Different beliefs about pain perception in the vegetative and minimally conscious states: a European survey of medical and paramedical professionals

Abstract

Pain management in severely brain-damaged patients constitutes a clinical and ethical stake. At the bedside, assessing the presence of pain and suffering is challenging due to both patients' physical condition and inherent limitations of clinical assessment. Neuroimaging studies support the existence of distinct cerebral responses to noxious stimulation in brain death, vegetative state, and minimally conscious state. We here provide results from a European survey on 2059 medical and paramedical professionals' beliefs on possible pain perception in patients with disorders of consciousness. To the question “Do you think that patients in a vegetative state can feel pain?,” 68% of the interviewed paramedical caregivers (n=538) and 56% of medical doctors (n=1166) answered “yes” (no data on exact profession in 17% of total sample). Logistic regression analysis showed that paramedical professionals, religious caregivers, and older caregivers reported more often that vegetative patients may experience pain. Following professional background, religion was the highest predictor of caregivers' opinion: 64% of religious (n=1009; 850 Christians) versus 52% of nonreligious respondents (n=830) answered positively (missing data on religion in 11% of total sample). To the question “Do you think that patients in a minimally conscious state can feel pain?” nearly all interviewed caregivers answered “yes” (96% of the medical doctors and 97% of the paramedical caregivers). Women and religious caregivers reported more often that minimally conscious patients may experience pain. These results are discussed in terms of existing definitions of pain and suffering, the remaining uncertainty on the clinical assessment of pain as a subjective first-person experience and recent functional neuroimaging findings on nociceptive processing in disorders of consciousness. In our view, more research is needed to increase our understanding of residual sensation in vegetative and minimally conscious patients and to propose evidence-based medical guidelines for the management of possible pain perception and suffering in these vulnerable patient populations.

Introduction

The International Association for the Study of Pain (IASP, 1994) defines pain as “an unpleasant sensory and emotional experience associated with real or potential tissue damage.” As stressed by the IASP, the inability to communicate verbally does not negate the possibility that an individual is experiencing pain and is in need of appropriate pain-relieving treatment. Pain may also be reported in the absence of tissue damage or any likely pathophysiological cause; usually this happens for psychological reasons. Activity induced in the nociceptor and nociceptive pathways by a noxious stimulus is not pain, which is always a psychological state, even though pain most often has a proximate physical cause. Pain is a subjective first-person experience with both physical and affective aspects (Kupers et al., 2005). It is a sensation in a part or parts of the body, which is, always unpleasant and, therefore, an emotional experience. Pain and suffering are not interchangeable constructs. However, the concept of suffering is surprisingly ill defined and given relatively little attention in medicine. A person might experience significant pain-related suffering from a relatively low-level noxious stimulation if she or he believes the implications are ominous, interminable, and beyond their control (Turk and Wilson, 2009). Cassell (1991) defined suffering as “the state of severe distress associated with events that threaten the intactness of the person.” Pain by itself does not seem to be sufficient to cause suffering; rather it seems that the person's interpretation of the symptoms is crucial. We will here consider (as expressed by the Multi-Society Task Force on PVS, 1994) that pain and suffering refer to the unpleasant experiences that occur in response to stimulation of peripheral nociceptive receptors and their peripheral and central afferent pathways or that they may emanate endogenously from the depths of human self-perception.

The management of pain and suffering in disorders of consciousness (DOCs) is challenging because, by definition, patients in a vegetative state (VS) or minimally conscious state (MCS) cannot verbally or nonverbally communicate their feelings or experiences (e.g., McQuillen, 1991; Bernat, 2006; Laureys and Boly, 2007). The VS is a condition of preserved wakefulness contrasted with absent voluntary interaction with the environment (Jennett and Plum, 1972). The MCS was only recently defined (Giacino et al., 2002) and is characterized by discernible but fluctuating signs of awareness without consistent communication with the environment. How can we know if patients in VS or in MCS feel pain or suffering? The perceptions of pain and suffering are conscious experiences: the wakeful unconsciousness of vegetative patients, by definition, precludes these experiences. Of course, there is a theoretical problem to evaluate the subjective experience of pain (and any other conscious perception or thought) in another person. At the patient's bedside, we are limited to evaluate the behavioral responsiveness to pain. If patients never show any sign of voluntary movement in response to noxious stimuli it will be concluded they do not experience pain. They may, however, be aroused by noxious stimuli by opening their eyes if they are closed, quickening their breathing, increasing heart rate and blood pressure, and occasionally show grimace-like or crying-like behavior. As all these abilities are also seen in infants with anencephaly (The Medical Task Force on Anencephaly, 1990; Payne and Taylor, 1997) they are considered to be of subcortical origin and not necessarily reflecting conscious perception of pain. We also know from studies in general anesthesia that motor or autonomic responses are no reliable indicators of consciousness (e.g., Halliburton, 1998).

DOC patients classically are bed- or chair-bound and may suffer from spasticity, contractures, fractures, pressure sores, soft tissue ischemia, peripheral nerve injuries, complex regional pain syndrome, central pain syndromes, and post-surgical incisional pain (Schnakers and Zasler, 2007). Since they cannot communicate their potential painful state, the existence of pain is clinically inferred from observing their spontaneous behavior or their motor responses to noxious stimulation. Stereotyped responses (i.e., slow generalized flexion or extension of the upper and lower extremities), flexion withdrawal (i.e., withdrawal of the limb away from the point of the stimulation), and localization responses (i.e., the nonstimulated limb locates and makes contact with the stimulated body part at the point of stimulation) are linked to, respectively, brainstem, subcortical, or cortical activity (e.g., Stevens and Nyquist, 2006). No response after intense noxious stimulation reveals a deep stage of coma; stereotyped responses are considered as “automatic” unconscious reflexes, whereas localization of noxious stimulation is usually considered as indicative of conscious perception (Posner et al., 2007).

Repeated clinical examinations by trained and experienced examiners are paramount for the behavioral assessment of pain. To date, several scales are used for assessing pain in noncommunicative individuals with end-stage dementia, in newborns and in sedated intensive care patients, but no scale was developed to assess pain in DOCs (Schnakers et al., 2009b). We therefore recently proposed the Nociception Coma Scale as a standardized and validated tool measuring motor, verbal, and visual responses and facial expression in response to pain (Schnakers et al., 2009a). However, the absence of a behavioral response cannot be taken as an absolute proof of the absence of consciousness (McQuillen, 1991; Bernat, 1992) and inferring pain and suffering solely by observing behavioral responses may be misleading, especially in patients with extreme motor impairment or with fluctuating levels of vigilance (e.g., Majerus et al., 2005). Given these limitations of our bedside clinical assessment of pain in noncommunicative brain injured patients, inherent to the first-person subjective dimension of pain, we will next review the usefulness of functional neuroimaging methods in the study of pain and suffering in VS and MCS.