Melzack & Katz, Pain. Part 9d: More about phantom body pain in paraplegics

The paper, Pain

Part 1 First two sentences Part 2 Pain is personal Also Pain is Personal addendum., Neurotags! Pain is Personal, Always.

Part 3a Pain is more than sensation: Backdrop Part 3b Pain is not receptor stimulation Part 3c: Pain depends on everything ever experienced by an individual

Part 4: Pain is a multidimensional experience across time

Part 5: Pain and purpose

Part 6a: Descartes and his era; Part 6b: History of pain - what’s in “Ref 4”?; Part 6c: History of pain, Ref 4, cont.. : There is no pain matrix, only a neuromatrix; Part 6d: History of Pain: Final takedown Part 6e: Pattern theories in the history of pain Part 6f: Evaluation of pain theories Part 6g: History of Pain, the cautionary tale. Part 6h: Gate Control Theory.

Part 7: Gate control theory has stood the test of time: Patrick David Wall;  Part 7b: Gate control: "The theory was a leap of faith but it was right!"

Part 8: Beyond the gate: Self as mayor Part 8b: 3-ring circus of self Part 8c: Getting objective about subjectivity

Part 9: Phantom pain - in the brain! Part 9b: Dawn of the Neuromatrix model Part 9c: Neuromatrix: MORE than just spinal projection areas in thalamus and cortex

Phantom body pain in paraplegics

Sometimes rivers have to take detours around large obstacles, and while they don't usually ever flow backwards, they do sometimes have to take a new course which takes their riverbed bend backwards a short way. 

We're going to go back, now, to the last paragraph of the section before, the one titled "Beyond the gate."

"In 1978, Melzack and Loeser17 described severe pains in the phantom body of paraplegic patients with verified total sections of the spinal cord, and proposed a central ‘pattern generating mechanism’ above the level of the section. This concept represented a revolutionary advance: it did not merely extend the gate; it said that pain could be generated by brain mechanisms in paraplegic patients in the absence of a spinal gate because the brain is completely disconnected from the cord. Psychophysical specificity, in such a concept, makes no sense; instead we must explore how patterns of nerve impulses generated in the brain can give rise to somesthetic experience."

Link 17 goes to Melzack R, Loeser JD. Phantom body pain in paraplegics: evidence for a central “pattern generating mechanism” for pain. Pain 1978,4:195–210

Yesterday's topic was unpleasant to write about. But I feel inoculated now, ready to backtrack and meander through this old 1978 paper. I took a quick look at it a few weeks ago, but now I feel ready to take it on in greater depth. Digest it. I want to get, really get, what it is that made this topic so compelling to Melzack. So, please bear with me as I read it, and write my take about it.  (I wish there were an abstract. But, since there isn't... here we go.) 

The introduction:

"Phantom body pain in paraplegic patients is the most mysterious of all pain phenomena. It has been traditionally assumed [45] that the essential cause of pain in any part of the body is activity in the receptor-fiber units that innervate it. In this paper, however, we shall describe paraplegic patients who had undergone removal of an entire section of the spinal cord (segmental cordectomy) in the attempt to alleviate phantom body pain, yet they still suffered severe pain in the denervated areas of the body. There is no reason to believe that the pain was due to depression or neurosis. Furthermore, the possibility that the pain was produced by nociceptive signals transmitted along the sympathetic chain is ruled out because the pain was not relieved by bilateral sympathetic blocks. The perception of severe, chronic pain in the absence of any input from those parts of the body in which pain is felt has profound implications for theories of pain. The purpose of this paper is to examine the properties of phantom body pains in paraplegics and to propose a theoretical concept to explain them."

Reference 45 goes to a 1955 book, by James Clarke White, William Herbert Sweet, Pain: its Mechanisms and Neurosurgical Control. It turns out they wrote another book, in 1969, a 1000-pager, called Pain and the Neurosurgeon, A forty-Year Experience. Here is a short review. 

[White and Sweet: I'm struck by the coincidental juxtaposition of these completely random surnames, given the specific era in which they authored books together.]

Anyway, back to the 1978 paper by Melzack and Loeser. 

"In this paper, however, we shall describe paraplegic patients who had undergone removal of an entire section of the spinal cord (segmental cordectomy) in the attempt to alleviate phantom body pain, yet they still suffered severe pain in the denervated areas of the body."

Phantom body pain in paraplegics

The next section starts out...

"Three kinds of pain [161 are reported by paraplegic patients: (1) root pain (or “girdle pain”) localized at or near the level of the cord lesion, (2) visceral pain which usually accompanies a distended bladder or bowel, and (3) phantom body pain which is felt in the areas of complete sensory loss."

Earlier studies were vague, didn't always distinguish among the three kinds: the best Melzack and Loeser came up with was 27% - 30% of paraplegic patients (partial or total SCI) had burning and tingling in various parts of the body below the cord lesion that could turn nasty - severe, crushing, vise-like pinching, streams of fire pouring out the toes, knives twisting and being withdrawn at the same time; of these, 6-7% "required surgical intervention." 

Source
Rene Magritte 1959
The Castle of the Pyrenees

Required.

I can kind of see how, if you factor in the mentality of the era, coupled with desperate patients willing to do anything to feel better, can put society on the spot: its representatives, trained to have heroic capabilities, were perhaps all too anxious to practice what they were trained to do. Maybe they felt 

completely certain. Maybe they felt they were standing on the firm ground of decades of prior scientific research that had started with von Frey. Maybe they were completely mistaken. 

After rhizotomies, cordotomies and sympathectomies and even amputation didn't work, where could surgery for pain go next for these people?
Let's realize, yet again, that even complete sympathetic block, both sides, lumbar and stellate ganglia, didn't work. Didn't stop the pain. Was without effect. 

Cases of total transection of the spinal cord

"The most striking feature of phantom body pain in paraplegics is its presence even when the spinal cord is known to be totally transected."

Riddoch, G., The reflex functions of the completely divided spinal cord in man, compared with those associated with less severe lesions, Brain, 40 (1917) 264-402. 

Kuhn, R.A., Functional capacity of the isolated human spinal cord, Brain, 73 (1950) l-51.

Cases of pain after cordectomy

"The report of pain in body areas well below the level of a total cord lesion is startling enough. Even more astonishing, though, are cases of pain after cordectomy - total removal of one or more segments of spinal cord. "

Davis, L. and Martin, J., Studies upon spinal cord injuries. II. The nature and treatment of pain, J. Neurosurg., 4 (1947) 483-491. 

Freeman, L.W. and Heimburger, R.F., Surgical relief of pain in paraplegic patients, Arch. Surg., 55 (1947) 433-440.

Botterell, E.H., Callaghan, J.C. and Jousse, A.T., Pain in paraplegia: clinical management and surgical treatment, Proc. roy. Sot. Med., 47 (1954) 281-288. (full pdf)

In the next section, five grisly cases are described at length. I will spare all of us the details. 

Mechanisms of Phantom Body Pain in Paraplegics

"The patients we have just described, together with the cases reported in the literature, present a remarkable puzzle: they feel pain in specific areas of the trunk or the limbs below the level of a known spinal transection. The removal of segments of spinal cord at one or more levels precludes any possibility of surviving “pain fibers” or ephaptic transmission across the cord break. Transmission from peripheral receptors to the brain, therefore, cannot occur through spinal cord pathways." 

Bors, E., Phantom limbs of patients with spinal cord injury, Arch. Neurol. Psythiat. (Chic.), 66 (1951) 610-631.

Melzack and Loeser go through the last few remaining possibilities one by one.

1. Autonomic-visceral contributions/sympathetic chain: Nope.

"This explanation of phantom body pain, however, is ruled out by the observations described above that bilateral sympathetic blocks or sympathectomy usually fail to relieve the pain. Furthermore, the cord transections and cordectomies at mid- to high-thoracic levels often lie well above the cord segments which receive visceral afferents from blood vessels in the legs or from the bladder and rectum.
"Another explanation, proposed by Guttmann, is that bladder distension at noxious pressures may produce vasoconstriction below the level of cord section and compensatory vasodilation above the level, leading to a rise in skin temperature, sweating, piloerection, feelings of being flushed, and even headaches. These compensatory circulatory changes could presumably be produced by any intense input, including noxious stimulation of a skin ulcer. Such circulatory changes would, of course, provide inputs to spinal or brain ceils above the level of the cord transection. While these inputs may contribute to the mechanisms that underlie phantom body pain in these patients, they are clearly not signals from segmental peripheral receptors that could produce pain localized in specific parts of the groin, thighs, knees or feet."

Guttmann, L., Spinal Injuries: Comprehensive Management and Research, Blackwell, Oxford, 1973.

2. Psychological contributions to paraplegic phantom pain: Nope. 

"It is reasonable to expect severe emotional stress and depression in paraplegics whose lives have been profoundly altered as a result of their injury. Some of the patients withdraw, become emaciated, and are deeply depressed. There is no evidence, however, that the pain is produced by neurosis, depression, or other psychological factors. Rather, these factors may augment the patient’s pain and are only a portion of the total contributions to it."

.....

Melzack and Loeser conclude:

"Paraplegic patients perceive phantom body pain in definite parts of the body below the level of transection. The pain is not relieved by segmental cordectomy. Furthermore, it persists even when the only other route that could be taken by impulses from the periphery - the sympathetic chain - is blocked by anesthetic agents or surgical section, or the cord injury is rostra1 to the known segmental sympathetic inflow. We conclude, therefore, that peripheral input up to the level of total transection is not the cause of pain in these patients. There is no known anatomical substrate for sensory input from the lower abdomen or legs entering the spinal cord above mid-thoracic
levels. Two conclusions must be made: 

(1) the mechanisms that underlie these pains must be sought central to the level of cord transection, and 

(2) the loss of input to central structures after deafferentation may play an important role in producing pain."

 
A bit further on:

"We propose that other nuclei along the course of the major somatosensory projection systems can act as pattern generating mechanisms.  These cells are normally under sensory and downstream control. When deafferentation occurs, however, the cells fire spontaneously in abnormal bursts for prolonged periods of time. We propose that the pattern generating mechanisms, in paraplegics, must lie above the level of spinal transection or cordectomy. Furthermore, those regions responsible for pattern generation are assumed to project to the regions of the brain involved in precise localization of sensory inputs - that is, those neural areas that subserve the body schema - as well as to the areas that subserve pain experience." 

Melzack, R. and Casey, K.L., Sensory, motivational, and central control determinants of pain: a new conceptual model. In: D. Kenshalo (Ed.), The Skin Senses, Thomas, Springfield, Ill., 1968, pp. 423-439. (Full pdf)

So, there it is. The pivotal paper, at which point Melzack and Loeser decided, look, you can't cut out pain by removing pathways that supposedly carry it. It doesn't seem to work. If it was going to work, it would have worked in paraplegics, every single time. But it doesn't.
Here is an examination of the results. They aren't so hot. Wouldn't you agree?
So, don't you think the problem might be arising more rostrally in the system? And no, it doesn't mean the patients are imagining it.

And that last paper by Melzack and Casey was the little acorn from which a pretty substantial oak, the Neuromatrix model, has been steadily growing for almost 5 decades already.

..............

Next, we will revisit the four conclusions.