Referred Pain Phenomena In The Clinical Context Referred Pain Hyperalgesia

Referral of pain to distant structures is a typical feature of visceral nociception (2,8). It is only in the very first episode, or early phases of the first episode, in fact, that pain symptoms from internal organs are perceived in a common site for all viscera (i.e., usually along the midline, in the thorax or abdomen, anteriorly, or posteriorly). At this stage, the symptom is a vague and poorly defined sensation, accompanied by marked neurovegetative signs and emotional reactions (the so-called "true visceral pain''). Soon after this phase (minutes or, at most, hours), visceral pain is "transferred" (and called ├╝bertragener Schmertz, i.e., transferred pain, by German authors) to somatic areas of the body wall, which differ according to the specific viscus and which are generally located within the related metameric field (2). Secondary hyperalgesia (increased sensitivity to painful stimuli/decreased pain threshold) most often takes place in the referred areas, starting in the skeletal muscle layer, to also extend upwards to the overlying subcutis and skin, especially in the case of recurrent and/or prolonged visceral stimuli (referred pain without and with hyperalgesia) (7,9).

In the clinical context, myocardial infarction is one of the most paradigmatic forms of the progression of pain in internal organs from the phase of "true visceral pain'' to the phase of pain referral with secondary hyperalgesia. The early stages are characterized by a vague sensation of malaise and oppression in the lowest sternal area and/or epigastrium, or aching in the interscapular region, with accompanying neurovegetative symptoms such as nausea, vomiting, pallor, sweating, alvus disturbances, and strong emotional alarm reactions (e.g., anguish or feeling of impending death). Subsequent phases, occurring after a few minutes to a few hours, are instead featured by a sharper and better defined pain sensation, which is perceived at the level of the thoracic wall, either anteriorly or posteriorly, and very often in the upper limbs, most commonly the left one (ulnar side of the arm and forearm) (referred pain). Hyperalgesia is typically found in muscles of the referred area, mostly the pectoralis major and muscles of the interscapular region and forearm, sometimes also the trapezius and deltoid muscles. In a low percentage of cases, the hypersensitivity also extends upwards to the subcutis and skin of the referred area, within dermatomes C8-T1 on the ulnar side of the upper limb (10).

Urinary colics from calculosis, among the most intense forms of pain that a human being can experience, are other typical examples of referred pain from internal organs. The symptom is normally felt at lumbar level on the affected side, with radiation to the ipsilateral flank and anteriorly to the groin. Deep hyperalgesia is detectable in muscles of the lumbar and flank area (quadratus lumborum and oblique muscles) (11). In symptomatic biliary calculosis, pain is referred to the upper right quadrant of the abdomen with radiation toward the back. Hyper-algesia typically affects the rectus abdominis at the cystic point, i.e., level of junction of the 10th rib with the outer margin of the same muscle (12). In pelvic pain conditions, e.g., dysme-norrhea, pain is referred to the lower abdomen, perineum, and sacral region, with radiation toward the groin and upper part of the thighs. Tenderness typically affects the lowest part of the rectus abdominis and muscles of the pelvic region (13). In all the previous examples, hyperalgesia may also possibly involve the subcutis and skin overlying the tender muscles, in cases of repeated and/or prolonged painful episodes (10).

The referred sensory changes (hyperalgesia) can be detected by clinical means and precisely quantified instrumentally. The clinical maneuvers reveal the hypersensitivity in an "on-off" manner, i.e., vigorous pain reaction by the subject upon firm manual compression of the muscle tissue, pinch palpation of the subcutis, and scratching of the point of a needle over an area of altered dermographic reactivity of the skin (14). The instrumental procedures mostly involve evaluation of the pain threshold, i.e., the minimum intensity of a stimulus corresponding to the first report of pain by the subject (15), with a threshold decrease indicating hyperalgesia. For the muscle and subcutis, mechanical (myometer for muscle and pinch algo-meter for subcutis), electrical (impulses delivered through needle electrodes), and chemical (injections of algogenic substances of progressively increasing concentrations) stimuli are usually employed. For the skin, thermal stimulation (thermal algometer) is also used in addition to mechanical (von Frey hairs) and electrical (impulses delivered through surface electrodes) stimuli (7,6,13,16).

These various procedures have been used to assess the profile of the referred sensory changes in different algogenic conditions from internal organs, e.g., the digestive system [gallbladder pathologies, irritable bowel syndrome (IBS)], urinary tract (calculosis), and female reproductive organs (dysmenorrhea and endometriosis) (6,7,9,13,17-20). The global outcome of these studies indicates that referred visceral hyperalgesia, mostly involving the skeletal muscle layer of the affected body wall area, is an early phenomenon, in that it is detected soon after the first visceral pain episodes. It is accentuated in extent by the repetition of the episodes (e.g., colics and painful menstruations), that is, the more numerous the episodes, the lower the threshold, and outlasts the spontaneous pain, being detectable in the pain-free intervals and sometimes remaining even after recovery from the primary visceral disease. An example is provided by the profile of muscle hyperalgesia in urinary calculosis, where hypersensitivity of the oblique musculature at L1 appears soon after the first one to two colics, increases in extent with their repetition, and is detectable in between the painful episodes (Fig. 1).

In about 90% of the cases, it also persists (for months and even years) after the urinary stone has been eliminated (6,7,9,17). As a general rule, it has been found that a minimum pain

URINARY COLIC Referred sensory changes

Figure 1 Referred sensory changes at muscle level in urinary colics from calculosis. Pain thresholds to electrical stimulation of the obliquus externus muscle ipsilateral to the affected urinary tract in different groups of patients who had experienced a progressively higher number of colics (recordings performed in the pain-free interval) as compared to thresholds measured in normal subjects at the same level. Note the progressively significant decrease in threshold with respect to normal. Asterisks refer to comparison between patients and normal subjects. Source: From Ref. 22.

Figure 1 Referred sensory changes at muscle level in urinary colics from calculosis. Pain thresholds to electrical stimulation of the obliquus externus muscle ipsilateral to the affected urinary tract in different groups of patients who had experienced a progressively higher number of colics (recordings performed in the pain-free interval) as compared to thresholds measured in normal subjects at the same level. Note the progressively significant decrease in threshold with respect to normal. Asterisks refer to comparison between patients and normal subjects. Source: From Ref. 22.

perception is required for the secondary sensory changes to take place. Asymptomatic diseases of internal organs, in fact, are not able to trigger referred hyperalgesia, as shown by the sensory normality of body wall tissues in the areas of projection of the gallbladder or the kidney/ureter in the case of silent calculosis (i.e., calculosis without colics). In contrast, painful nonorganic visceral diseases do provoke referred sensory changes, as happens in biliary diskinesia (19) or in IBS. Regarding the latter, in fact, recent studies have shown somatic hyperalgesia in the abdominal referred pain area, which was particularly accentuated in the muscle layer (20).

In acute inflammatory visceral pain, the referred hyperalgesia tends to also involve the superficial somatic tissues. Patients with acute appendicitis show increased ratings to pinprick (von Frey hairs) and thermal stimuli (warm and cold metal rollers), together with a reduction of cutaneous pain thresholds to electrical stimuli and of pain thresholds to pressure stimuli, in the referred abdominal pain area (McBurney's point) versus the contralateral control area. The pain thresholds to electrical and pressure stimuli are lower in the referred pain area in patients compared with the same area in healthy control subjects (21). In acute cholecystitis, there is hypersensitivity to pinprick, heat, cold, pressure, and single and repeated cutaneous electrical stimulation in the referred pain area and in the contralateral control area of the abdomen. However, the hypersensitivity appears normalized after cholecystectomy (21-23). This latter finding is different from the above-reported results on the persistence of some degree of hyperalgesia even after removal of the primary visceral focus. It probably indicates that repeated algogenic inputs from viscera (e.g., recurrent conditions such as colics or painful menstruations) rather than isolated acute episodes, are required to leave persistent hyperalge-sic traces in the referred area.

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