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Ann Thorac Surg 1997;64:207-210
© 1997 The Society of Thoracic Surgeons


Original Articles: General Thoracic

Postoperative Pain and Superficial Abdominal Reflexes After Posterolateral Thoracotomy

Fabrizio Benedetti, MD, Martina Amanzio, MS, Caterina Casadio, MD, Pier Luigi Filosso, MD, Massimo Molinatti, MD, Alberto Oliaro, MD, Franco Pischedda, MD, Giuliano Maggi, MD

Department of Neuroscience, CIND Center for the Neurophysiology of Pain, and Department of Thoracic Surgery, University of Torino Medical School, Torino, Italy

Accepted for publication January 15, 1997.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Background. Posterolateral thoracotomy can produce stretching of/or damage to the intercostal nerves and their branches. To assess intercostal nerve impairment after operation, we measured the superficial abdominal reflexes, which are mediated, at least in part, by the most inferior intercostal nerves.

Methods. Using electrophysiologic techniques, we made recordings from the left and right abdominal walls to study the responses evoked by mechanical stimulation of the skin after operation. In addition, we assessed postoperative pain intensity according to a numeric rating scale and recorded postoperative opioid dose.

Results. We found that the patients with complete disappearance of the superficial abdominal reflexes experienced more severe postoperative pain than those in whom the reflexes were maintained. Moreover, opioid treatment was less effective in the patients with no reflexes postoperatively.

Conclusions. Our findings show a strict correlation between pain intensity after posterolateral thoracotomy and absence of abdominal reflexes. We suggest that the higher pain intensity together with the absence of reflexes may be due to intercostal nerve impairment, be it anatomic or functional, and thus to a larger neuropathic component of postoperative pain. This finding may be used as a predictor of patients with high analgesic requirements.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
The mechanisms underlying postoperative pain are only partially understood. Certainly, tissue damage and inflammation, associated with the release of local substances, play an important role, but other factors are also involved [1]. For example, both segmental (such as muscle spasm) and suprasegmental (such as blood pressure and hormones) factors contribute to postoperative pain [13]. Nevertheless, it is not clear why, after the same surgical procedure, some patients complain of severe and unbearable pain, whereas others report only mild to moderate pain. Similarly, whereas some patients respond well to low doses of opioids, others require very large doses and have unsatisfactory results [4].

A thoracotomy produces severe postoperative pain. Again, however, there is a large variability in postoperative pain intensity. After thoracotomy, 45% to 65% of patients report severe pain and 25% to 35%, moderate pain [1]. Similarly, the duration of severe pain after thoracotomy ranges from approximately 3 days to 7 days [1]. In addition, low doses of opioids are effective in some patients, whereas in others, even large doses often cannot provide a satisfactory degree of analgesia [4]. This aspect is particularly important in thoracic surgery, as large doses of opioids may result in undesirable side effects such as respiratory depression [1, 5].

To investigate the factors influencing both intensity and time course of postoperative pain, we studied the superficial abdominal reflexes after posterolateral thoracotomy. The superficial abdominal reflexes are mediated, at least in part, by the most inferior intercostal nerves whose branches innervate the superior portion of the abdomen [6]. A posterolateral thoracotomy often produces stretching or damage of the intercostal nerves and their deep and superficial branches; therefore, measurement of the abdominal reflexes can be used as an index of nerve impairment. The rationale underlying measurement of the abdominal reflexes is the possibility that an important component of the postoperative pain after thoracotomy is due to nerve impairment, be it anatomic or functional. It is interesting to note that pain resulting from nerve damage is relatively insensitive to opioid treatment [79], a fact that might be correlated to the poor response to opioids of some patients after thoracotomy.

On the basis of these considerations, we analyzed the time course of the superficial abdominal reflexes after thoracotomy and found a correlation between their absence and the intensity and duration of postoperative pain.


    Material and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Forty-two patients gave informed consent and participated in the study. All had lung cancer and underwent lung resection through a standard posterolateral thoracotomy. Patients were divided into two groups on the basis of the presence (group 1, 23 patients) or absence (group 2, 19 patients) of the superficial abdominal reflexes on the first postoperative day. Mean age (group 1, 58 ± 7 years, and group 2, 61 ± 9 years), sex (group 1, 15 men and 8 women, and group 2, 13 men and 6 women), and number of pneumonectomies (six in group 1 and five in group 2) and lobectomies (17 in group 1 and 14 in group 2) did not differ between the two groups.

Electrophysiologic Recordings
Electrophysiologic recordings were made the day before operation and 1 day, 1 week, and 2 to 3 months after operation. Recordings were obtained from both abdominal walls, ipsilateral and contralateral to the thoracotomy, through silver chloride electrodes, 5 mm in diameter, placed on the skin overlying the external oblique muscles. The signal from the electrodes was amplified by a differential amplifier (WPI, DAM 50) and displayed on a digital oscilloscope (Tektronix 222A). Electrophysiologic responses were elicited by scratching the skin overlying the external oblique muscles in the lateral to medial direction with a needle. The results from both sides were analyzed.

Procedure
Only those patients showing abdominal reflexes on the day before operation were considered. However, because the reflexes contralateral to the stimulation were inconstant in all patients, we studied only the reflexes ipsilateral to the stimulation. On the day after the operation, the patients were tested for electrophysiologic responses both ipsilateral and contralateral to the thoracotomy. The same electrophysiologic analysis was repeated 1 week and 2 to 3 months postoperatively. Before the recording, each patient reported his or her present pain intensity on the basis of a numeric rating scale ranging from 0 (no pain) to 10 (unbearable pain). Pain intensity was assessed by one individual who did not know the aim of the study. In addition, the patients were completely blinded, as they did not know the outcome of the electrophysiologic recordings.

Postoperative analgesic treatment consisted of intravenous infusions of standardized doses of buprenorphine hydrochloride (0.3 mg in 250 mL of NaCl 0.9%) given only at the request of the patient. Buprenorphine was administered by nurses who were blinded to the status of the abdominal reflexes. The total dose of buprenorphine given during the first days after operation was recorded.

Statistical analysis
Differences in pain intensity scores, amplitudes of electrophysiologic responses, and total opioid dose were tested by analysis of variance followed by the Newman-Keuls multiple range test for multiple comparisons. The amplitude of the abdominal reflexes was measured using the mean of the first three responses to needle stimulation, as habituation occurred very quickly in some patients. Data are presented as the mean ± the standard deviation. Differences were considered significant at a p value of less than 0.05.


    Results
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Recordings of the superficial abdominal reflexes on the day after thoracotomy suggested that the patients could be divided into two groups. Group 1 (23 patients) was characterized by maintenance of the abdominal reflexes both ipsilateral and contralateral to the thoracotomy, whereas group 2 (19 patients) had total disappearance of the reflexes ipsilateral to the thoracotomy and maintenance of the contralateral reflexes. Therefore, in both groups, the reflexes contralateral to the thoracotomy were present, with no significant differences in response amplitude with respect to the preoperative recordings (group 1, p = 0.308; group 2, p = 0.214). Although the ipsilateral reflexes were maintained in group 1, we found a significant reduction in their response amplitude (Fig 1Go). The mean preoperative amplitude was 148.4 ± 64.8 µV and the postoperative amplitude, 72.5 ± 37.2 µV (p < 0.001). In group 2, the mean preoperative response amplitude was 135.2 ± 73.5 µV; there was no ipsilateral response postoperatively (see Fig 1Go).



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Fig 1. . Time course of abdominal reflex amplitude ipsilateral to the thoracotomy in patients with reflexes present (black circles) and absent (white circles) 1 day after operation.

 
The time course of the amplitude of the abdominal reflexes ipsilateral to the thoracotomy is shown for both groups in Figure 1Go. In group 1 (patients with postoperative reflexes), there was recovery of the response amplitude after 1 week and normal reflex function after 2 to 3 months. Conversely, none of the patients in group 2 had short-term recovery, as shown by the total absence of reflexes after 1 week. However, after 2 to 3 months, we found complete recovery of abdominal reflex function in 15 patients; in the remaining 4, there was still a total absence of reflexes (Table 1Go).


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Table 1. . Mean Amplitude of Reflexes Ipsilateral to the Thoracotomy, Pain Intensity, and Opioid Dose in Two Groups at Different Postoperative Intervalsa
 
Figure 2Go shows the time course of postoperative pain in the two groups. Whereas the group 1 patients had a quick decrease in pain intensity, the patients in group 2 complained of more severe and long-lasting postoperative pain. Table 1Go shows the amplitude of the reflex response and the pain scores in the two groups 1 day, 4 days, 1 week, and 2 to 3 months after operation. The differences between the two groups were significant for every postoperative period considered except the last. However, at 2 to 3 months after operation, 4 patients in group 2 continued to have no recovery of abdominal reflex function (amplitude = 0), and 2 of these 4 patients complained of chronic paroxysmal pain.



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Fig 2. . Time course of postoperative pain in patients with abdominal reflexes present (black circles) and absent (white circles) after thoracotomy.

 
Interestingly, the higher pain scores of the patients in group 2 were not due to a lower dose of opioids. In fact, the patients received larger amounts of buprenorphine than the patients with reflexes (Fig 3Go). In other words, the absence of the reflexes was correlated to a larger overall dose of buprenorphine, a finding indicating that these patients were relatively insensitive to opioids. Table 1Go shows the amount of buprenorphine administered 1 day, 4 days, 1 week, and 2 to 3 months postoperatively. After 2 to 3 months, 2 patients with no reflex recovery and chronic paroxysmal pain were on a regimen of sublingual buprenorphine, with unsatisfactory results.



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Fig 3. . Buprenorphine dose administered to patients with abdominal reflexes present (black circles) and absent (white circles) after thoracotomy.

 

    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
The results of the present study show that postthoracotomy pain was more severe and long lasting when the superficial abdominal reflexes disappeared after operation. In addition, the pain intensity of these patients was high and of long duration despite a large overall dose of opioids, findings indicating a low sensitivity to opioid treatment in patients without abdominal reflexes after thoracotomy. Although there is no doubt that these patients had no abdominal reflexes after operation, on the basis of these results, we cannot say whether this postsurgical deafferentation was anatomic or functional. Incision of superficial and deep tissues and stretching of the ribs may represent an important traumatic factor damaging the nerve fibers that mediate the superficial abdominal reflexes. On the other hand, local inflammation and edema may induce a functional impairment of some nerve fibers. Therefore, the recovery of abdominal reflex function after several months can be viewed either as nerve regeneration or as restoration of nerve function. Whatever the case, the correlation between pain intensity and absence of abdominal reflexes may clarify some mechanisms underlying postoperative pain.

Usually, damage to deep and superficial tissues that is associated with inflammation and edema appears to play a primary role in postoperative pain [1]. However, at least for some surgical procedures, it is also important to consider the impairment of peripheral nerves. Damage to the peripheral nerves induces a painful condition called neuropathic pain. One of the proposed mechanisms underlying pain after nerve damage is represented by extensive deafferentation, which, in turn, is associated with absence of afferent inhibition of nociceptive input from the damaged large afferent fibers [1012]. Neuropathic pain is characterized by a poor response to opioid treatment [79], a fact that might be due to the up-regulation of the antiopioid peptide cholecystokinin in the primary afferent fibers [13].

Taking into account all these considerations, we suggest that the more severe pain experienced by patients with disappearance of the superficial abdominal reflexes after thoracotomy is due to more extensive deafferentation, be it anatomic or functional, and to a larger neuropathic component of postoperative pain. This conclusion is in agreement with the relative insensitivity of neuropathic pain to opioids, a finding also present in the patients with no reflexes after posterolateral thoracotomy. It is interesting that 2 of the 4 patients showing no recovery of abdominal reflex function after 2 to 3 months complained of paroxysmal chronic pain insensitive to sublingual buprenorphine.

These results have both theoretic and practical implications. In the first instance, they help us to understand the mechanisms of postoperative pain, in particular, those responsible for pain after posterolateral thoracotomy. Understanding the origin of pain (for example, in deep and superficial tissues and nerves) is essential to plan new therapeutic strategies. In the second instance, the measurement of the superficial abdominal reflex function can be used as an index of intercostal nerve impairment and, thus, as a predictor of pain intensity and duration and of opioid effectiveness.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 
Address reprint requests to Dr Benedetti, Dipartimento di Neuroscienze, Università di Torino, Corso Raffaello 30, 10125 Torino, Italy.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 References
 

  1. Bonica JJ. Postoperative pain. In: Bonica JJ, ed. The management of pain. Philadelphia: Lea & Febiger, 1990:469–88.
  2. Bonica JJ. Introduction to recent advances in the management of acute and chronic pain. Hosp Pract 1979;1:4–10.
  3. Conseiller C, Ortega D. Douleur post-opératoire. In: Conseiller C, Bruxelle J, eds. Douleur et analgésie post-opératoires et obstétricales. Paris: Masson, 1991:13–31.
  4. Austin KL, Stapleton JV, Mather LE. Relationship between blood meperidine concentrations and analgesic response: a preliminary report. Anesthesiology 1980;53:460–6.[Medline]
  5. Goth A. Medical pharmacology. St. Louis: Mosby, 1984:319–35.
  6. Bonica JJ. Chest pain. In: Bonica JJ, ed. The management of pain. Philadelphia: Lea & Febiger, 1990:980–1021.
  7. Arner S, Meyerson BA. Lack of analgesic effect of opioids on neuropathic and idiopathic forms of pain. Pain 1988;33:11–23.[Medline]
  8. McQuay HJ. Pharmacological treatment of neuralgic and neuropathic pain. Cancer Surv 1988;7:141–59.[Medline]
  9. Portenoy RK, Foley KM, Inturrisi C. The nature of opioid responsiveness and its implications for neuropathic pain. New hypotheses derived from studies of opioid infusions. Pain 1990;43:273–86.[Medline]
  10. Cassinari V, Pagni CA. Central pain: a neurosurgical survey. Cambridge, MA: Harvard University Press, 1969.
  11. Tasker RR, Tsuda T, Hawrylyshyn P. Clinical neurophysiological investigation of deafferentation pain. Adv Pain Res Ther 1983;5:713–38.
  12. Fields HL. Pain. New York: McGraw-Hill, 1987.
  13. Xu X-J, Puke MJC, Verge VMK, Wiesenfeld-Hallin Z, Hughes J, Hokfelt T. Up-regulation of cholecystokinin in primary sensory neurons is associated with morphine insensitivity in experimental neuropathic pain in the rat. Neurosci Lett 1993;152:129–32.[Medline]



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