assessment of this sub-group of 'low level' patients. Neither does there exist a historical literature germane to assignation of viable neurobehavioral descriptors. There are clear implications for clinical practice in terms of the ramifications of such a behavioral sub-categorization relative to initial assessment strategies, outcome prognostication, and clinical treatment that are profoundly disparate from those germane to patients in vegetative or permanent vegetative state. Further discussion and re-
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search is absolutely necessary to more specifically define the incidence, prevalence, outcome and treatment strategies for this sub-group of patients before any practice guidelines can be proposed, even on a preliminary basis. 3. Nomenclature rationale A concerted effort is needed to reach consensus opinion across all neuroscience disciplines as to the appropriate nomenclature germane to this special patient population. The rationale for coming to 'terms' with this nomenclature is several fold: (1) to classify patients for research purposes; (2) to insure that we are comparing 'apples with apples'; (3) to better identify early markers of good versus bad neurologic prognosis; (4) to allow for appropriate ethical and legal decisions; and (5) to guide efforts at maintenance, prevention as well as rehabilitation including potential discontinuance of care (withdrawal and/or withholding). Some researches have tried to summarize what any term or phrase should provide to be considered 'good' nomenclature. A summary of these criteria include: (1) the term should be descriptive; (2) the full spectrum of the 'syndrome' should be encompassed; (3) implications regarding unknowns should be included; (4) the nomenclature should be accurate pathophysiologically; (5) the terminology should be respectful and 'user friendly'; (6) survivors, families, payors and clinicians alike should understand it; (7) avoidance of eponymous names i.e. call it what it is not what it's not; (8) everyone should agree to use it.
References [1] [2] [3] [4] [5] [6] [7]
[8] [9] [10] [11] [12]
[13]
[14]
4. Conclusions The contemplation, consternation, and collaboration continue. We ultimately must continue to strive towards a uniform nomenclature defining the spectrum of neurobehavioral conditions noted following severe traumatic brain injury. This effort must be multidisciplinary as well as interdisciplinary if it is expected to effectuate any tangible changes in the way these patients are diagnosed and managed, both in the acute as well as post-acute arena.
7
[15)
[16] [17]
Rosenblath W. Uber einen bemerkenswerten Fall von Hirnerschutterung (aus dem Landkrankenhaus Kassel). Arch K1in Med 1899;64:406-424. Jennett B, Plum F. Persistent vegetative state after brain damage. A syndrome in search of a name. Lancet 1972;1:734-737. Kretschmer E. Das appalli8sche Syndrom Zbl. ges. Neurol. Psychiatrist 1940;169:576-579. Cairns H, Oldfield RC, Pennybacker JB et al. Akinetic mutism with an epidermoid cyst of the third ventricle. Brain 1941;64:273-290. Skultety FM. Clinical and experimental aspects of akinetic mutism. Arch NeuroI1968;19:1-14. Nemeth G, Hegedus K, Monar L. Akinetic mutism and locked-in syndrome: The functional anatomical basis for their differentiation. Funct Neurol 1986;1(2):128-139. Giacino JT, Zasler ND, Whyte J et al. Recommendations for Use of Uniform Nomenclature Pertinent to Patients with Severe Alterations in Consciousness. Arch Phys Med Rehabil 1995;76:205-209. Jefferson G. The nature of concussion. Sr Med J 1994;1:1-5. Duensing F. Das Elektroenzephalogramm bei Storungen der BewuBtseinslage. Arch Psychiatr Nervenkr 1949;183:71-115. Le Beau J, Funck-Brentano JL, Castaigne P. Le traitement des comas prolonges. Presse Med 1958;66:829-833. Jacobson SA. Protracted unconscousness due to closed head injury. Neurology 1956;6:281-287. Jouvet M, Pellin S, Mounier, D. Etude Polygraphique des differentes phases du sommeil au cours des troubles de conscience chroniques (comas prolonges). Rev Neurol 1961;105:181-186. Carlsson CA, Von Essen C, Lofgren J. Factors affecting the clinical course of patients with severe head injuries. Part 1: Influence of biological factors. Part 2: Significance of post-traumatic coma. J Neurosurg 1968;29:242-251. Bricolo A, Gentilomo, Rosadine R, Rossi GR. Long lasting post-traumatic unconsciousness. A study based on nocturnal EEG and polygraphic recording. Acta Neurol Scan 1968b;4:512-532. Wieck H, Rottelbach R, Heerklotz B, Flugel K. Courses of protracted states of coma. In: The Apallic Syndrom, Proc. Conferenza Veronese sulla Sindrome Apallica, Valeggio sui Mincio. Heidelberg, Springer: Monographien aus dem Gesamtgebiete der Psychiatrie, 1970. Jellinger K. Nervous system lesions in prolonged disorders of responsiveness. Communicat. Danube Symposium of Neurology and Neuropathology, Warsaw, 1972. Sazbon L, Groswasser Z. Outcome in 134 patients with prolonged post-traumatic unawareness. Part 1: Parameters determining late recovery of consciousness. J Neurosurg 1990;72:75-80.
8 [18]
[19]
[20]
[21]
[22] [23]
[24] [25]
N.D. Zasler / NeuroRehabilitation 6 (1996) 3-8
Sazbon L, Groswasser Z. Prolonged coma, vegetative state, post-comatose unawareness: Semantics or better understandings? Brain Injury, 1995;(5)1:1-2. Facon R, Steriade M, Wertheim N. Hypersomnie prolongee engendree par des lesions bilaterales du systeme activateru medial. Le syndrome thrombotique de la bifurcation du tronc basilaire. Rev Neurol 1958;98:117-133. Castaigne P, Buge A, Escourolle R, Masson M. Ramollissement pedunculaire median tegmentothalamique avec ophtalmoplegie et hypersomnie (Etude ana tomeclinique). Rev Neurol 1962;106:357-367. Thiebaut F, Rohner F, Kurtz D. Les hypersomnies symptomatiques continues (Etude clinique et electroencephalographique). Rev Neurol 1967;116:491-546. Fischgold H, Mathis P. Obnubilations, comas et stupeurs. Paris: Masson et Cie, 1959;125. Strich S]. Diffuse degeneration of cerebral while matter in severe dementia following head injury. ] Neurol Neurosurg Psychiatr 1956;19:163-185. Nystrom S. A case of decortication following a severe head injury. Acta Psychiat Scand 1960;35:101-112. Scarcella AG, Fiels W. Recovery from coma and ecerebrated rigidity of young patients following head injury. Acta Neurochir (Wein) 1962;10:134-144.
[26]
[27] [28]
[29] [30]
[31]
[32] [33]
[34] [35]
Freedman H. Recovery from the decerebrate state associated with supratentorial space-taking lesions. J Neurosurg 1952;9:52-58. Gerstenbrand F. Das traumatisch appalische Syndrome. New York: Springer, 1967. Giacino JT, Zasler ND. Outcome following severe brain injury: The comatose, vegetative and minimally responsive patient. J Head Trauma Rehabil 1995;10(1):40-56. Ingvar DH, Brun A. Das komplette apailische Syndrom. Arch. Psvchiat. Nervenkr 1972;215:219-239. Alajouanine T. Les alterations des etats de conscience causes par les desordres neurologiques. Bruxelles, I Congress International Science Neurology Acta Medical Belgium 1957;2:19-41. Arnaud M, Vigouroux R, Vigouroux M. Etats frontiers entre la vie et la mort en nero-traumatologie Neurochiriurgia (Stuttg.) 1963;6:1-21. Vapalahti M, Troupp H. Prognosis for patients with severe brain injuries. Br Med J 1971;404-407. Multi-society task force on PVS Medical aspects of the persistent vegetative state: Statement of a multi-society task force. New Engl J Med 330, 1994;21:1499-1508. Jennett B. Personal communication, 1995. Young W. Personal communication, 1994.
