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“Mr. Dockery was a police officer in the town of Walden, northwest of Chattanooga, when he was shot in the forehead as he responded to a call on Sept. 17, 1988. He has been motionless and speechless in a nursing home most of the time since then but was recently moved to Columbia Parkridge Medical Center here because of a lung infection. Suddenly, on Monday, he spoke, amazing his family and physicians.” (NY Times, February 17, 1996)
What does a medical doctor really mean when he says that a patient is in a vegetative state? Does it mean that the patient is somehow like a vegetable? This term has caused much misunderstanding among patient’s families, and it is also confusing among non-neurologist physicians. The thought behind it is that, after a severe brain injury, certain patients may awake from a coma but remain unaware of the environment (wakefulness without awareness; for a review of the terms, refer to (1)). Vegetative state is, thus, the state in which a patient opens his/her eyes but remains unresponsive (Table). A set of criteria for the definition of vegetative state is provided by Monti et al. (1): “Three main clinical features define the vegetative state: (a) cycles of eye opening and closing, giving the appearance of sleep-wake cycles [...]; (b) complete lack of awareness of the self or the environment; and (c) complete or partial preservation of hypothalamic and brain stem autonomic functions.”
Table: Characteristics of the locked-in syndrome and disorders of consciousness
|Locked-in syndrome||No or very limited purposeful motor behavior (such as eye movement only) in a conscious subject|
|Coma||Unarousable, without purposeful behavior|
|Minimally conscious state||Wakefulness* with inconsistent signs of awareness|
|Vegetative state||Wakefulness* with no signs of awareness|
*Periods, typically brief, of eye lid opening, versus periods of lid closure
Adapted from Monti(1).
Medical professionals have frequently assumed that, since patients in this state do not speak or move, they also would probably not think and feel. This point is illustrated by a recently published survey from Belgium, in which 44% of medical doctors responded “no” to the question: “Do you think that patients in a vegetative state can feel pain?” (compared with 32% of paramedical caregivers)(2). In the logistic regression analysis, nonreligious physicians were the subgroup most likely to believe that patients in vegetative state do not feel pain. This is surprising, given that it is expected of physicians to know that pain circuits are some of the most primitive structures of the nervous system, and therefore the most likely to remain intact after a severe neurological injury (as pointed out by Billings(3)).
Vegetative state is without doubt a stage of brain injury with dismal prognosis (4)(5). It causes families enormous amounts of pain and suffering, and we currently know very little about the subjective aspects that patient’s may experience in this condition. The prognosis is not homogenous among the different causes of brain injury (better in traumatic, worse in anoxic injury), and it also varies significantly with age and comorbidities (1)(4)(5).
Several clinical assessment scales have been developed for the diagnosis and grading of disorders of consciousness. It has been recommended that one standardized assessment be used for the clinical evaluation of patients. The CRS-R (The JFK coma recovery scale-revised (6)) is one of the most commonly used scales. Even with experienced clinicians using standardized protocols, misdiagnosis still may occurs up to 40% of the time (1)(7)(8).
From the difficulty with establishing a clinical diagnosis of disorders of consciousness, it naturally follows that more sensitive techniques should be employed. In fact, there has been important research evaluating the use of electroencephalography (EEG) and functional magnetic resonance imaging (fMRI) (9)(10)(11). Although EEG is an old and established neurologic tool, new patterns and signs are being recognized in patients with disorders of consciousness, and have been associated with different prognosis. Conversely, fMRI is a labor intensive technique that requires special expensive equipment of very limited availability. Both techniques have introduced important insights into the understanding of the disorders of consciousness, but their role in clinical neurology is still undefined (for a review of the role of these techniques in the research of persistent vegetative state and minimally conscious state, see Cruse and Owen (11)).
Even if the roles of supplementary exams are not perfectly clear in current clinical practice, it is certain that lack of responsiveness cannot be equated to lack of awareness(1). Owen and colleagues published an impressive single case report in the Science journal in 2006(12). They described the use of fMRI to study the conscious awareness of a 23-year-old female in a vegetative state after a traumatic brain injury. The patient was able to modulate brain activity according to prompted verbal stimuli by means of two imagery tasks: imagining playing tennis versus imagining visiting all the rooms of the patient’s house. The fMRI patterns were compared with the patterns from healthy volunteers, and the researchers concluded that the patient retained the ability to understand spoken commands and to respond by modulating her brain activity.
The recent work by Monti and colleagues builds on that result to describe how the same techniques perform in a large heterogeneous group of patients with disorders of consciousness (8). They used similar imagery tasks (that trigger motor and spatial patterns), but assigned yes or no values to each imagery task, in order to let patients answer questions about their history, such as “do you have any brothers?” Out of 54 patients studied, the scientists were able to reliably communicate with five. Three of these five subjects were in fact found to have subtle awareness signs on repeat clinical examination, being reclassified as in a minimally conscious state, but two remained diagnosed as in a persistent vegetative state.
Allan Ropper, in an accompanying editorial to Monti’s paper (13), and others (3), are not convinced that cortical activation is evidence of a “stream of thought”, a truly inner life. Their argument is based on the supposition that the trigger cues for the imagery tasks could have elicited some type of cortical response independent of awareness, some kind of a very sophisticated knee-jerk reflex. Ropper suggested that instead of cuing the patients with “playing tennis” versus “relax”, Monti’s team should have asked patients “imagine playing tennis” and compared with “imagine not playing tennis”.
Perhaps nothing in clinical medicine is as complex as the assessment of consciousness, thus Allan Ropper, Andrew Billings, and others(3)(13)(14)(15) all hold merit in calming one’s excitement at the prospect of communicating with patients in vegetative or minimally conscious states. Should the default assumption be, therefore, that patients who cannot communicate their inner life do not experience one? We are seeing results that show similar brain activation patterns between patients with traumatic brain injury and healthy volunteers, and patients were able to answer rather complex questions about their biography. Even if this is not enough evidence to say that patients in a vegetative state have rich inner mental processes and are just disconnected from the outside world, certainly there is not enough evidence to assume the opposite.
What are the implications of the new evidence? The most immediate consequence to physicians of the recent research into disorders of consciousness is that they will probably have less confidence in counseling family members about whether patients can listen or understand them, in the absence of more sophisticated testing (13).
The new functional imaging and electroencephalogram techniques being developed will likely improve diagnostic accuracy, and may someday allow patients to express their feelings. Whether the finding that patients in persistent vegetative state may not be really “vegetating” will influence how we think about care-giving for the extremely disabled patient, and whether this will change physicians’ and family’s behaviors are profound ethical questions with no straightforward answer.
On the other hand, the knowledge that patients may suffer emotional and physical pain regardless of their ability to communicate should not be seen as surprising. By the same token, the goals of medicine should remain unchanged, the relief of suffering being the priority in patients with minimal or no chance of recovery.
Finally, for the physicians who are uncomfortable with diagnosing patients with the term “persistent vegetative state”, Laureys and colleagues suggest a more descriptive name for this condition: “unresponsive wakefulness syndrome”(16).
Commentary by Giacinto Grieco
There are many neurologic disorders diagnosed exclusively, or nearly so, based on clinical criteria. These disorders include the vegetative state, the minimally conscious state, coma and generalized motor seizures. In many cases, the diagnosis can be arrived at only with great care and deliberation. It is unfortunately all too common to find these diagnoses entered in medical charts as if they were physical exam findings. These are no more exam findings than myocardial infarction or acute appendicitis are considered exam findings. “Coma,” “vegetative” and “unresponsive” are even entered as reasons for not performing some or any part of a neurologic examination (“Cr Ns: unable to perform, pt comatose/vegetative”). It is incumbent on the physician to carefully examine the patient with disordered consciousness, and accurately record the findings. The diagnosis is then usually straightforward. If not, special tests or evaluation by an expert may be required.
How can you approach examining a patient who may be in a vegetative state and ascertain the diagnosis?
First, observe, do not touch! It may be necessary to observe for several minutes before laying hands on the patient. Dim the lights (to allow the pupils to adapt to relative darkness). Too many patients have “non-reactive” pupils because of a combination of senile meiosis and bright overhead lights.
Note the patient’s body position and postures.
Observe the respiratory rate and pattern. If the patient is on a mechanical respirator, count how many spontaneous, assisted and mandatory (“control” on some of the newest machines) breaths there are over an adequate period of observation.
Note all non-respiratory spontaneous activity. Carefully observe the eyelids, eyes, jaw, face, tongue, neck and limbs. Are there any stereotyped or repetitive actions?
Only after the above should you check pupillary light reactivity and manipulate the patient. Manipulation (including nursing activities such as bathing, suctioning, changing bed sheets, and repositioning) can provoke involuntary motor responses that are sometimes vigorous, and sustained for long periods.
A vegetative patient typically presents a classic set of findings:
1) Nearly 100% will have alternating periods, lasting seconds to a few minutes, of eye lid opening and closing.
2) Next most common are roving horizontal (with or without evident vertical component) eye movements, with the eyes yoked but the gaze slightly horizontally divergent; vertical disjugacy may be present. The movements can vary from fast to quite slow. They can be almost constantly present, or rarely seen.
3) Automatic chewing (lips typically closed) and swallowing are frequently present.
4) Blinking is a common finding (including blinking while the lids are closed).
The patient who has an essentially preserved brain stem, intact cranial nerves and end organs, will have preserved pupillary, corneal, oculocephalic, vestibulo-ocular, gag and cough reflexes. With brain stem or cranial nerve lesions, various pupillary, ocular motility, and other disturbances may be present.
The more the clinical picture diverges from the above, the more one should be suspicious of a diagnosis of vegetative state. Seek expert consultation.
Dr. Saraiva, Infectious Disease, NYU Langone Medical Center
Peer reviewed by Neil Shapiro, Editor-In-Chief, Clinical Correlations
Image courtesy of Wikimedia Commons
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