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a Department of Neurosurgery, Medical University of Vienna, Vienna, Austria
b Center for Anatomy and Cell Biology, Medical University of Vienna, Vienna, Austria
c Division of General Surgery, Department of Surgery, Medical University of Vienna, Vienna, Austria
Accepted for publication May 21, 2008.
* Address correspondence to Dr Neumayer, Division of General Surgery, AKH - E21.A, Department of Surgery, Medical University of Vienna, Währinger Gürtel 18-20, Vienna, 1090, Austria (Email: christoph.neumayer{at}meduniwien.ac.at).
| Abstract |
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Methods: Video-assisted thoracoscopy was performed in 33 thoracic cavities of fresh human cadavers within 48 hours postmortem, followed by anatomic dissection of the first intercostal space. Kuntz's nerves and concomitant blood vessels were of special interest. Statistical analysis included frequencies and
2 tests.
Results: Kuntz's nerves were identified in 12.1% by thoracoscopy, whereas anatomic dissection revealed KNs in 66.7% (p = 0.003). Subpleural veins (mean diameter, 2.2 ± 0.9 mm) parallel to KNs were found in 81.8%. No collateral arteries were identified. Diameters of KNs were 1.4 ± 0.7 mm; distances between the first thoracic ganglion and the middle of KNs were 9.7 ± 3.0 mm. Thoracoscopic recognition of these Kuntz veins was higher than that of KNs (62.5% vs 18.2%, p < 0.005).
Conclusions: The low thoracoscopic detection rate of KNs may be due to the low color contrast of these small fibers. They have, however, most frequently concomitant subpleural veins that are easier to detect. These veins may serve as orientation landmarks of KNs and thus contribute to a more complete denervation improving the outcome of thoracoscopic sympathectomies.
| Introduction |
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First and foremost, collateral nerve fibers bypassing the sympathetic trunk have been made responsible for these failures [7, 12–19]. In particular, Kuntz's nerve (KN), connecting the first and second thoracic nerves, has been blamed for poor surgical outcome [7, 12–16, 18]. These sympathetic fibers reach the brachial plexus without passing through the sympathetic trunk [12, 20, 21]. The prevalence of the KNs, however, varies considerably between surgical and anatomic literature. Clinical studies describe KNs in about 10% of cases [7–9, 15, 18, 22], whereas anatomic investigations report KNs in up to 80% [12, 16–21, 23].
The aim of this clinically orientated cadaveric study was to investigate the presence and distribution of alternate neural pathways in the first intercostal space by video-assisted thoracoscopy. Endoscopic investigation was followed by anatomic dissection of this region of interest. Subsequent comparison of thoracoscopic and anatomic findings tried to elucidate the controversy about the prevalence of KNs. In addition, emphasis was placed on anatomic structures possibly serving as landmarks of KNs.
| Material and Methods |
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All thoracoscopies and anatomic dissections were done at the Department of Anatomy and Cell Biology at the Medical University of Vienna. The study was performed according to the guidelines of "Good Scientific Practice" edited by the Medical University of Vienna and is in line with the Helsinki Declaration. All donors gave their written consent to participate in the study before they died, which was approved by the Institutional Review Board.
Video-assisted thoracoscopy was performed using a 10-mm endoscope (Storz Company, Tuttlingen, Germany) inserted in the fourth intercostal space in the midaxillary line. After identification of the sympathetic trunk, the topographic anatomy of its upper thoracic segments was analyzed, and special attention was given to the presence of KNs and concomitant veins. The procedures were recorded by video-assisted digital imaging and analyzed thereafter to obtain maximal accuracy. Thoracoscopic investigations were followed by anatomic dissections of the first intercostal space. The anterior chest wall was removed from the first to the fourth intercostal space for macroscopic dissections of the sympathetic trunk and its neural pathways. Likewise, subpleural veins such as superior intercostal veins were dissected in this region of interest. Distances between the first thoracic ganglia and the middle of the KNs were recorded.
Statistical analysis was performed with SPSS 14.0 software (SPSS Inc, Chicago, IL). Variables have been described by frequencies and means and standard deviations. Statistical significance was tested with
2 tests. Values of p < 0.05 were considered statistically significant.
| Results |
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Thoracoscopic identification of KNs was significantly lower than the actual prevalence revealed by anatomic dissection (p = 0.003). The detection rate of superior intercostal veins by thoracoscopy was significantly higher than that of KNs (15 of 24 [62.5%] vs 4 of 22 [18.2%], p < 0.005). KNs in combination with concomitant superior intercostal veins were found most frequently by anatomic dissection compared with all other combinations; that is, the presence of single KNs, single veins, and no KNs or veins at all (p = 0.001).
The mean diameter of KNs was 1.4 ± 0.7 mm (range, 0.4 and 3.4 mm). The mean distance between the first thoracic ganglion and the middle of the KNs was 9.7 ± 3.0 mm (range, 3 to 18 mm).
| Comment |
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The actual prevalence of KNs was 66.7% as revealed by anatomic dissection in our study. These findings are in accordance with other anatomic studies [12, 16–21, 23]. However, most of the KNs were not identified thoracoscopically. This problem is striking because it reflects the discrepancy of different detection rates within the surgical [7–9, 15, 18, 22] and anatomic literature [12, 16–21, 23].
The reasons for the low detection rates of KNs during ETS are varied. Identification of nerve fibers beneath the parietal pleura may be more difficult in case of pleural adhesions, which have been reported in up to 58% in patients undergoing repeated sympathectomy [7]. In fact, pleural adhesions have been described as the most important reason for failure of ETS [22]. In patients without previous thoracic operations or diseases, however, the incidence of pleural adhesions was 2.3% to 6.4% [8, 22, 26]. In our own clinical experience of more than 1200 ETS procedures, pleural adhesion rates were below 3% in young hyperhidrotic adults and adolescents. Consequently, pleural adhesions and increased fibrosis may in fact reduce the recognizability of KNs in distinct cases, but are unlikely the major factor for the low detection rate of KNs in general.
Pronounced subpleural fat tissue may additionally aggravate the low recognizability of KNs. In future, this problem may become even more prevalent because obesity is an increasing phenomenon in Western European countries and North America. Nevertheless, most hyperhidrotic patients are lean, young adults.
Varying definitions of the KN probably add to the discrepancy of its prevalence. Originally, only nerve fibers in the first intercostal space between the first and second intrathoracic nerves were classified as KNs [12]. Recently, two different anatomic classifications of rami communicantes have been published [16, 17, 21]. Both are in line with the original definition of KNs [12], to which we adhered in our present study, too. On contrary, there is anatomic [17, 19] as well as surgical literature [27] defining rami communicantes in the upper thoracic trunk between the T1 or T2 ganglion to the T4 ganglion as KNs, even though these variations did not necessarily contribute to the brachial plexus.
The major reason for the low recognition rate of KNs below the parietal pleura, however, is—at least according to our own experience—the low color contrast of these small neural structures. In addition, the quality of the endoscopic equipment may influence the detection rate of KNs. When a high-definition camera that provides a sharp, bright picture is used, many more KNs may be identified. On the other hand, technology of the latest generation is not always available in the clinical situation. Moreover, the sympathetic trunk, which is at least three to four times as thick as the KN, is even in experienced hands not readily visible intraoperatively in one-third of patients [28]. As a consequence, landmarks for the identification of KNs may be helpful during sympathetic surgery.
Subpleural veins parallel to KNs (ie, superior intercostal veins) were found in 81.8% after anatomic dissection, and the thoracoscopic detection rate of these veins was significantly higher than that of KNs. These findings may be due to the better contrast of subpleural veins compared with small neural structures such as KNs. Consequently, looking for subpleural veins in the first intercostal space may enhance the detection rate of KNs intraoperatively. Moreover, KNs in combination with concomitant subpleural veins were found most frequently.
Only two reports have commented on the superior intercostal vein (sometimes called vein of Kuntz), which is a large branch draining into the azygos vein on the right side but lies lateral to the second thoracic ganglion on the left side [18, 29]. However, it has been detected in only 12% of thoracoscopies by Ramsaroop and colleagues [18]. Moreover, both articles recommended caution, because these veins can sometimes cause troublesome bleeding [18, 29].
The occurrence of vessels "close to a sympathetic nerve" has been blamed for surgical failures in 11.5% of repeat sympathectomies by Lin [7]; however, Lin did not further comment on these observations or explain the anatomy in detail. In our view, the superior intercostal veins could serve as landmarks for the identification of KNs. Other authors, however, suggested that the venous system is more variable than the arterial system and concluded that it is therefore not suitable as an orientation landmark of the T2 ganglion [30]. In this study, we found these veins parallel to KNs regularly in 81.8% after anatomic dissection. It seems rather unlikely that these veins might not be identified by thoracoscopy because they have a significant caliber (mean diameter, 2.2 mm). Moreover, if blunt dissection is performed without diathermy and clips are applied on the veins, injuries and bleeding can be easily avoided.
Interestingly, we did not find superior intercostal arteries, which Chiou and Liao [30] proposed as orientation landmarks for the T2 ganglion. In children, however, they also were not obvious [31]. Moreover, none of the numerous reports dealing with the anatomy of KNs has mentioned these arteries [12, 16, 17, 19, 23]. One may speculate that this discrepancy may be due to racial anatomic variations, because superior intercostal arteries have been described in Asians, whereas we investigated Europeans. The suitability of the superior intercostal veins serving as orientation landmarks for KNs is reinforced by the fact that KNs were found more frequently in combination with these veins than any other anatomic combination.
The major question is whether the surgical failure rate does correspond to the presence of KNs or not. Several reports had stressed the importance of KNs [4, 7–9, 12–16, 18, 19, 22, 30, 32, 33]. Two reports described successful reoperations in which KNs were divided after an initial failure of ETS [9, 33], whereas Lin [7] blamed KNs as being responsible for 18.8% of palmar recurrences in hyperhidrotic patients. In contrast, a recent report concluded that resection of KNs is inessential [27]. Although the authors did not provide detailed data, they emphasized the importance of applying one clip above and another one below the different ganglions to obtain an effective sympathetic block [27].
Clip application does not necessarily include additional treatment of accessory nerve fibers or KNs. As a consequence, one might assume that this technique should result in increased failure rates, but which has not been reported so far. None of the studies dealing with clip application, however, described the surgical technique concerning KNs in detail or provided long-term results and recurrence rates.
Our group, for example, always transects accessory fibers, and in the presence of a pronounced collateral nerve bundle, these fibers are blocked by an additional clip to enable potential reversibility of the procedure. Therefore, T2 to T4 sympathectomy and T4 sympathetic block had similar success rates [34]. By the way, we followed Lin and Wu's [27] recommendation to apply one clip above and one below the sympathetic ganglion to exclude branches of the sympathetic nerve joining with upper intercostal nerves [17].
Singh and coworkers [32] stressed the importance of the T2 ganglionectomy resulting in less clinical significance of KNs, as this procedure interrupts the sympathetic outflow to the upper limb proximal to these alternate neural pathways [32]. Palmar overdryness reported after T2 sympathectomy is possibly another indication for a more complete denervation compared with limited T4 procedures [34, 35].
The question arises, however, why an incidence of more than 60% of KNs does not cause similar failure rates, especially after limited T4 or T3 procedures. The persistence or return of sympathetic activity depends on the proportion of sympathetic fibers that pertain to or reestablish a functional pathway [32]. Moreover, central nervous structures such as the hypothalamus contribute to the regulation of a variety of neural activities [21]. This complex system, along with the wide anatomic variability of other alternate neural pathways, may explain why in selected cases a small persisting KN may not necessarily cause immediate failure as long as most of the sympathetic outflow has been successfully interrupted by ETS.
In contrast to this hypothesis, compensatory sweating, the most frequent and unwanted side effect of ETS, has been shown to be lower when interruption of afferent fibers to the anterior portion of the hypothalamus is spared by performing limited T4 procedures [7, 34, 35]. To the best of our knowledge, no data are available showing that compensatory sweating is associated or influenced by the presence of intact KNs. As a consequence, we cannot conclude that KNs do not play a clinical role, but have to emphasize that the surgical technique will influence the effect of KNs for sympathetic denervation [16, 18, 27, 32].
Moreover, interruption of aberrant neural pathways has already previously been recommended regardless of the surgical technique [19]. In addition, collateral innervation of sweat glands has been demonstrated [36, 37], which may—besides KNs with reestablished function—contribute to higher recurrence rates in the long-term. Finally, KNs will have a certain effect on the extent of denervation as long as sympathetic fibers can bypass the sympathetic chain and reach the brachial plexus directly [16, 20, 32].
In conclusion, this study explains the different prevalence of KNs between the surgical and anatomic literature. KNs are identified thoracoscopically only in a low number of patients although they are present in about 70%. The problem of visualization and recognition of KNs is primarily due to the low color contrast of these small nerve fibers. Subpleural veins in the first intercostal space parallel to KNs were found in more than 80% of specimens and were identified most frequently by thoracoscopy. Therefore, we recommend using these veins as landmarks for identification of KNs, which may allow a more complete denervation to optimize the outcome of thoracoscopic sympathectomies.
| Acknowledgments |
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