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Ann Thorac Surg 2006;81:2155-2159
© 2006 The Society of Thoracic Surgeons

Original article: Cardiovascular

Blood Supply of the Sternum and Its Importance in Internal Thoracic Artery Harvesting

Denis Berdajs, MD * , Gregor Zünd, MD, Marko I. Turina, MD, Michele Genoni, MD

Department of Cardiovascular Surgery, University Hospital Züric, Zürich, Switzerland

Accepted for publication January 4, 2006.

* Address correspondence to Dr Berdajs, Department of Cardiovascular Surgery, University Hospital Zürich, Rämistrasse 100, 8091 Zürich, Switzerland. (Email: denis.berdajs{at}usz.ch).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: The internal thoracic artery (ITA) is the conduit of choice in coronary bypass grafting, due to the excellent long-term results achieved using it. However, increased incidence of sternal infections after pedicled ITA harvesting has revived interest in the morphology of sternal blood supply. Our aim was to discuss the topography of the sternal branches with emphasis on internal thoracic artery harvesting.

METHODS: This study was conducted on 50 fresh specimens of the anterior thorax wall. Radio-opaque material was injected and angiograms of the ITA were performed. Subsequently, the specimens were preserved and a dry dissection of each ITA and its branches was carried out.

RESULTS: In dry dissected specimens, four types of vessels were identified that have the potential to carry blood to the sternum after harvesting the ITA. In the first group, the artery to the sternum also supplies the intercostal space. In the second morphologic variant, the sternal branch gives off the perforating and anterior intercostal arteries. In the third group, we classified the common branch of the sternal and perforating arteries. In the fourth group, the sternal artery originated from the ITA as an independent branch.

CONCLUSIONS: For sternal-intercostal, perforating-intercostal, and sternal-perforating branches to function as collaterals after ITA harvesting, the common trunk of origin must remain intact. Based on morphologic data, we recommend ligating the common trunk as close as possible to the ITA; in this way, collateral blood flow to the sternum remains intact.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The increased incidence of sternal complications after internal thoracic artery (ITA) grafting [1, 2] is believed to be due to damaged blood supply to the sternum [3, 4]. It has been proven that collaterals of the ITA do exist, and that can provide sternal blood supply after mobilization of the ITA [5]. Based on this initial morphologic data it has been suggested that, in order to preserve collateral blood supply after ITA mobilization, surgeons should divide the branches as close as possible to the ITA [6, 7].

The wisdom behind this suggestion was proven by Galbut and colleagues [8] who reported a large series of bilateral ITA grafting in skeletonized fashion. When compared with pedicled grafts, there was a lower incidence of sternal wound complications. More recently, Cohen and colleagues [9] compared the blood supply of the sternum after skeletonized versus pedicled harvesting of the ITA by means of single photon emission computed tomographic scanning. Mobilization of the ITA in a pedicled fashion was associated with a significant reduction in perfusion versus that observed with native or skeletonized ITA.

Theoretically, there are two possible sources of collateral blood supply after ITA harvesting: the anterior intercostal branches which anastomose to the posterior intercostal arteries and the perforating branches, which are connected to branches of the lateral thoracic artery. Recent morphologic literature contains little information regarding the topography of the sternal collaterals of the ITA. The sternal, perforating, and anterior intercostal branches are mentioned as terminal arteries, without collaterals to other vascular systems [10]. In light of the mentioned clinical and morphologic facts, there is a need for a detailed description of the blood supply to the sternum.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
This study was carried out on 50 human cadavers (37 males and 13 females) with ages varying from 8 to 75 years, obtained from cadavers purposed for scientific investigations at the Department of Anatomy, Embryology, and Histology, Semmelweis Medical School, Budapest, Hungary. The study was approved by the local Ethical Committee of the Semmelweis University Medical School.

The anterior sternocostal wall, containing the subclavian and internal thoracic arteries, was removed during routine autopsy. The left and right ITA arteries were cannulated separately and contrast material was injected into both arteries. For radio-opaque material, we used a 70% density barium sulfate suspension. Subsequently, angiograms were taken on Structurix D2 plates (Gevaert, Antwerp, BE) from 100 cm, with exposure time adjusted to 3.6 mAS and kV set at 50. The runoff of the artery and the pattern of the branches were determined by selective angiograms. The specimens were placed in 4% formaldehyde solution for 3 weeks followed by a bath consisting of 25% propyl alcohol, 20% propylene glycol, and 5% benzalkonium chloride. After the preservation procedure, dry dissections of the ITA and their branches were performed. The ITA was dissected from its origin up to its branch termination. On the dry dissected specimens, we were focusing on the morphology of the sternal arteries and their topographic relationships to the perforating and anterior intercostal arteries.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
The left and right ITA were present in all specimen studied. We noted that the sternal branches are the main source of sternal blood supply. A total of 666 branches were found to provide blood supply to the sternum. Sternal branches primarily were located in the intercostal spaces, a phenomenon which was especially evident among children (Fig 1A). This intercostal position also was present in the adult specimens (Fig 1B). The sternal branches were arranged in arcade formations. These arcades, in most cases, existed as an anastomosis between two sternal branches or, in some rare cases, as a formation of one to three sternal arteries (Fig 2). However, not only the sternal but also the perforating branches appeared to contribute to sternal blood supply. These branches, after their initial runoff, provided small arteries to the sternum. These arteries, which also demonstrated an arcade-like arrangement, were positioned at the superficial sternal level and were directly connected to the sternal branches (Fig 3).


Figure 1
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  		Fig 1. Angiograms of the infant and adult internal thoracic arteries. In the juvenile sternums (A), the position of the ossification zones is well identified. Note the blood supply of this area is carried out by the sternal branches. In the adult specimens (B), the presence of the ossification zones was not as pronounced; however, the phenomenon of the segmental arrangement of the sternal branches remains unchanged. (1 = manubrium of sternum; 2 = body of the sternum; 3 = ossification zone; 4 = internal thoracic artery; 5 = sternal branches; 6 = anterior intercostal branch; 7 = musculophrenic branch; 8 = superior epigastric artery; 9 = xyphoid branch.)

 

Figure 2
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  		Fig 2. Schematic drawings of the sternal branches, representing the arcade pattern of the sternal blood supply. In most cases the intercostal arcade is an anastomosis of two sternal arteries (A), or a formation of one (B) or even of three sternal arteries (C). (1 = manubrium of sternum; 2 = body of the sternum; 3 = internal thoracic artery; 4 = sternal branches.)

 

Figure 3
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  		Fig 3. Morphologic variants of the sternal blood supply. Note the perforating branches contribute to the sternal blood supply. In the sternocostal branch (A) both the sternal and the perforating artery directly connected to the anterior intercostal branch. After harvesting, the collateral blood flow reaches the sternum by the way of the anterior intercostal artery and supplies the sternal and perforating branches. In the sternocostal branch (B) the perforating and anterior intercostal artery arises from the common artery. In this case the collateral blood flow reaches the anterior aspect of the sternum by the way of the anterior intercostal artery. Sternal-perforating branch (C) is not connected to the anterior intercostal artery. The retrograde blood flow reaches the sternum by the sternal and perforating branches. Namely the perforating branches are connected to the lateral thoracic artery. In sternal branches (D) all the arteries arise as separate arteries. Theoretically, there are no collateral pathways which may contribute to the sternal blood supply. (1 = cross section of the sternum; 2 = internal thoracic artery; 3 = sternal branch; 4 = perforating branch; 5 = anterior intercostal branch; 6 = pectoralis major; 7 = intercostal muscles.)

 
According to the topographic relationship between the sternal, perforating, and anterior intercostals arteries, three main types of sternal collaterals were identified. We refer to these variants as the sternocostal branches, perforating-costal branches, sterno-perforating branches, and sternal branches. The frequency of each morphologic variant is given in Table 1.


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  		Table 1. Frequency of the Sternal Collaterals
 
Sternocostal Branches
In this case all three branches arise from the common artery (Fig 3A) referred to as the sternocostal branch. The main stem branches off from the medial aspect of the internal thoracic artery. Passing laterally toward the sternal edge, the artery gives off the sternal, perforating, and anterior intercostal branches. The sternum is supplied both by the sternal and perforating branches.

After mobilization of the internal thoracic artery, the collateral blood supply may reach the sternum by means of the anterior intercostal artery. To preserve this function, the division point of the sternocostal branch must be protected from surgical manipulation.

Perforating-Costal Branch
From the perforating-costal branch arise the perforating and the anterior intercostal arteries. The sternal branch is an independent artery, from the medial aspect of the internal thoracic artery (Fig 3B). The perforating-costal branch arises occasionally from the lateral aspect of the internal thoracic artery after the short run of the artery branches off into the perforating and anterior intercostal arteries. In this case, the collateral blood supply may reach the sternum by way of the anterior intercostal artery. For this to occur, the branching point of the perforating-costal artery must remain intact during surgical harvesting.

Sterno-Perforating Branch
In this case, the anterior intercostal artery arises as an independent branch (Fig 3C) from the IMA. The sterno-perforating branch arises from the medial aspect of the internal thoracic artery. After a short run, the artery branches off into the perforating and sternal branches. Theoretically, the collateral blood supply may reach the sternum through the perforating artery; it is anatomic evidence that the perforating branches are connected to the branches of the lateral thoracic artery. To preserve these functions, the branching point should remain intact during surgical manipulations.

Sternal Branches
In this group, we classified all variants where all three branches arise as separate independent branches from the internal thoracic artery (Fig 3D). In this case only the perforating branch may contribute to the collateral blood supply, by way of the lateral thoracic artery branches.

The numbers and distribution of the branches in the intercostal space are shown in Table 2. Statistical analysis of the data revealed a significant difference in the number of branches between the three most superior intercostal spaces and the inferior three intercostal spaces (p < 0.05). There was no significant difference between the number of branches arising from the left and right ITA within individual intercostal spaces (p > 0.05). The mean number of branches in the first intercostal space was 1.68 on the right and 1.65 on the left. The mean number of arteries in the second intercostal space was approximately identical to the first intercostal space; on the left 1.68 and on the right 1.66 (p = 0.5). A slight decrease in the number of branches versus the first and second intercostal spaces was observed in the third intercostal space (p = 0.049); we identified 1.42 branches on the left and 1.40 on the right. An explicit reduction in the number of branches was observed in the inferior half of the sternum. In the fourth intercostal space we found, on average, 1.0 branches on the left and 0.9 branches on the right side (p < 0.05); in the fifth, an average of 0.9 branches were on the left and 0.7 branches on the right; in the sixth intercostal space, 0.49 branches were on the left and 0.44 branches on the right.


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  		Table 2. Number of the Branches in the Corresponding Intercostal Space of the Left or Right Interal Thoracic Artery
 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
Based upon our morphologic data, we can state that vessels exist that have the potential to carry blood supply to the sternum after ITA mobilization. These arteries are branches of the ITA and are directly connected to the vascular system of the intercostal arteries or to the lateral thoracic artery. Main sources of sternal blood supply are sternal branches that arise as independent arteries or as conjoined branches from the perforating and anterior intercostal arteries. According to their morphologic relationships, four variants of sternal collateral blood supply were found.

Of the four variants described herein, the sternocostal and sterno-perforating branches, as well as branches that are analogous to our sternal formations, were mentioned by de Jesus and Acland [11], whose description was based upon an examination of 10 anatomic specimens. The sternal arteries were investigated as possible anastomoses to other vascular systems; however, a detailed description of blood supply to the sternum was not provided. We noted that the effective end branch, which provides the sternal blood supply, creates a vascular plexus. These vascular structures were found both at the superficial and deep sternal levels. At the deep level are direct continuations of the sternal branches. At the superficial sternal level, a plexus was identified between the superficial and deep intercostal muscles; at this level, the perforating branches contribute to create a sternal vascular plexus. Furthermore, by means of roentgenography, the position of these arcades was identified. The position of the vascular arcades corresponds to the ossification zones of the sternum. This especially was prominent in juvenile sternums. However, the segmental arrangement of the vascular arcades in the intercostal spaces also was present in adults. In our report, the sternal collaterals were evaluated as connections between the sternal, perforating, and anterior intercostal branches.

We observed wide variations between individuals in the number and position of collaterals. It seems clear that patients with sternums containing more collaterals are at less risk of sternal complications than individuals with fewer. It also seems that the regional distribution of the collaterals may influence the nature of complications. Our investigation revealed that most ITA branches are found at the level of the first three intercostal spaces (Table 1). Similar to results found in the literature [11, 12], we found significantly (p < 0.05) fewer common trunks located within the inferior part of the sternum. In fact, the lower three intercostal spaces comprise only 30% of all observed collaterals. This poorer vascularization of the inferior part of the sternum likely contributes to the increased incidence of distal sternotomy wound infections after ITA mobilization.

Our morphologic data strongly reinforce previous suggestions [11, 12] to ligate the ITA branches as close as possible to the main vessel trunk, in order to minimize collateral damage to the sternum. Compared with the literature, in which investigations on blood supply primarily have been limited to dry dissected specimens, we combined data received by angiograms and dry dissections. In this way, we were able to locate the position of the terminals of the sternal branches.

The sternal collateral vessels are prone to damage not only when the ITA is harvested, but also when the sternal wound is being closed. If sternal wires are placed lateral to the sternal edge in the intercostal spaces, the sternal and perforating branches may be occluded. Furthermore, sternal wires may harm sternal circulation by interrupting the superficial and deep arcades. These arcades, which are functional terminals of the sternal and perforating arteries, play a significant role in sustaining tissue viability after the operation.

Our only practical recommendation in this regard is that the sternal cerclage should be positioned as close as possible to the sternal edge. Furthermore, because of the intercostal position of the sternal arcades, we strongly recommend positioning the sternal wires in front of the sternocostal joint. During our examinations of this specific anatomic area, no sternal vessels were detected.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This work was carried out in the Laboratory of Clinical Anatomy, at the Department of Anatomy, Embryology, and Histology, Semmelweis Medical School, Budapest Hungary. The dry dissected specimens belong to the Laboratory of Clinical Anatomy.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Grossi EA, Esposito R, Harris LJ, et al. Sternal wound infections and use of internal mammary artery grafts J Thorac Cardiovasc Surg 1991;102:342-346.[Abstract]
  2. Ridderstolpe L, Gill H, Granfeldt H, Ahlfeldt H, Rutberg H. Superficial and deep sternal wound complicationsincidence, risk factors and mortality. Eur J Cardiothorac Surg 2001;20:1168-1175.[Abstract/Free Full Text]
  3. Lorberboym M, Medalion B, Bder O, et al. 99mTc-MDP bone SPECT for the evaluation of sternal ischaemia following internal mammary artery dissection Nucl Med Commun 2002;23:47-52.[Medline]
  4. Carrier M, Gregoire J, Tronc F, Cartier R, Leclerc Y, Pelletier LC. Effect of internal mammary artery dissection on sternal vascularization Ann Thorac Surg 1992;53:115-119.[Abstract]
  5. Green GE. Sternotomy incision, mobilization, and routing of ITA graftsIn: Green GE, Singh RN, Sosa JA, editors. Surgical revascularization of the heart. the internal thoracic arteries. New York, NY: Igaku-Shoin Medical; 1991. pp. 119-127.
  6. Athanasiou T, Crossman MC, Asimakopoulos G, et al. Should the internal thoracic artery be skeletonized? Ann Thorac Surg 2004;77:2238-2246.[Abstract/Free Full Text]
  7. Calafiore AM, Vitolla G, Iaco AL, et al. Bilateral internal mammary artery graftingmidterm results of pedicled versus skeletonized conduits. Ann Thorac Surg 1999;67:1637-1642.[Abstract/Free Full Text]
  8. Galbut DL, Traad EA, Dorman MJ, et al. Seventeen-year experience with bilateral internal mammary artery grafts Ann Thorac Surg 1990;49:195-201.[Abstract]
  9. Cohen AJ, Lockman J, Lorberboym M, et al. Assessment of sternal vascularity with single photon emission computed tomography after harvesting of the internal thoracic artery J Thorac Cardiovasc Surg 1999;118:496-502.[Abstract/Free Full Text]
  10. Luzsa Gy. X-ray anatomy of the vascular system. Philadelphia, PA: Lippincott; 1974.
  11. de Jesus RA, Acland RD. Anatomic study of the collateral blood supply of the sternum Ann Thorac Surg 1995;59:163-168.[Abstract/Free Full Text]
  12. Pietrasik K, Bakon L, Wojda UG, Dobosz P, Kolesnik A. Clinical anatomy of the internal thoracic artery branches Clin Anat 1999;12:307-314.[Medline]



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