- Email: [email protected]
Contralateral temperature changes of the finger surface during video endoscopic sympathectomy for palmar hyperhidrosis
Journal of the
Autonomic Nervous System EUEVIER
Journal of the Autonomic
Nervous System 59 (I 996) 9% 102
Contralateral temperature changes of the finger surface during video endoscopic sympathectomy for palmar hyperhidrosis Jionn-Jong Wu a3*, Che-Chiao Hsu a, Shong-Yu Liao a, Jiang-Chuan
Liu b, Chun-Jen Shih
’
a Division of Neurosurgery, Department of Surgery, Far Eastern Memorial Hospital. Taipei, Taiwan, ROC b Department of Biology and Anatomy, National Defense Medical Center, Taipei, Taiwan. ROC ’ Professor Emeritus (Neurosurgery), National Defense Medical Center. Taipei, Taiwan, ROC Received 26 October
1995; revised 16 January
1996; accepted
16 January
1996
Abstract One hundred and eight consecutive patients with primary sympathetic ganglia using video thoracoscopic techniques. surface temperature of the ipsilateral index finger was post-operative temperature was 2.74 f 0.27”C (mean + SE)
palmar hyperhidrosis were surgically managed by coagulation of bilateral T2 Patients were divided into two groups. In the first group (N = 461, finger recorded before and after T2 ganglionectomy. The average increase of on the right side and 2.67 + 0.33”C on the left (P < 0.05). The significant rise of temperature resulting from sympatholytic vasodilatation was only noted in cases of exact ablation of the T2 ganglion. In the second group (N = 62), surface temperatures of both index fingers were monitored and recorded simultaneously. These patients were arbitrarily subdivided into Group 2-A (N = 29) when right side ganglionectomy was performed first and Group 2-B (N = 33) when left side ganglionectomy was done initially. After the first ganglionectomy was completed, an ipsilateral increase with a contralateral decrease of temperature was observed; the average increase of temperature was 1.92 + 0.3X and 2.19 k 0.3O”C, and the average decrease was 1.50 + 051°C and 1.67 + 0.39”C for Group 2-A and 2-B respectively (P < 0.05). The authors postulate that a cross-inhibitory effect by the post-ganglionic neurons innervating blood vessels of the upper extremities may exist in humans and this effect is released after ganglionectomy, resulting in contralateral vasoconstriction and decrease of finger surface temperature. Keywords: Thoracic
sympathectomy;
Hyperhidrosis;
Sudomotor;
Vasoconstrictor
1. Introduction Primary palmar hyperhidrosis (PH) seems to be an ethnic disorder. It is quite common in Chinese, Japanese and Jews [1,5,21]. Surgical thoracic sympathectomy of the T2 ganglion (or T2 and T3) is widely accepted as an effective method for the treatment of PH [ 1,4,5,7,12,15, 21,271. Among various surgical modalities, video endoscopic sympathectomy (VES) is a relatively safe and simple method [7,16]. An increase of unilateral palmar temperature after T2 ganglionectomy had been reported [S]. In this case study, the authors continuously monitored the finger surface temperature (FST) of the ipsilateral index finger, and both index fingers simultaneously during 5 different stages of the operation. To our knowledge, not much information is available on the temperature change of the finger on the
* Corresponding
author. Tel.: + 886-2-9546200;
fax: + 886-2-9545567.
01651838/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved PII SO165- 1838(96)00012-4
non-denervated side after contralateral T2 ganglionectomy. We report here the significance of FST changes on both sides and our experience with VES for PH in 108 patients.
2. Materials
and methods
2. I. Patient population From June 1992 to March 1995, 108 consecutive cases of PH were surgically treated at the Far Eastern Memorial Hospital. There were 52 males and 56 females. The age ranged from 12 to 42 years, with a mean age of 22.4 years. They were free from any neurological deficit except for the excessive sweating problem. None had laboratory evidence indicative of underlying systemic diseases. Forty-five patients (41.7%) had a strong family history of hyperhidrosis in first degree relatives. Patients were divided into two groups. Initially (from
J.-J. Wu et al. / Journal of the AutonomicNerwus System 59 (19%) 98-102 June 1992 to May 1993), we only monitored FST of the ipsilateral index finger (Group 1, N = 46). In the later period (from June 1993 to March 1995), simultaneous monitoring of both index finger temperatures was carried out (Group 2, N = 62). 2.2. Operative
technique
Under general anesthesia with a double-lumen endotracheal tube, a 1.5 cm skin incision was made at the third intercostal space in the anterior axillary line. A thoracoscope (Model 26037 A, Karl Storz Co., Stuttgart, Germany) was inserted into the thoracic cavity and connected to a computer compact disc camera video system (Video Processor, Model 86200 C/L, Welch Allyn Inc., NY, USA). The T2 ganglion (including its adjacent rami) was identified and then coagulated completely with a unipolar diathermy probe. The same procedure was repeated on the contralateral side. The average interval between bilateral T2 ganglionectomies was about 10 minutes. 2.3. Temperature
monitoring
Surface temperature of the distal phalanx of the second digit was continuously monitored by a thermometer (Thermalert, Model TH-5, Sensortek Inc., NJ, USA). In Group 1 (N = 46), FST of the ipsilateral index finger was recorded before and 3 minutes after completion of T2 ganglionectomy and the difference was measured. In Group 2 (N = 62), FST of bilateral index fingers was monitored simultaneously and was recorded during 5 different stages of the operation (Stage A: before induction of general anesthesia, Stage B: after draping but before incision, Stage C: before
99
coagulation of the T2 ganglion on the first operative side, Stage D: 3 minutes after coagulation of the T2 ganglion on the first operative side, Stage E: 3 minutes after contralatera1 T2 ganglionectomy). The differences between Stage D and C, and Stage E and D were measured. The patients of Group 2 were arbitrarily subdivided into Group 2-A (N = 29) when ganglionectomy was performed on the right side first and Group 2-B (N = 33) when ganglionectomy was carried out on the left side initially. The pre- and post-operative rectal temperature was monitored in 28 cases of Group 2. The ambient temperature of the operating room was 22.33 f. 0.15”C (mean k standard error>. 2.4. Statistical
analyses
The data concerning temperature changes of the index fingers and rectal temperature in different stages of operation for bilateral T2 ganglionectomy were analyzed by an analysis of variance (ANOVA). The temperature differences between pre- and post-ganglionectomy on the ipsilatera1 side (Group 1) and between ipsilateral finger compared to that of contralateral finger (Group 2) were considered significant when P values < 0.05. Temperature change was not significant when P > 0.05.
3. Results 3.1. Temperature
changes in group 1
After adequate coagulation of each T2 ganglion, a gradual increase of FST on the ipsilateral side was ob-
40 38 -
*
36 -
34.25+0.20
34 -
34.58+0.16
32.43+0.51 33.7120.27
32 G =g 30 :: 28 26 -
27.40+0.50
I
24 -
I -
22 -
RT LT
I
20
/
I
I
I
I
I
I
A
B
C
D
E
STAGES OF OPERATION
Fig. 1. Average temperature
changes in Group 2-A.
100
J.-J. Wu et al. /Journal
of thr Autonomic
served. The average difference was 2.74 + 0.27”C (mean & SE) on the right side and 2.67 k 0.33”C on the left side (P < 0.05). One patient failed to undergo T2 ganglionectomy on the right side because of severe pleural adhesions. There was, of course, no change of FST. A limited elevation of post-coagulation FST was noted on the left side of another patient. This case had persistent profuse sweating of the left palm post-operatively. 3.2. Temperature
changes
in group 2
When the first T2 ganglionectomy (either right or left) was completed, a gradual decrease of FST on the contralatera1 side in addition to the ipsilateral increase of FST was noted (differences between Stage D and C>. And, after completion of the second (contralateral) T2 ganglionectomy, an elevation of FST on both sides (more remarkable on this side) was observed (difference between Stage E and D). In Group 2-A (Fig. 11, after completion of the first (right) side ganglionectomy, the average increase of FST (right side) was 1.92 + 0.35”C and the average decrease (left side) was 1.50 + 0.51”C. After contralateral (left side) ganglionectomy, the average increase of FST was 0.33 ? 0.10°Con the right side and 3.26 + 0.45”C on the left side (P < o.os>. In Group 2-B (Fig. 2), after first (left) side ganglionectomy, the average increase of FST (left side) was 2.19 + 0.3O”C and the average decrease (right side) was 1.67 k 0.39”C. After contralateral (right side) ganglionectomy, the average increase of FST was 0.36 + 0.24”C on the left side and 3.52 + 0.42”C on the right side (P < 0.05). Rectal temperature was monitored in 28 patients. The average pre-operative temperature was 36.77 _t 0.09”C and
Nerrous
S.vstem 59 (19%)
98-102
the average post-operative temperature was 36.46 ? O.lO”C. The difference was 0.36 Ifr 0.09”C (P > 0.05). 3.3. Operatice
results
Ninety-two out of 108 patients (85%) have had followup for a mean period of 23.1 (range, 2-35) months. Ninety patients (97.8%) had satisfactory results. Of the 2 failed cases (Group I), the first patient still had profuse sweating of the right palm and it seemed that sweating amount was not influenced by the contralateral ganglionectomy. He underwent reoperation one week later. The pleural adhesions were dissected free through an additional skin incision and the right side T2 ganglion was cauterized. The second patient was reoperated 10 days later with ablation of the T3 ganglion and coagulation of the sympathetic trunk below the Tl ganglion. The reoperative result of both patients was good. No patient developed Horner’s syndrome. Thirty-three patients (35.9%) had varying degrees of compensatory hyperhidrosis, but it was much less distressing than in the original condition.
4. Discussion Palmar hyperhidrosis is a condition of excessive perspiration of the palms without an obvious etiology. A state of hyperreactivity of the cerebral cortical areas where somatotopic representation of sweating is present and hyperfunction of the sympathetic nervous fibers was proposed to explain this condition [5,17,20,26]. Contralateral hemihyperhidrosis after cerebral infarction has been reported [3,9]. A lesion of a putative sympathoinhibitory pathway which might originate in the cortex was postulated [9]. This suggestion may support the hypothesis of the existence of
40 -
38 -
*
36 -
34.75+0.14
34.32+0.28 32.96+0.50 T
34 -
32 G g
30
if
28.16+0.40
26
L--_--l
24
-
22
20 28 :
I A
I C
B STAGES
Fig. 2. Average
temperature
, E
/ D
OF OPERATION changes
in Group
RT LT
2-B
I
J.-J.
Wu et al. / Joumul
of the
Autonomic
sudomotor neurons in the cortex, but it still remains to be verified. Among the many surgical modalities for treatment of PH, the video endoscopic procedure with ganglionectomy of T2 or T2 and T3 ganglia has proven to be simple, less-invasive and effective [7,16]. For patients with radiologic evidence of chronic pleurisy, other alternatives could be chosen [4,5,27]. It has been well documented that the second thoracic sympathetic ganglion is a key ganglion for sympathetic innervation to the upper extremities [5,19,2 l]. Adequate T2 ganglionectomy is usually sufficient for the treatment of PH. However, postganglionic fibers (Kuntz nerve) arising from the T2 and/or T3 ganglia joining the first thoracic nerve [I I]. and a major sympathetic pathway leaving via the first thoracic ganglion have been demonstrated to provide additional sympathetic innervation to the upper extremities 1151. For cases without elevation of the postganglionectomy FST or failed cases treated previously with T2 ganglionectomy, T3 and even Tl ganglionectomy should be considered [ 12,211. Various methods of intraoperative evaluation, such as electrophysiological studies of the palmar skin perfusion and sympathetic skin response [ 13,241, aside from skin temperature monitoring [8], have been described to confirm the exact sympathetic segment for ablation. Kao et al. [8] observed a significant rise of the ipsilateral palmar skin temperature after interruption of the T2 segment, resulting from sympatholytic vasodilatation. The same result was also noticed in this series and the authors suggest to monitor FST routinely during sympathectomy. The mechanism of FST drop on the non-denervated side after contralateral sympathectomy in the present series (Group 2) is not clear. Many factors and physiologic mechanisms are related to temperature regulation. For example, heat is lost from the respiratory tract and skin, in excretion, by changes in dermal skin blood flow and thermoregulatory sweating [2.18]. In the present study, the patient’s palm is anhidrotic under general anesthesia. Thus, the cause of FST drop is not related to heat loss through increased sweat excretion. Studies in man have shown reflex vasodilatation in the fingers of one hand after heating of the opposite extremity. A mechanism by which the central temperature-sensitive structures may be activated by a reflex whose afferents come from the skin and the temperature of the blood is considered [2]. In this study, the increase of FST on the sympathectomized hand did not induce reflex vasodilatation in the fingers of the non-denervated hand and instead vasoconstriction (significant decrease of FST) was observed. In effect. this finding is thought not related to the mechanism of vasomotor response due to the activity of the central temperature-sensitive structures. Therefore, the authors propose that the reduction of FST on the non-denervated side is due to vasoconstriction induced by the denervation of the cross-inhibitory fibers
Ner~~ous Swern
59 (19%)
9K- 102
101
which originate from the contralateral T2 ganglion. These fibers can modulate the activity of the contralateral postganglionic neuron. When the first T2 ganglionectomy is performed, effect of cross inhibition is released, accounting for contralateral vasoconstriction. Moreover. in our previous study of the origins of the afferent fibers to the cat superior cervical ganglia (SCG) [28], we found out that the pre-ganglionic sympathetic neurons were located not only in the ipsilateral spinal cord (C8-T5 segments), extra-SCG neurons (ipsilateral middle and stellate ganglia) and ipsilateral mandibular division of the trigeminal ganglion, but also in the caudal part of the contralateral SCG. Based on this experimental study and the findings in this series, we believe that similar cross innervations exist in humans. Janig et al. [6] reported that vasoconstrictor neurons are remarkably under inhibitory control of various afferent input system from the body surface while sudomotor neurons under excitatory control. Both systems are almost completely reciprocally organized and the determinant neuronal arrangement of this reciprocal organization may be at the spinal level. Konishi et al. [ 10,251 demonstrated that some afferent fibers appear to pass through the sympathetic ganglia and enter the spinal cord. They also suggested that the preganglionic cholinergic signals to the postganglionic neurons in mammalian sympathetic ganglia is under the influence of peptidergic excitatory and inhibitory transmitters. Accordingly, cross inhibition by visceral afferent in the spinal cord may be another possibility to explain the contralateral FST reduction. The autonomic nervous system CANS) has been classically shown to be a simple ‘two-neurons system’ in which the post-ganglionic neuron receives innervation from the pre-ganglionic neuron only. But the results of this series and the cat SCG study are consistent with the idea that the ANS may be a ‘complex system’ in which the post-ganglionic neuron at any given level in the spinal cord can modulate activities reciprocally. However, presently, it is unclear why an inhibitory effect by the contralateral post-ganglionic neuron has been favored by evolutionary time. Since the organism usually sweats bilaterally and not unilaterally. there seems to be no need for developing or evolving a mechanism to inhibit sweating on the contralateral side. On the other hand, one can envision another scenario in which the cross inhibitory effect serves to ‘fine-tune’ the sweating response. In fact, the idea of reciprocal innervation has been suggested in the skin-pressure sweating reflex in humans. The pressure, on the specified area of the body surface, caused inhibition of sweating on the ipsilateral side and facilitation on the contralateral side [ 14,22,23]. The authors would like to propose the idea of cross-inhibitory effect to explain the possible mechanism of abnormal profuse sweating which may be due to either a decrease of cross-inhibitory effect or the abnormal control of the inhibitory fibers by the sudomotor center. In either
102
J.-J. Wu et al. /Journal
of the Autonomic
case, cross-inhibitory fibers play a crucial role in the sweating response. The detailed anatomical pathway of cross innervation remains relatively elusive and provides us a fertile ground for further experimental studies. An understanding of such a pathway will undoubtedly afford the opportunity to unravel the etiology of palmar hyperhidrosis.
Acknowledgements The authors wish to thank Dr. Nien-Hsien valuable assistance in statistical analyses.
Liou for his
References [l] Adar, R., Kurchin, A., Zweig, A. and Mozes, M. (1977) Palmar hyperhidrosis and its surgical treatment: A report of 100 cases. Ann. Surg. 186, 34-41. [2] Appenzeller, 0. (19901 The Autonomic Nervous System. Elsevier, Amsterdam, 35 pp. [3] Bassetti, C. and Staikov, IN. (1995) Hemiplegia vegetativa altema (ipsilateral Homer’s syndrome and contralateral hemihyperhidrosis) following proximal posterior cerebral artery occlusion, Stroke 26, 702-704. [4] Chuang, K.S., Liou, N.H. and Liu, J.C. (1988) New stereotactic technique for percutaneous thermocoagulation upper thoracic ganglionectomy in cases of palmar hyperhidrosis. Neurosurgery 22, 600-604. [51 Cloward, R.B. (19691 Hyperhidrosis. J. Neurosurg. 30, 545-55 1. [6] Janig, W. and Kummel, H. (1981) Organization of the sympathetic innervation supplying the hairless skin of the cat’s paw. .I. Auton. Nerv. Syst. 3, 215-230. 171 Kao, M.C. (1992) Video endoscopic sympathectomy using a fiberop tic CO, laser to treat palmar hyperhidrosis. Neurosurgery 30, 131135. [8] Kao, M.C., Tsai, J.C., Lai, D.M., Hsiao, Y.Y., Lee, Y.S. and Chiu, M.J. (1994) Autonomic activities in hyperhidrosis patients before, during, and after endoscopic laser sympathectomy. Neurosurgery 34, 262-268. [9] Kim, B.S., Kim, Y.I. and Lee, K.S. (1995) Contralateral hyperhidrosis after cerebral infarction. Clinicoanatomic correlations in five cases. Stroke 26, 896-899. [lo] Konishi, S., Tsunoo. A., Yanaihara, N. and Otsuka. M. (1980) Peptidergic excitatory and inhibitory synapses in mammalian sympa-
Newous
System 59 (1996) 9X-102
thetic ganglia: Roles of substance P and enkephalin. Biomedical Res. 1, 528-536. [Ill Kuntz, A., Alexander, W.F. and Furcolo, C.L. (1938) Complete sympathetic denervation of the upper extremity. Ann. Surg. 107, 25-36. 1121Kux, M. (1978) Thoracic endoscopic sympathectomy for palmar hyperhidrosis. Arch. Surg. 10, 292-296. [I31 Lindquist, C., Fedorcsak, I. and Steig, P.E. (1989) Electrophysiological aid in high thoracic sympathectomy for palmar hyperhidrosis. Neurosurgery 24, 449-452. t141 Ogawa, T., Asayama. M., Ito, M. and Yoshida, K. (1979) Significance of skin pressure in body heat balance. Jpn. J. Physiol. 29, 805-816. approach for upper [I51 Palumbo, L.T. (1956) Anterior transthoracic thoracic sympathectomy. Arch. Surg. 72, 659-666. [161Robertson, D.P., Simpson, R.K., Rose, J.E. and Garza, J.S. (1993) Video-assisted endoscopic thoracic ganglionectomy. J. Neurosurg. 79, 238-240. [I71 Shih, C.J. (1979) Compensatory sweating after upper dorsal sympathectomy. J. Neurosurg. 51, 424-425. sweating in [I81Shih, C.J. and Lin, M.T. (1979) Thermoregulatory palmar hyperhidrosis before and after upper thoracic sympathectomy. J. Neurosurg. 50, 88-94. t191 Shih, C.J. and Lin, M.T. (1980) Effects of cholinomimetic drugs on sudomotor, metabolic, respiratory, vasomotor, and temperature response in palmar hyperhidrosis. J. Neurosurg. 53, 684-689. 1201 Shih, C.J., Wu, J.J. and Lin, M.T. (1983) Autonomic dysfunction in palmar hyperhidrosis. J. Auton. Nerv. Syst. 8, 33-43. 1211Shih, C.J. and Wang, Y.C. (1978) Thoracic sympathectomy for palmar hyperhidrosis: Report of 457 cases, Surg. Neurol. 10, 291296. 1221Tadaki, E., Kumazawa, T., Mizumura, K. and Takagi, K. (1981) Hemihidrosis due to skin pressure with particular remarks on the intenisity and area of the pressure stimuli. Jpn. J. Physiol. 31, 259-267. [231 Tdkagi, K. and Kobayasi S. (1955) Skin pressure-vegetative reflex. Acta Med. Biol. 4, 31-57. [241 Tsai. Y.L., Chiu. M.J., Kao, M.C. and Chen, R.C. (1992) Sympathetic skin response in hyperhidrosis: An electrophysiological evaluation for surgical treatment. Actd. Neurol. Sin. I, 25-30. f251 Tsunoo, A., Konishi, S. and Otsuka M. (1982) Substance P as an excitatory transmitter of primary afferent neurons in guinea-pig sympathetic ganglia. Neuroscience 7, 2025-2037. [261 Veal, J.R. and Shadid, J.N. (1949) Hyperhidrosis: Observation on the study of sixty-one cases. Surgery 26, 89-98. upper thoracic [271Wilkinson, H.A. (19841 Percutaneous radiofrequency sympathectomy: A new technique. Neurosurgery 15, 8 1 l-8 14. [281Yau, J.I., Wu, J.J. and Liu, J.C. (1991) Origins of the afferent fibers to the cat superior cervical ganglion. Proc. Nat. Sci. Count. B. ROC 15, l-7.
Autonomic Nervous System EUEVIER
Journal of the Autonomic
Nervous System 59 (I 996) 9% 102
Contralateral temperature changes of the finger surface during video endoscopic sympathectomy for palmar hyperhidrosis Jionn-Jong Wu a3*, Che-Chiao Hsu a, Shong-Yu Liao a, Jiang-Chuan
Liu b, Chun-Jen Shih
’
a Division of Neurosurgery, Department of Surgery, Far Eastern Memorial Hospital. Taipei, Taiwan, ROC b Department of Biology and Anatomy, National Defense Medical Center, Taipei, Taiwan. ROC ’ Professor Emeritus (Neurosurgery), National Defense Medical Center. Taipei, Taiwan, ROC Received 26 October
1995; revised 16 January
1996; accepted
16 January
1996
Abstract One hundred and eight consecutive patients with primary sympathetic ganglia using video thoracoscopic techniques. surface temperature of the ipsilateral index finger was post-operative temperature was 2.74 f 0.27”C (mean + SE)
palmar hyperhidrosis were surgically managed by coagulation of bilateral T2 Patients were divided into two groups. In the first group (N = 461, finger recorded before and after T2 ganglionectomy. The average increase of on the right side and 2.67 + 0.33”C on the left (P < 0.05). The significant rise of temperature resulting from sympatholytic vasodilatation was only noted in cases of exact ablation of the T2 ganglion. In the second group (N = 62), surface temperatures of both index fingers were monitored and recorded simultaneously. These patients were arbitrarily subdivided into Group 2-A (N = 29) when right side ganglionectomy was performed first and Group 2-B (N = 33) when left side ganglionectomy was done initially. After the first ganglionectomy was completed, an ipsilateral increase with a contralateral decrease of temperature was observed; the average increase of temperature was 1.92 + 0.3X and 2.19 k 0.3O”C, and the average decrease was 1.50 + 051°C and 1.67 + 0.39”C for Group 2-A and 2-B respectively (P < 0.05). The authors postulate that a cross-inhibitory effect by the post-ganglionic neurons innervating blood vessels of the upper extremities may exist in humans and this effect is released after ganglionectomy, resulting in contralateral vasoconstriction and decrease of finger surface temperature. Keywords: Thoracic
sympathectomy;
Hyperhidrosis;
Sudomotor;
Vasoconstrictor
1. Introduction Primary palmar hyperhidrosis (PH) seems to be an ethnic disorder. It is quite common in Chinese, Japanese and Jews [1,5,21]. Surgical thoracic sympathectomy of the T2 ganglion (or T2 and T3) is widely accepted as an effective method for the treatment of PH [ 1,4,5,7,12,15, 21,271. Among various surgical modalities, video endoscopic sympathectomy (VES) is a relatively safe and simple method [7,16]. An increase of unilateral palmar temperature after T2 ganglionectomy had been reported [S]. In this case study, the authors continuously monitored the finger surface temperature (FST) of the ipsilateral index finger, and both index fingers simultaneously during 5 different stages of the operation. To our knowledge, not much information is available on the temperature change of the finger on the
* Corresponding
author. Tel.: + 886-2-9546200;
fax: + 886-2-9545567.
01651838/96/$15.00 0 1996 Elsevier Science B.V. All rights reserved PII SO165- 1838(96)00012-4
non-denervated side after contralateral T2 ganglionectomy. We report here the significance of FST changes on both sides and our experience with VES for PH in 108 patients.
2. Materials
and methods
2. I. Patient population From June 1992 to March 1995, 108 consecutive cases of PH were surgically treated at the Far Eastern Memorial Hospital. There were 52 males and 56 females. The age ranged from 12 to 42 years, with a mean age of 22.4 years. They were free from any neurological deficit except for the excessive sweating problem. None had laboratory evidence indicative of underlying systemic diseases. Forty-five patients (41.7%) had a strong family history of hyperhidrosis in first degree relatives. Patients were divided into two groups. Initially (from
J.-J. Wu et al. / Journal of the AutonomicNerwus System 59 (19%) 98-102 June 1992 to May 1993), we only monitored FST of the ipsilateral index finger (Group 1, N = 46). In the later period (from June 1993 to March 1995), simultaneous monitoring of both index finger temperatures was carried out (Group 2, N = 62). 2.2. Operative
technique
Under general anesthesia with a double-lumen endotracheal tube, a 1.5 cm skin incision was made at the third intercostal space in the anterior axillary line. A thoracoscope (Model 26037 A, Karl Storz Co., Stuttgart, Germany) was inserted into the thoracic cavity and connected to a computer compact disc camera video system (Video Processor, Model 86200 C/L, Welch Allyn Inc., NY, USA). The T2 ganglion (including its adjacent rami) was identified and then coagulated completely with a unipolar diathermy probe. The same procedure was repeated on the contralateral side. The average interval between bilateral T2 ganglionectomies was about 10 minutes. 2.3. Temperature
monitoring
Surface temperature of the distal phalanx of the second digit was continuously monitored by a thermometer (Thermalert, Model TH-5, Sensortek Inc., NJ, USA). In Group 1 (N = 46), FST of the ipsilateral index finger was recorded before and 3 minutes after completion of T2 ganglionectomy and the difference was measured. In Group 2 (N = 62), FST of bilateral index fingers was monitored simultaneously and was recorded during 5 different stages of the operation (Stage A: before induction of general anesthesia, Stage B: after draping but before incision, Stage C: before
99
coagulation of the T2 ganglion on the first operative side, Stage D: 3 minutes after coagulation of the T2 ganglion on the first operative side, Stage E: 3 minutes after contralatera1 T2 ganglionectomy). The differences between Stage D and C, and Stage E and D were measured. The patients of Group 2 were arbitrarily subdivided into Group 2-A (N = 29) when ganglionectomy was performed on the right side first and Group 2-B (N = 33) when ganglionectomy was carried out on the left side initially. The pre- and post-operative rectal temperature was monitored in 28 cases of Group 2. The ambient temperature of the operating room was 22.33 f. 0.15”C (mean k standard error>. 2.4. Statistical
analyses
The data concerning temperature changes of the index fingers and rectal temperature in different stages of operation for bilateral T2 ganglionectomy were analyzed by an analysis of variance (ANOVA). The temperature differences between pre- and post-ganglionectomy on the ipsilatera1 side (Group 1) and between ipsilateral finger compared to that of contralateral finger (Group 2) were considered significant when P values < 0.05. Temperature change was not significant when P > 0.05.
3. Results 3.1. Temperature
changes in group 1
After adequate coagulation of each T2 ganglion, a gradual increase of FST on the ipsilateral side was ob-
40 38 -
*
36 -
34.25+0.20
34 -
34.58+0.16
32.43+0.51 33.7120.27
32 G =g 30 :: 28 26 -
27.40+0.50
I
24 -
I -
22 -
RT LT
I
20
/
I
I
I
I
I
I
A
B
C
D
E
STAGES OF OPERATION
Fig. 1. Average temperature
changes in Group 2-A.
100
J.-J. Wu et al. /Journal
of thr Autonomic
served. The average difference was 2.74 + 0.27”C (mean & SE) on the right side and 2.67 k 0.33”C on the left side (P < 0.05). One patient failed to undergo T2 ganglionectomy on the right side because of severe pleural adhesions. There was, of course, no change of FST. A limited elevation of post-coagulation FST was noted on the left side of another patient. This case had persistent profuse sweating of the left palm post-operatively. 3.2. Temperature
changes
in group 2
When the first T2 ganglionectomy (either right or left) was completed, a gradual decrease of FST on the contralatera1 side in addition to the ipsilateral increase of FST was noted (differences between Stage D and C>. And, after completion of the second (contralateral) T2 ganglionectomy, an elevation of FST on both sides (more remarkable on this side) was observed (difference between Stage E and D). In Group 2-A (Fig. 11, after completion of the first (right) side ganglionectomy, the average increase of FST (right side) was 1.92 + 0.35”C and the average decrease (left side) was 1.50 + 0.51”C. After contralateral (left side) ganglionectomy, the average increase of FST was 0.33 ? 0.10°Con the right side and 3.26 + 0.45”C on the left side (P < o.os>. In Group 2-B (Fig. 2), after first (left) side ganglionectomy, the average increase of FST (left side) was 2.19 + 0.3O”C and the average decrease (right side) was 1.67 k 0.39”C. After contralateral (right side) ganglionectomy, the average increase of FST was 0.36 + 0.24”C on the left side and 3.52 + 0.42”C on the right side (P < 0.05). Rectal temperature was monitored in 28 patients. The average pre-operative temperature was 36.77 _t 0.09”C and
Nerrous
S.vstem 59 (19%)
98-102
the average post-operative temperature was 36.46 ? O.lO”C. The difference was 0.36 Ifr 0.09”C (P > 0.05). 3.3. Operatice
results
Ninety-two out of 108 patients (85%) have had followup for a mean period of 23.1 (range, 2-35) months. Ninety patients (97.8%) had satisfactory results. Of the 2 failed cases (Group I), the first patient still had profuse sweating of the right palm and it seemed that sweating amount was not influenced by the contralateral ganglionectomy. He underwent reoperation one week later. The pleural adhesions were dissected free through an additional skin incision and the right side T2 ganglion was cauterized. The second patient was reoperated 10 days later with ablation of the T3 ganglion and coagulation of the sympathetic trunk below the Tl ganglion. The reoperative result of both patients was good. No patient developed Horner’s syndrome. Thirty-three patients (35.9%) had varying degrees of compensatory hyperhidrosis, but it was much less distressing than in the original condition.
4. Discussion Palmar hyperhidrosis is a condition of excessive perspiration of the palms without an obvious etiology. A state of hyperreactivity of the cerebral cortical areas where somatotopic representation of sweating is present and hyperfunction of the sympathetic nervous fibers was proposed to explain this condition [5,17,20,26]. Contralateral hemihyperhidrosis after cerebral infarction has been reported [3,9]. A lesion of a putative sympathoinhibitory pathway which might originate in the cortex was postulated [9]. This suggestion may support the hypothesis of the existence of
40 -
38 -
*
36 -
34.75+0.14
34.32+0.28 32.96+0.50 T
34 -
32 G g
30
if
28.16+0.40
26
L--_--l
24
-
22
20 28 :
I A
I C
B STAGES
Fig. 2. Average
temperature
, E
/ D
OF OPERATION changes
in Group
RT LT
2-B
I
J.-J.
Wu et al. / Joumul
of the
Autonomic
sudomotor neurons in the cortex, but it still remains to be verified. Among the many surgical modalities for treatment of PH, the video endoscopic procedure with ganglionectomy of T2 or T2 and T3 ganglia has proven to be simple, less-invasive and effective [7,16]. For patients with radiologic evidence of chronic pleurisy, other alternatives could be chosen [4,5,27]. It has been well documented that the second thoracic sympathetic ganglion is a key ganglion for sympathetic innervation to the upper extremities [5,19,2 l]. Adequate T2 ganglionectomy is usually sufficient for the treatment of PH. However, postganglionic fibers (Kuntz nerve) arising from the T2 and/or T3 ganglia joining the first thoracic nerve [I I]. and a major sympathetic pathway leaving via the first thoracic ganglion have been demonstrated to provide additional sympathetic innervation to the upper extremities 1151. For cases without elevation of the postganglionectomy FST or failed cases treated previously with T2 ganglionectomy, T3 and even Tl ganglionectomy should be considered [ 12,211. Various methods of intraoperative evaluation, such as electrophysiological studies of the palmar skin perfusion and sympathetic skin response [ 13,241, aside from skin temperature monitoring [8], have been described to confirm the exact sympathetic segment for ablation. Kao et al. [8] observed a significant rise of the ipsilateral palmar skin temperature after interruption of the T2 segment, resulting from sympatholytic vasodilatation. The same result was also noticed in this series and the authors suggest to monitor FST routinely during sympathectomy. The mechanism of FST drop on the non-denervated side after contralateral sympathectomy in the present series (Group 2) is not clear. Many factors and physiologic mechanisms are related to temperature regulation. For example, heat is lost from the respiratory tract and skin, in excretion, by changes in dermal skin blood flow and thermoregulatory sweating [2.18]. In the present study, the patient’s palm is anhidrotic under general anesthesia. Thus, the cause of FST drop is not related to heat loss through increased sweat excretion. Studies in man have shown reflex vasodilatation in the fingers of one hand after heating of the opposite extremity. A mechanism by which the central temperature-sensitive structures may be activated by a reflex whose afferents come from the skin and the temperature of the blood is considered [2]. In this study, the increase of FST on the sympathectomized hand did not induce reflex vasodilatation in the fingers of the non-denervated hand and instead vasoconstriction (significant decrease of FST) was observed. In effect. this finding is thought not related to the mechanism of vasomotor response due to the activity of the central temperature-sensitive structures. Therefore, the authors propose that the reduction of FST on the non-denervated side is due to vasoconstriction induced by the denervation of the cross-inhibitory fibers
Ner~~ous Swern
59 (19%)
9K- 102
101
which originate from the contralateral T2 ganglion. These fibers can modulate the activity of the contralateral postganglionic neuron. When the first T2 ganglionectomy is performed, effect of cross inhibition is released, accounting for contralateral vasoconstriction. Moreover. in our previous study of the origins of the afferent fibers to the cat superior cervical ganglia (SCG) [28], we found out that the pre-ganglionic sympathetic neurons were located not only in the ipsilateral spinal cord (C8-T5 segments), extra-SCG neurons (ipsilateral middle and stellate ganglia) and ipsilateral mandibular division of the trigeminal ganglion, but also in the caudal part of the contralateral SCG. Based on this experimental study and the findings in this series, we believe that similar cross innervations exist in humans. Janig et al. [6] reported that vasoconstrictor neurons are remarkably under inhibitory control of various afferent input system from the body surface while sudomotor neurons under excitatory control. Both systems are almost completely reciprocally organized and the determinant neuronal arrangement of this reciprocal organization may be at the spinal level. Konishi et al. [ 10,251 demonstrated that some afferent fibers appear to pass through the sympathetic ganglia and enter the spinal cord. They also suggested that the preganglionic cholinergic signals to the postganglionic neurons in mammalian sympathetic ganglia is under the influence of peptidergic excitatory and inhibitory transmitters. Accordingly, cross inhibition by visceral afferent in the spinal cord may be another possibility to explain the contralateral FST reduction. The autonomic nervous system CANS) has been classically shown to be a simple ‘two-neurons system’ in which the post-ganglionic neuron receives innervation from the pre-ganglionic neuron only. But the results of this series and the cat SCG study are consistent with the idea that the ANS may be a ‘complex system’ in which the post-ganglionic neuron at any given level in the spinal cord can modulate activities reciprocally. However, presently, it is unclear why an inhibitory effect by the contralateral post-ganglionic neuron has been favored by evolutionary time. Since the organism usually sweats bilaterally and not unilaterally. there seems to be no need for developing or evolving a mechanism to inhibit sweating on the contralateral side. On the other hand, one can envision another scenario in which the cross inhibitory effect serves to ‘fine-tune’ the sweating response. In fact, the idea of reciprocal innervation has been suggested in the skin-pressure sweating reflex in humans. The pressure, on the specified area of the body surface, caused inhibition of sweating on the ipsilateral side and facilitation on the contralateral side [ 14,22,23]. The authors would like to propose the idea of cross-inhibitory effect to explain the possible mechanism of abnormal profuse sweating which may be due to either a decrease of cross-inhibitory effect or the abnormal control of the inhibitory fibers by the sudomotor center. In either
102
J.-J. Wu et al. /Journal
of the Autonomic
case, cross-inhibitory fibers play a crucial role in the sweating response. The detailed anatomical pathway of cross innervation remains relatively elusive and provides us a fertile ground for further experimental studies. An understanding of such a pathway will undoubtedly afford the opportunity to unravel the etiology of palmar hyperhidrosis.
Acknowledgements The authors wish to thank Dr. Nien-Hsien valuable assistance in statistical analyses.
Liou for his
References [l] Adar, R., Kurchin, A., Zweig, A. and Mozes, M. (1977) Palmar hyperhidrosis and its surgical treatment: A report of 100 cases. Ann. Surg. 186, 34-41. [2] Appenzeller, 0. (19901 The Autonomic Nervous System. Elsevier, Amsterdam, 35 pp. [3] Bassetti, C. and Staikov, IN. (1995) Hemiplegia vegetativa altema (ipsilateral Homer’s syndrome and contralateral hemihyperhidrosis) following proximal posterior cerebral artery occlusion, Stroke 26, 702-704. [4] Chuang, K.S., Liou, N.H. and Liu, J.C. (1988) New stereotactic technique for percutaneous thermocoagulation upper thoracic ganglionectomy in cases of palmar hyperhidrosis. Neurosurgery 22, 600-604. [51 Cloward, R.B. (19691 Hyperhidrosis. J. Neurosurg. 30, 545-55 1. [6] Janig, W. and Kummel, H. (1981) Organization of the sympathetic innervation supplying the hairless skin of the cat’s paw. .I. Auton. Nerv. Syst. 3, 215-230. 171 Kao, M.C. (1992) Video endoscopic sympathectomy using a fiberop tic CO, laser to treat palmar hyperhidrosis. Neurosurgery 30, 131135. [8] Kao, M.C., Tsai, J.C., Lai, D.M., Hsiao, Y.Y., Lee, Y.S. and Chiu, M.J. (1994) Autonomic activities in hyperhidrosis patients before, during, and after endoscopic laser sympathectomy. Neurosurgery 34, 262-268. [9] Kim, B.S., Kim, Y.I. and Lee, K.S. (1995) Contralateral hyperhidrosis after cerebral infarction. Clinicoanatomic correlations in five cases. Stroke 26, 896-899. [lo] Konishi, S., Tsunoo. A., Yanaihara, N. and Otsuka. M. (1980) Peptidergic excitatory and inhibitory synapses in mammalian sympa-
Newous
System 59 (1996) 9X-102
thetic ganglia: Roles of substance P and enkephalin. Biomedical Res. 1, 528-536. [Ill Kuntz, A., Alexander, W.F. and Furcolo, C.L. (1938) Complete sympathetic denervation of the upper extremity. Ann. Surg. 107, 25-36. 1121Kux, M. (1978) Thoracic endoscopic sympathectomy for palmar hyperhidrosis. Arch. Surg. 10, 292-296. [I31 Lindquist, C., Fedorcsak, I. and Steig, P.E. (1989) Electrophysiological aid in high thoracic sympathectomy for palmar hyperhidrosis. Neurosurgery 24, 449-452. t141 Ogawa, T., Asayama. M., Ito, M. and Yoshida, K. (1979) Significance of skin pressure in body heat balance. Jpn. J. Physiol. 29, 805-816. approach for upper [I51 Palumbo, L.T. (1956) Anterior transthoracic thoracic sympathectomy. Arch. Surg. 72, 659-666. [161Robertson, D.P., Simpson, R.K., Rose, J.E. and Garza, J.S. (1993) Video-assisted endoscopic thoracic ganglionectomy. J. Neurosurg. 79, 238-240. [I71 Shih, C.J. (1979) Compensatory sweating after upper dorsal sympathectomy. J. Neurosurg. 51, 424-425. sweating in [I81Shih, C.J. and Lin, M.T. (1979) Thermoregulatory palmar hyperhidrosis before and after upper thoracic sympathectomy. J. Neurosurg. 50, 88-94. t191 Shih, C.J. and Lin, M.T. (1980) Effects of cholinomimetic drugs on sudomotor, metabolic, respiratory, vasomotor, and temperature response in palmar hyperhidrosis. J. Neurosurg. 53, 684-689. 1201 Shih, C.J., Wu, J.J. and Lin, M.T. (1983) Autonomic dysfunction in palmar hyperhidrosis. J. Auton. Nerv. Syst. 8, 33-43. 1211Shih, C.J. and Wang, Y.C. (1978) Thoracic sympathectomy for palmar hyperhidrosis: Report of 457 cases, Surg. Neurol. 10, 291296. 1221Tadaki, E., Kumazawa, T., Mizumura, K. and Takagi, K. (1981) Hemihidrosis due to skin pressure with particular remarks on the intenisity and area of the pressure stimuli. Jpn. J. Physiol. 31, 259-267. [231 Tdkagi, K. and Kobayasi S. (1955) Skin pressure-vegetative reflex. Acta Med. Biol. 4, 31-57. [241 Tsai. Y.L., Chiu. M.J., Kao, M.C. and Chen, R.C. (1992) Sympathetic skin response in hyperhidrosis: An electrophysiological evaluation for surgical treatment. Actd. Neurol. Sin. I, 25-30. f251 Tsunoo, A., Konishi, S. and Otsuka M. (1982) Substance P as an excitatory transmitter of primary afferent neurons in guinea-pig sympathetic ganglia. Neuroscience 7, 2025-2037. [261 Veal, J.R. and Shadid, J.N. (1949) Hyperhidrosis: Observation on the study of sixty-one cases. Surgery 26, 89-98. upper thoracic [271Wilkinson, H.A. (19841 Percutaneous radiofrequency sympathectomy: A new technique. Neurosurgery 15, 8 1 l-8 14. [281Yau, J.I., Wu, J.J. and Liu, J.C. (1991) Origins of the afferent fibers to the cat superior cervical ganglion. Proc. Nat. Sci. Count. B. ROC 15, l-7.