Extra-Anatomical Revascularization of the Adamkiewicz Artery Using the Internal Mammary Artery: Preliminary Anatomical Study
Article Outline
Ischemic spinal cord injury remains a major complication of both open and endovascular repairs of extensive lesions of the thoracic or thoracoabdominial aorta. Patients undergoing endovascular treatment cannot benefit from direct revascularization of the Adamkiewicz artery (AA). Primary revascularization of the intercostal artery (ICA) giving rise to the AA using the internal mammary artery (IMA) could ensure uninterrupted flow in the AA even if the origin of the feeding ICA was obstructed. The purpose of this study was to assess the anatomical feasibility of revascularization of the ICA giving rise to the AA using the IMA. Twenty-four dissections were carried out on 12 cadavers (eight men, four women) with a mean age of 76 at the time of death. Preparation consisted of intra-arterial injection of polymethylsiloxane (Rhodorsil®, Rhodia, France). For each IMA, the following parameters were determined: diameter in relation to the ICA in the paravertebral region before division, length, and level of the intercostal space in which direct anastomosis was possible. Dissection showed that the mean diameter at the end of the IMA was 1.8
mm (range 1.2-2.4). The mean diameter of the ICA in the paravertebral region was compatible with that of the IMA, i.e., 1.6
mm (range 0.9-2.5). The mean length of the IMA was 185
mm (range 165-230). The lowest intercostal space available in the paravertebral region for direct anastomosis between the IMA and ICA was the seventh space in one case, the eighth in 12, the ninth in eight, and the tenth in three. The findings of this preliminary study document the feasibility of using the IMA to revascularize the ICA in the paravertebral region. This technique could provide a means of preserving spinal cord vascularization during endovascular treatment of thoracic or thoracoabdominal aortic lesions.
Introduction
The reported risk of neurological defects due to spinal cord ischemia during open repair ranges 5-16% for thoracoabdominal aortic aneurysm1, 2 and 2.7-6.5% for isolated thoracic aortic aneurysm.3, 4 The importance of intercostal artery (ICA) reattachment in preserving vascularization of the Adamkiewicz artery (AA) has been documented.5 Although the superior dorsal artery, middle dorsal artery, and terminal cone artery contribute, the AA (arteriaradicularis magna) is the main source of spinal cord blood flow at the thoracolumbar level. Although more difficult to evaluate, the risk of spinal cord injury is also present during endovascular repair of thoracic aortic aneurysm using the techniques currently under investigation. Reported risk rates during endovascular repair have ranged 3.7-12%.6, 7, 8 By definition, use of endovascular techniques rules out direct revascularization of the AA. We speculate that primary revascularization of the ICA giving rise to the AA using the internal mammary artery (IMA) would ensure uninterrupted blood flow to the spinal cord even if the ostium of that ICA was obstructed (Fig. 1). The purpose of this study was to evaluate the anatomical feasibility of revascularization of the ICA giving rise to the AA using the IMA, to determine the length and diameter of the IMA, and to compare the diameters of the IMA and ICA in the paravertebral region.
Materials and Methods
Twenty-four anatomical dissections were carried on 12 cadavers (eight men, four women) with a mean age of 76 years at the time of death. The cadavers were preserved by the Winckler method. Preparation consisted of intra-arterial injection of colored latex. Dissections were carried out using microsurgical instrumentation and a binocular magnifying loupe. The IMA was dissected from the origin up to the superior epigastric artery. The following parameters were noted for each IMA: origin, branching, length, distal diameter, and relationship with the phrenic nerve.
For the ICA, the posterior segment was exposed between the projections of the paravertebral and middle axillary lines (Fig. 2). The posterior segment was chosen because of its accessibility since the ICA is located in the middle of the intercostal space at that level and its diameter is regular and fairly large. The parietal and intercostal perforating branches arise distally. All ICAs studied included between the fourth intercostal space and the lower edge of the twelfth rib (twelfth ICA or subcostal artery, level D12). All IMAs were mobilized and transposed into the paravertebral region to determine the feasibility of anastomosis with any of the ICAs that might give rise to the AA. The following parameters were noted for each IMA: length, level in intercostal spaces where direct anastomosis between the IMA and ICA was possible, and diameter in comparison with that of the ICA.

Fig. 2
ICAs were studied in the area between the paravertebral region (A) and middle axillary line (B). 1, dorsospinal branch; 2, lateral and inferior perforating branch.
Results
The origin of the IMA was located on the proximal part of the subscapular artery in all 24 dissections. In 22 dissections, the origin was a single trunk. In the remaining two dissections, there was a common trunk for the IMA and suprascapular artery. The second variant was observed on both sides. The mean distance between the origin of the internal mammary vein and IMA was 25
mm (range 10-30), and this arrangement was more pronounced on the right.
The phrenic nerve crossed the IMA in most cases (15 of 24 observations), and its direction was most often oblique from the outside to inside. The phrenic nerve crossed the IMA in the front in 12 cases and in the back in three cases (Fig. 3). The mean distance between the origin of the IMA and the phrenic nerve crossing point nerve was 22
mm (range 10-35).

Fig. 3
Dissection of the proximal segment of the IMA. Point of crossing between the IMA (A) and phrenic nerve (B).
A lateral costal branch was observed in six cases including one in which its diameter was equal to that of the IMA. The pericardiophrenic artery was present in most cases (n
=
21). The mean distance between the origin of the IMA and the beginning of the pericardiophrenic artery was 52
mm (range 25-65). In four cases the diameter of the IMA decreased significantly after the beginning of the pericardiophrenic artery.
The mean diameter of the distal part of the IMA was 1.8
mm (range 1.2-2.4). The mean length of the IMA was 185
mm (range 165-230). In 17 cases the IMA was longer on the left than on the right. In most cases the end of the IMA reached the rib cage at the level of the sixth intercostal space (Table I).
Table I. Level of termination of the IMA
| Level | Left | Right |
|---|---|---|
| Fifth rib | 0 | 1 |
| Fifth space | 1 | 2 |
| Sixth rib | 6 | 7 |
| Sixth space | 13 | 12 |
| Seventh rib | 3 | 2 |
| Seventh space | 1 | 0 |
| Total | 24 | 24 |
In 22 cases, the IMA bifurcated into the superior epigastric artery and musculophrenic artery. In the remaining three cases, the IMA trifurcated with an additional musculophrenic artery. Dissection of the epigastric artery down to the intersection with diaphragm (Fig. 4) resulted in a mean increase of 40
mm (range 25-60) in the length of the IMA.

Fig. 4
Dissection of the distal segment of the IMA. Dissection was extended in the direction of the epigastric artery (arrow) to the point of intersection with the diaphragm.
Exposure of the intercostal arteries between the paravertebral and middle axillary lines was easy. The artery ran in the middle part of the intercostal space and was not covered by intercostal muscle. The mean diameter of the ICA in the paravertebral region from D5 to D12 was 1.6
mm (range 0.9-2.5). The mean diameters measured at each level are listed in Figure 5. Only three ICAs had mean diameters <1
mm at the level of the paravertebral line. This finding, i.e., diameter <1
mm, involved the fourth ICA in two cases and the fifth ICA in one case. In all dissections, the diameter of the ICA was observed to increase gradually from D5 to D12.

Fig. 5
Mean diameter of the ICAs facing the paravertebral line (PVL) and middle axillary line (MAL) at the D5 and D12 levels. A progressive increase in the diameter of the ICAs was observed in all dissections.
Comparison of the anatomical features of the IMA and ICA showed that the lowest intercostal space in which direct anastomosis could be performed between the IMA after mobilization and transposition in the paravertebral region and the ICA in this territory was the seventh intercostal space in one case, the eighth in 12, the ninth in eight cases, and the tenth in three cases. In five cases, anastomosis in the eleventh intercostal space could be achieved by extending dissection of the IMA in the direction of the epigastric artery (Fig. 6).

Fig. 6
Anatomical preparation showing transposition of the mammary artery into the paravertebral region. The ICAs were also dissected. The lowest level at which direct anastomosis between the IMA and ICA was feasible was the eleventh intercostal space.
Discussion
This study demonstrates the anatomical feasibility of revascularization of the ICA giving rise to the AA using the IMA. Our findings showed that the available length of the IMA after transposition into the paravertebral region was adequate and that the diameter of the IMA was comparable to that of the ICA for microsurgical anastomosis. Recent minimally invasive techniques either by thoracoscopy9 or by video-assisted minithoracotomy10 could be used for harvesting the IMA for extra-anatomical revascularization of the AA.
This technique raises several unresolved hemodynamic issues. The main issue involves creation of competitive flow in the ICA supplying the AA. Indeed, this technique consists of making an anastomosis between the IMA and ICA downstream from the origin of the spinal artery. An animal model study will be needed to answer this question.
The first extra-anatomical revascularization of visceral arteries was proposed by Macierewicz et al.11 to enable endovascular treatment of some types of aortic aneurysm. This principle led us to evaluate the possible advantages of primary revascularization of the AA. Data from recent anatomical12, 13, 14 and angiographic15, 16, 17 studies determined that the origin of the AA was usually located between D5 and L3, with the greatest frequency being between D8 and D12. The surgical anatomy of the ICA in the posterior region of the thorax was specifically studied by Larichev in 1990.18 Findings demonstrated that the anatomical relations of the ICA at the paravertebral level were highly stable and consistent. Anatomoclinical studies designed to evaluate the feasibility of transferring a costal graft also demonstrated the feasibility of performing microsurgical anastomosis on the posterior segment of the ICA.19, 20 Our study confirms data from the literature and shows that the diameter of the posterior segments of the ICA is greater than 1
mm and that these vessels can be mobilized. These features are important for performing microsurgical anastomosis under favorable conditions.
Although surgical anatomy of the IMA has been described in several recent studies focusing on myocardial revascularization,21, 22, 23 there has been no information on transposition of the IMA into the paravertebral region or on its relationship with the ICA. Transposition requires mobilization of the IMA all the way to its origin in order to rotate the vessel backward as far as possible. Mobilization is difficult due to the presence of the proximal branches of the IMA (the lateral costal branch and pericardiophrenic branch), to the anatomy of the origin of the mammary vein, and to the intersection with the phrenic nerve. In some cases, transposition may be facilitated by the presence of a common trunk between the IMA and the suprascapular artery since this arrangement results in a posterior course of the IMA. This feature was noted in two of our dissections (8%). In a series of 100 dissections, Henriquez-Pino et al.21 noted the presence of a common trunk in 30% of cases.
The lateral costal branch noted in six of our dissections (25%) was studied by Sutherland and Desai,24 who noted the presence of this “redundant” artery in one-third of their dissections. In our dissections, the presence of the pericardiophrenic artery was observed much more consistently. Henriquez-Pino et al.21 reported the same anatomical arrangement, with the distance between the IMA and beginning of the pericardiophrenic artery being 43
±
9
mm.
Numerous anatomical studies have been carried out to evaluate the risk of paralysis of the diaphragm after mobilization of the IMA.21, 25, 26 In agreement with previously published data, our findings show that the phrenic nerve crosses the IMA in 50% of cases. The distance between the origin of the IMA and the phrenic nerve crossing point is around 20
mm (range 5-45).
To improve mobilization of the IMA, some authors27 have advised section of the internal mammary vein at the origin. In agreement, our dissection showed that the origin of the internal mammary vein is located at a mean distance of 25
mm in front of the origin of the IMA.
Measurements made in the larger series published by Henriquez-Pino et al.21 and Lachman and Satyapal22 showed that the mean length of the IMA was 180
±
6
mm and 240
±
21
mm, respectively. According to an angiographic study carried out on 80 patients,28 the distal diameter of the IMA was 2.19
±
0.24
mm. Measurement of the same diameter in a morphometric study on 62 cadavers22 gave 1.98
±
0.2
mm. Despite the differences in techniques, these measurements are comparable with those in our study. A bifurcation IMA ending was observed in 93% of cases in the series of Henriquez-Pino et al.21 and 97.5% in that of Peric et al.28
Based on comparison of our anatomical data with those in the literature12, 13, 14 and on those from our previous study,29 extra-anatomical revascularization of the AA using the proposed technique should be possible in about 60% of cases. Preoperative location of the AA is an indispensable requirement for this technique. Improvements in spinal cord arteriographic techniques17 and especially the use of recent noninvasive methods such as three-dimensional magnetic resonance angiography30 and multi-detector row computed tomography31 have opened new perspectives in this domain.
This report presents the results of an exclusively anatomical feasibility study. Further anatomosurgical research and animal studies will be necessary to develop the surgical technique for clinical application.
Conclusion
This anatomical study demonstrates the feasibility of revascularization of the ICA in the paravertebral region using the IMA. This technique could be useful for preservation of spinal cord blood supply in patients undergoing endovascular repair of thoracic or thoracoabdominal aortic lesions.
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Presented at the Sixteenth Annual Meeting of the French Language Vascular Surgery Society, Marseille, France, June 28, 2004.
PII: S0890-5096(09)00246-5
doi:10.1016/j.avsg.2009.09.001
© 2009 Annals of Vascular Surgery Inc. Published by Elsevier Inc All rights reserved.

