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Brain Function in the Vegetative State

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Brain Function in the Vegetative State Acta neurol. belg., 2002, 102, 177-185 Brain function in the vegetative state Steven LAUREYS1,2,6, Sylvie ANTOINE5, Melanie BOLY1,2, Sandra ELINCX6, Marie-Elisabeth FAYMONVILLE3, Jacques BERRÉ7, Bernard SADZOT2, Martine FERRING7, Xavier DE TIÈGE6, Patrick VA N BOGAERT6, Isabelle HANSEN2, Pierre DAMAS3, Nicolas MAVROUDAKIS8, Bernard LAMBERMONT4, Guy DEL FIORE1, Joël AERTS1, Christian DEGUELDRE1, Christophe PHILLIPS1, George FRANCK2, Jean-Louis VINCENT7, Maurice LAMY3, André LUXEN1, Gustave MOONEN2, Serge GOLDMAN6 and Pierre MAQUET1,2 1Cyclotron Research Center, 2Department of Neurology, 3Anesthesiology and Intensive Care Medicine and 4Internal Medicine, CHU Sart Tilman, University of Liège, Liège, 5Department of Neurology, AZ-VUB, Brussels, 6PET/Biomedical Cyclotron Unit and 7Department of Intensive Care and 8Neurology, ULB Erasme, Brussels, Belgium ———— Abstract Some of these patients recover from their coma Positron emission tomography (PET) techniques rep- within the first days after the insult, others will take resent a useful tool to better understand the residual more time and go through different stages before brain function in vegetative state patients. It has been fully or partially recovering awareness (e.g., mini- shown that overall cerebral metabolic rates for glucose mally conscious state, vegetative state) or will per- are massively reduced in this condition. However, the manently lose all brain functions (i.e., brain death). recovery of consciousness from vegetative state is not Clinical practice shows how puzzling it is to recog- always associated with substantial changes in global nize unambiguous signs of conscious perception of metabolism. This finding led us to hypothesize that some the environment and of the self in these patients. vegetative patients are unconscious not just because of a This difficulty is reflected by frequent misdiag- global loss of neuronal function, but rather due to an noses of locked-in syndrome, coma, minimally altered activity in some critical brain regions and to the et al. abolished functional connections between them. We used conscious state and vegetative state (Childs , voxel-based Statistical Parametric Mapping (SPM) 1993 ; Andrews et al., 1996). Objective assessment approaches to characterize the functional neuroanatomy of residual brain function is difficult in patients of the vegetative state. The most dysfunctional brain with severe brain injury because their motor regions were bilateral frontal and parieto-temporal responses may be limited or inconsistent (Laureys associative cortices. Despite the metabolic impairment, et al., 2002b). In addition, consciousness is not an external stimulation still induced a significant neuronal all-or-none phenomenon but should rather be con- activation (i.e., change in blood flow) in vegetative ceptualized as a continuum between different states patients as shown by both auditory click stimuli and (Wade and Johnston, 1999). There is also a theoret- noxious somatosensory stimuli. However, this activation ical limitation to the certainty of our clinical diag- was limited to primary cortices and dissociated from nosis, since we can only infer the presence or higher-order associative cortices, thought to be neces- sary for conscious perception. Finally, we demonstrated absence of conscious experience in another person that vegetative patients have impaired functional con- (Bernat, 1992). nections between distant cortical areas and between the In 1972, Jennet and Plum defined the vegetative thalami and the cortex and, more importantly, that state as a clinical condition of “wakefulness with- recovery of consciousness is paralleled by a restoration out awareness”. They cited the Oxford English of this cortico-thalamo-cortical interaction. Dictionary to clarify their choice of the term “veg- etative” as : “to vegetate is to live a merely physi- Key words : Vegetative state ; consciousness ; functional neuroimaging ; positron emission tomography ; brain cal life devoid of intellectual activity or social metabolism, cerebral blood flow ; functional connecti- intercourse” and “vegetative describes an organic vity ; brain plasticity. body capable of growth and development but devoid of sensation and thought”. Table 1 summa- rizes the criteria for the diagnosis of vegetative Introduction state (The Multi-Society Task Force on PVS, 1994). It is important to distinguish between per- Progress of medicine in general and intensive sistent and permanent vegetative state. A vegetative care in particular has increased the number of state is said persistent when it persists after an arbi- patients who survive severe acute brain injury. trary period of one month after acute traumatic or 178 S. LAUREYS ET AL. Table 1 Criteria of vegetative state – No evidence of awareness of self or environment and an inability to interact with others. – No evidence of sustained, reproducible, purposeful, or voluntary behavioral responses to visual, auditory, tactile, or noxious stimuli. – No evidence of language comprehension or expression. – Intermittent wakefulness manifested by the presence of sleep-wake cycles. – Sufficiently preserved hypothalamic and brainstem auto- nomic functions to permit survival with medical and nursing care. – Bowel and bladder incontinence. – Variably preserved cranial-nerve and spinal reflexes. From the Multi-Society Task Force on PVS (1994). FIG. 1. — Flow chart of the different clinical conditions that follow a severe brain lesion. non-traumatic brain injury (The Multi-Society Task and reproducible visual fixation, or response to Force on PVS, 1994) but this does not imply irre- threatening gestures. When patients undergo a tran- versibility. A vegetative state is said permanent sition from the vegetative state to a state of aware- when one predicts that the patient will not recover. ness, one of the first and most readily observed This distinction was introduced by the American clinical signs of this transition is the appearance of Multi-Society Task Force on PVS in 1994 to denote sustained visual pursuit. The crucial element to irreversibility after three months following a non- ascertain is the formal absence of any sign of con- traumatic brain injury and twelve months after scious perception or deliberate action. Any evi- traumatic injury (Fig. 1). However, even after these dence of communication, including a consistent long and arbitrary delays, some patients may response to command, or any purposeful move- exceptionally recover. Hence, the American ment rules out the diagnosis. This evidence can Congress of Rehabilitation Medicine advocated to easily be missed, especially in patients whose sens- abandon the term “permanent” in favor of simply es and motor capacities are severely impaired and defining the duration of the vegetative state in whom a blink of an eye (e.g., locked-in syn- (American Congress of Rehabilitation Medicine, drome) or the subtle movement of a finger (e.g. 1995). minimally conscious state) may provide the only Patients in a vegetative state usually show reflex evidence of awareness. Careful and prolonged or spontaneous eye opening and breathing. At observation is indispensable as fluctuating arousal times they seem to be awake with their eyes open, or motivation can prevent the assessment of mini- sometimes showing spontaneous roving eye move- mal yet present awareness in these patients. ments and occasionally moving trunk or limbs in Apallic state or syndrome is an archaic term for meaningless ways. At other times they may keep a condition that is now considered equivalent to their eyes shut and appear to be asleep. They may vegetative state. The term neocortical death has be aroused by painful or prominent stimuli opening been used differently by various authors. Some their eyes if they are closed, increasing their respi- refer to it as a vegetative state with absence or sub- ratory rate, heart rate and blood pressure and occa- stantial slowing of electrocortical activity on elec- sionally grimacing or moving. Pupillary, corneal, troencephalography (EEG), in addition to the char- oculocephalic and gag reflexes are often preserved. acteristics of vegetative state. Others equate neo- Vegetative patients can make a range of sponta- cortical death with the ostensible death of all neu- neous movements including chewing, teeth-grind- rons of the cerebral cortex. It is not clear whether ing and swallowing. More distressingly, they can this term denotes a clinical syndrome or its electri- even show rage, cry, grunt, moan, scream or smile cal, pathologic, or anatomical features (The Multi- reactions spontaneously or to non-verbal sounds. Society Task Force on PVS, 1994). The American Their head and eyes sometimes, inconsistently, turn Neurological Association has suggested abandon- fleetingly towards new sounds or sights. These ing the terms apallic state or syndrome, neocortical abilities are also seen in another group of patients death, coma vigile, alpha coma and permanent showing preserved wakefulness without awareness unconsciousness (ANA Committee on Ethical – namely, infants with anencephaly – and are con- Affairs, 1993). sidered to be of subcortical origin (The Medical Three factors clearly influence the chances of Task Force on Anencephaly, 1990). The diagnosis recovery from vegetative state : age, etiology, and of vegetative state should be questioned when there time already spent in a vegetative state. The out- is any degree of sustained visual pursuit, consistent come is better after traumatic than non-traumatic
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