I feel therefore I am? Understanding Pain in Disorders of Consciousness

I feel therefore I am? Understanding Pain in Disorders of Consciousness

Tags: , ,

By: Natalie Osborne

When a person’s consciousness is severely impaired after brain damage, they are said to have a Disorder of Consciousness (DOC). DOCs challenge our ideas about what constitutes the conscious human experience, and one of its most compelling mysteries: pain. Pain is a multidimensional psychological and physical experience, combining sensory, cognitive, and emotional processes. Whether or not patients with DOCs can experience pain is currently unknown. However, the answer will profoundly impact their treatment and care, as no single accepted strategy for pain detection and remediation currently exists for these patients.1

To understand the experiences of a person with a DOC, we must first appreciate that human consciousness exists on a spectrum. Severe brain damage, such as oxygen deprivation from a stroke or traumatic injury from a motor vehicle accident, can often result in a complete loss of arousal and awareness, known as a coma. While some patients wake up and recover from this state, others get “stuck” in intermediate levels of consciousness, where they can remain for months and even years.

For example, Unresponsive Wakefulness Syndrome (UWS, also known as Vegetative State) is defined as a return of arousal (e.g., sleep and wake cycles) without awareness. UWS patients can breathe on their own, sit up, and even look around the room. However, they do not appear to have awareness of their environment, and the behaviours they show (moving, swallowing, vocalizing, and even smiling, laughing, and crying) are considered reflexive and unconscious. Patients in a Minimally Conscious State (MCS) show fluctuating, intermittent signs of awareness. MCS patients make purposeful movements, recognize familiar objects, and can even respond to simple commands, such as “move your right hand” or “touch your nose.”

There are many potential sources of pain for DOC patients, including severe brain injury and spasticity, as well as bedsores, muscle atrophy, and limb contraction brought about by prolonged immobility. But without conscious awareness of the world around you, does a painful stimulus register as pain? Without awareness of the self, can the unpleasantness and suffering associated with pain be felt? Because DOC patients cannot communicate, there is no way to know for certain what they are experiencing.

Medicine urgently needs a more thorough understanding of the experience of pain in DOC patients to inform clinical management and treatment options. Currently these options are few, as the very existence of pain in DOCs is disputed in the literature. Some physicians recommend a “default approach,” where DOC patients are automatically treated for pain.1 However, there are concerns that the blanket use of sedative or analgesic drugs could mask or decrease arousal in patients, which would be counterproductive to recovery. Conversely, severe pain left untreated could also impair or inhibit recovery of consciousness.

Physicians currently rely on bedside behavioural assessments to diagnose DOCs. One such test has a subsection designed specifically to evaluate patients’ responses to “nociceptive” stimuli—stimuli that would cause pain in a healthy individual—called the Nociception Coma Scale (NCS). Patients considered to have neither environmental nor self-awareness can still show “nociception”—unconscious, subcortical pain processing that results in reflexive withdrawal movements or autonomic responses such as grimacing and crying.2 Behaviours thought to reflect more awareness of pain, such as verbalizing distress or touching the area where the painful stimulus was applied, result in higher NCS scores. Higher NCS scores correlate with increased levels of consciousness, as well as more activity in the anterior cingulate cortex, a brain area involved in pain processing.3

Still, behavioural tests are not always reliable. A seminal study by Owen et al. in 2009 used neuroimaging to uncover signs of awareness in a UWS patient who had been behaviourally diagnosed as unaware.4 The patient responded to commands not by moving, but by thinking—alternately imagining playing tennis or walking around their home when asked. Their brain activity while performing these mental imagery tasks was indistinguishable from healthy participants. This finding sparked many similar studies which revealed that about 30% of UWS patients are diagnosed as completely unaware based on behavioural tests, yet they retain signs of consciousness revealed through mental tasks.5 The misdiagnosis rate for behavioural tests raises an important question: could we similarly be missing signs of pain in these patients?

Neuroimaging studies have found that UWS patients show limited activation in the sprawling network of brain structures involved with somatosensory, cognitive, and emotional pain processing.6 This activation extends to include higher-order pain processing networks when the intensity of the painful stimulus increases.7 Moving up the scale of consciousness to MCS, brain activation in response to painful stimuli is more reliable, and begins to resemble the patterns seen when healthy people are given painful stimuli.8 A recent study found activation in the limbic system, which is thought to be involved in the emotional aspect of pain, in both UWS and MCS patients.9 The authors suggested this could mean that some patients may be capable of experiencing the unpleasantness of painful stimuli.

Using brain activity to infer whether or not a person is experiencing pain is, however, a precarious endeavour. Pain is a highly individual and variable experience, influenced by a multitude of factors including context, emotion, previous experience, and attention. Researchers have long pursued a definitive “neural signature” of pain, which has proven difficult to establish even in healthy brains. While advances in neuroimaging techniques and analyses may improve our understanding of how pain is represented in the brain, it cannot yet be regarded as an exclusive authority on whether or not a person is in pain.

Intriguingly, neuroimaging may offer another route towards improving patient care. A small proportion of DOC patients who mentally respond to commands can use these responses to communicate. Researchers establish with the patients which mental states represent yes and no, and then interpret their brain activity after asking them verifiable questions about their history, family, and present situation. In another landmark experiment in 2012, Dr. Adrian Owen and colleagues asked one such UWS patient “Are you in pain?” to which the patient answered, “No.”10

If a physician suspects a DOC patient may be in pain, there are several treatment options that may be effective. A 2014 case report by Lanzillo et al. described a DOC patient suffering from spasticity who, when treated with a combination of baclofen and the analgesic ziconotide, improved dramatically on behavioural tests of consciousness. When ziconotide was removed, the patient’s condition deteriorated but was restored when ziconotide was reintroduced. The patient went on to recover consciousness.11 Baclofen itself, commonly used to treat severe spasticity and any potential corresponding pain in DOC patients, has also been associated with improved consciousness in several other case studies.12 However, further research is needed to specifically explore if these drugs are indeed acting as analgesics, because an increase in consciousness does not necessarily equate to pain relief.

Advances in emergency medical care have made it possible for more patients to survive after catastrophic brain injuries. Therefore, medical care providers have a responsibility to ensure these patients have the highest quality of life possible. Researchers and clinicians should take advantage of innovations in neuroimaging technology to gain insight into these patients’ internal experiences, and make the effort to reach out to them any way they can… for they may be more in need than we think.

References

  1. Schnackers C, Zasler ND, (2007). Pain assessment and management in disorders of consciousness. Curr Opin Neurol. 20(6): 620-6.
  2. Pistoia F, Sacco S, Sara M, Carolei A. et al. (2013). The Perception of Pain and its Management in Disorders of Consciousness. Curr Pain Headache Rep; 17: 374
  3. Chatelle C, Thibaut A, Bruno MA, Boly M, Bernard C, Hustinx R, Schnakers C and Laureys S. (2013). Nociception Coma Scale-Revised Scores Correlate with Metabolism in the Anterior Cingulate Cortex. Neurorehabil Neural Repair. 28:149-152.
  4. Owen AM, Coleman MR, Boly M, Davis MH, Laureys S, Pickard JD. (2006). Detecting awareness in the vegetative state. Science ;313:1402.
  5. Monti MM, Vanhaudenhuyse A, Coleman MR, Boly M, Pickard JD, Tshibanda L, Owen AM, and Laureys S. (2010). Willful Modulation of Brain Activity in Disorders of Consciousness. N Engl J Med ;362:579-89.
  6. Laureys S, Faymonville E, Peigneux P, Damas P, Lambermont B, Del Fiore G, Degueldre C, Aerts J, Luxen A, Franck G, Lamy M, Moonen G, and Maquet P. (2002). Cortical processing of noxious somatosensory stimuli in the persistent vegetative state. NeuroImage 17: 732-741.
  7. de Tommaso M, Navarro J, Ricci K, Lorenzo M, Lanzillotti C, Colonna F, Resta M, Lancioni G, Livrea P. (2013). Pain in prolonged disorders of consciousness: Laser evoked potentials findings in patients with vegetative and minimally conscious states. Brain Inj 27(7-8): 962-972.
  8. Boly M, Faymonville ME, Schnackers C, Peigneux P, Lambermont B, Phillips C, et al. (2008). Perception of pain in the minimally conscious state with PET activation: an observational study. Lancet Neurol. 7: 1013-20.
  9. Calabrò RS, Naro A, Manuli A, Leo A, De Luca R, Lo Buono V, Russo M, Bramanti A, Bramanti P. (2017). Pain perception in patients with chronic disorders of consciousness: What can limbic system tell us? Clin Neurophys. 128: 454-462.
  10. Fernández-Espejo D & Owen AM. (2013). Detecting awareness after severe brain injury. Nat Rev Neurosci. 14:1-9.
  11. Lanzillo B., Loreto V., Calabrese C., Estraneo A., Moretta P. and Trojano L. (2014). Does pain relief influence recovery of consciousness? A case report of a patient treated with ziconotide. Eur J Phys Rehabil Med. (Pistoia et al, 2015).
  12. Pistoia F, Sacco S, Sara M, Franceschini M, and Carolei A. (2015). Intrathecal baclofen: effects on spasticity, pain, and consciousness in disorders of consciousness and locked-in syndrome. Curr Pain Headache Rep; 19: 466.