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100 Rectal Heat Thresholds [2003년 5월 DCR] 2011-11-17 3574
 
A Novel Test of the Sensory Afferent Pathway
 
Christopher L. H. Chan, F.R.C.S.,* S. Mark Scott, Ph.D.,*Malcolm J. Birch, Ph.D.,† Charles H. Knowles, F.R.C.S.,*Norman S. Williams, F.R.C.S.,* Peter J. Lunniss, F.R.C.S.*
 
From the *Academic Department of Surgery, Barts and The London School of Medicine and Dentistry, and †Department of Clinical Physics, Barts and The London NHS Trust, London, United Kingdom
 
PURPOSE: Currently, rectal sensation may be measured by balloon distention or mucosal electrostimulation. This study investigated the application of a graded heat stimulus to the rectum using a novel thermal probe as a further method of evaluating rectal sensory afferent mechanisms.
METHODS: A thermal probe specially designed in our institution was used to test rectal heat sensitivity in 31 healthy subjects. This was compared with all other standard anorectal physiologic measurements. Repeatability studies were also performed.
RESULTS: Heat stimulation of the mid rectum elicited sensory responses in all subjects. The most common reported response was not heat but a sharp or prickling sensation. The median rectal heat threshold was similar in males (median, 47°C; range, 44–50°C) compared with females (median, 45°C; range, 43–50°C; P > 0.05). There was a high degree of repeatability with rectal heat and balloon
distention thresholds, but not electrostimulation thresholds. A strong correlation was found between rectal heat thresholds and defecatory desire (r = 0.71; P < 0.001) and maximum tolerable volumes (r = 0.8; P < 0.001) measured with balloon distention.
CONCLUSION: This is the first demonstration of a repeatable sensory response to heat stimulation in the rectum of normal subjects. Strong correlation between heat thresholds and balloon distention to
maximum tolerable volumes and defecatory desire suggest common sensory afferent pathway excitation. Heat stimulation is a simple technique that has a high degree of repeatability and may be an objective assessment of polymodal nociceptor function in the rectum.
 
The somatosensory system is able to detect temperature changes over a wide range. When a hot
or cold stimulus is applied, a specific set of primary afferent neurons (predominantly C fibers) is excited.
The stimulus is then transduced into electrochemical signals, which are subsequently relayed to the brain and spinal cord. Thermoreceptors are found not only in the skin and mucous membranes but also in the upper gastrointestinal tract. The role of these visceral thermoreceptors is unclear, but it is suggested they are involved in body temperature regulation and
coordination of digestive activity. The precise location of these receptors is unknown. However, intraperitoneal and intraluminal application of saline at 45°C into the small and large bowel produces marked reflex (cardiovascular and circulatory) activity, indicating that the receptors lie either in the mucosal or serosal layers of the bowel wall. In the lower gastrointestinal tract, the anal canal is highly sensitive to temperature changes. It has been postulated that this mechanism is involved in the maintenance of continence, although later work has questioned this hypothesis. Early studies investigating rectal sensation to thermal stimulation were able to elicit only a negligible response. However, these studies involved thermal probe designs that were cumbersome in construction, reached target temperatures slowly, and achieved only a limited range of relatively low temperatures of between 31 and 41.5°C. A more recent study, primarily investigating rectal pressure responses to thermal changes, reported a rectal pain response in healthy volunteers during infusion of saline at 45°C.
 
The first aim of this study was to evaluate the sensory response to heat stimulation in the rectum using a specially designed thermal probe over a wider range of temperatures than previously used. The second aim was to correlate these findings with other physiologic tests of anorectal sensorimotor function and consequently investigate whether such a technique was a more accurate measure of rectal sensory function compared with conventional tests.
 
DISCUSSION
This study provides the first report of a repeatable sensory response to heat stimulation in the rectum of
normal subjects and demonstrates that rectal sensation may be precisely evaluated by this method. The
nerve supply to the rectum is derived from the sympathetic and parasympathetic nervous systems and
from the inferior hemorrhoidal branches of the pudendal nerves. The sympathetic fibers arise from the
lower six thoracic and upper two lumbar segments of the spinal cord with ganglion cells lying at the level of L-1 and L-2. The parasympathetic supply comes from the second, third, and fourth sacral segments. An early study suggested that the sensation of rectal distention was conveyed solely via the parasympathetic system to the second and third sacral segments. Sensory receptors responding to distention, chemical, osmotic, and thermal stimuli have been characterized functionally but not structurally in the gastrointestinal tract, except for Pacinian corpuscles in the mesentery. In this study the temperatures at which an altered sensation was perceived in the rectum were much higher than normal core temperature. Pain was the most common perceived sensation on heat stimulation. This suggests that nociceptors (sensory receptors responding to noxious stimuli) were being excited.
Mechanoreceptors in the rectum are believed to be responsible for the sensation of fullness, urge to
defecate, discomfort, and pain
. The afferents to these mechanoreceptors are C or A∂ fibers. Colorectal distention has been shown in animal studies to be a noxious visceral stimulus. We demonstrate a strong correlation between rectal heat thresholds and threshold volumes for defecatory desire and maximum toleration on balloon distention. This suggests that common visceral afferents are being stimulated. Animal studies have shown that over 90 percent of mechanosensitive receptors in the colon are polymodal and respond to heat and chemical stimuli. A rich supply of beaded nonmyelinated nerve fibers has been observed in the rectal mucosa, and polymodal nociceptive axons are known to terminate in a “chain of beads.” Thus, heat stimulation in the rectum is most likely to be exciting nonmyelinated C or A∂ fiber pathways. Recently, the cloned capsaicin receptor, known as vanilloid receptor subtype 1 (VR1) and its homolog vanilloid-receptor-like protein 1 have been identified and cloned. VR1 and vanilloid-receptor-like protein 1 are heat-sensitive ion channels that transduce medium-threshold and high-threshold heat, respectively, and are found on nociceptive afferents. Nociceptive afferents are predominantly polymodal C fibers and express the heat-sensitive ion
channel VR1. VR1 receptors have been identified in normal human large bowel mucosa on immunohistologic staining and Western blotting using monoclonal antibodies, thus providing further evidence for the heat stimulation response in the rectum.
 
Previous investigators have failed to elicit a distinct sensory response to thermal stimulation in the rectum of normal subjects. The temperatures used in these studies were, however, low, being several degrees Celsius below the lowest heat threshold in the present study. Absence of a reported response to heat is therefore most likely to be caused by failure to reach the stimulating thermal threshold. The findings in the present study would be in accordance with a more recent article reporting a sensation of rectal pain in healthy subjects after instillation of saline at 45°C into an intrarectal balloon.
 
Our thermal probe design is safe, compact, and has a high degree of subject comfort and acceptability. In addition, the thermal probe reached a wide range of target temperatures within seconds and could be used at various sites on the rectal wall. This study has confirmed that measuring rectal sensory thresholds with simple balloon distention and rectal heat threshold measurements with a thermal probe both have a high degree of repeatability. These results are in keeping with previous studies investigating the repeatability and reproducibility of tests of anorectal function. In general, male subjects had slightly
higher rectal heat thresholds compared with female subjects, although this did not reach statistical significance. In this study rectal sensory threshold volumes were higher in males than in females. This finding is in keeping with the results of a large study of 91 healthy subjects investigating the influences of age and gender on anorectal function. The poor correlation between rectal heat thresholds and rectal electromucosal sensitivity levels is surprising, because one would envisage that these two techniques stimulate the same nociceptive afferents. This discrepancy may be explained by the fact that a marked
variance in rectal electromucosal sensitivity recordings was observed in the present study, confirming
similar findings in a previous study that questioned the validity of rectal electromucosal sensitivity as a
test of anorectal function.
 
We do not believe that the rectal heat threshold temperatures, which are within the noxious range, play a direct role per se in the defecation or continence reflex processes. The range of rectal heat thresholds may, however, reflect different levels of visceral afferent excitability. Heat threshold may be a more precise indicator of rectal sensory function, because it seems to be generated by direct stimulation of
polymodal nociceptive afferents that express heatsensitive ion channels. These polymodal afferents also respond to mechanical and chemical stimuli and so may be indirectly involved in anorectal continence mechanisms.