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Ann Thorac Surg 1995;59:163-168
© 1995 The Society of Thoracic Surgeons

Anatomic Study of the Collateral Blood Supply of the Sternum

Ramon A. de Jesus, MD, Robert D. Acland, FRCS

Division of Plastic and Reconstructive Surgery, University of Louisville, Louisville, Kentucky

Accepted for publication July 29, 1994.


    Abstract
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
A microdissection study was carried out on ten injected, cleared human sternal specimens. Three types of vessel were identified that have the potential to carry blood to the sternum after mobilization of the internal thoracic artery (ITA): (1) branches of the ITA that supply both the sternum and the pectoralis major (``sternal/perforating branches''), (2) branches of the ITA that supply both the sternum and an adjoining intercostal space (``sternal/intercostal branches''), and (3) posterior intercostal arteries that do not anastomose with an ITA branch but continue past the ITA to reach the sternum. All three types of vessel were found more frequently in the proximal than in the distal half of the sternum. For sternal/perforating and sternal/intercostal vessels to function as collaterals after ITA bypass grafting, their short common trunks of origin must remain intact. The data support the recommendation that the branches of the ITA be ligated as close as possible to the ITA itself to preserve collateral blood flow to the sternum.


    Introduction
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The increased incidence of sternal wound complications that is reported [14] after internal thoracic artery (ITA) bypass grafting is believed [5, 6] to be caused by damage to the blood supply of the sternum. Green [7] has stated that there are important collateral blood vessels lying close to the ITA that, if unharmed, can provide a continued blood supply to the sternum after mobilization of the ITA. To avoid damage to these collateral vessels, Green has recommended that when the ITA is mobilized, its branches should be divided as close to the ITA trunk as possible [7]. This recommendation also has been made by Galbut and associates [8], who presented a large series of bilateral ITA bypass procedures in which mobilization of the ITA in a painstaking, ``skeletonized'' fashion was associated with an unusually low wound complication rate. In light of these recommendations there is a need for clear and specific information on the anatomy of the collateral blood supply of the sternum. To date, such information has been lacking.

There are two possible sources of collateral supply to the sternum after mobilization of the ITA. These are the posterior intercostal arteries, which anastomose with the intercostal branches of the ITA, and the thoracoacromial arteries, which anastomose (by their branches in the pectoralis major muscles and in the overlying soft tissue) with the perforating branches of the ITA. For the sternum to receive blood from these sources, blood vessel connections must exist that would let blood pass retrogradely along the intercostal or perforating branches of the ITA, then pass antegradely along its sternal branches.

The literature contains little information on the existence of such connections. Textbook accounts [9] of the relevant branches of the ITA describe them as being of three simple types: sternal, intercostal, or perforating. Each branch type is named and described as having only one destination. Connections between the three different branch types, or branches having a common trunk and serving more than one destination, are not described. Green [7], on the basis of direct surgical observation, has described ITA branches arising from the anterior aspect of the vessel that divide to supply both the sternum and the intercostal space. These branches, if ligated close enough to the ITA to preserve their point of division, would serve as conduits for collateral flow to the sternum.

In this article we describe a microdissection study on 10 fresh, injected cadaveric specimens to determine the existence, frequency, diameter, and location of connections between the anterior intercostal, perforating, and sternal branches of the ITA. Our study shows that such connections are abundant, that they take the form of shared branch origins, and that they lie directly in harm's way in the course of ITA bypass grafting.


    Material and Methods
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Ten fresh human cadavers were studied. Their ages ranged from 68 to 93 years (mean, 81 years). Each ITA was exposed and cannulated just above the first rib. Twenty milliliters of red Microfil (Flow Tek, Inc, Boulder, CO) was injected at a pressure of approximately 200 mm Hg, and the vessels were then tied off. A 10-cm-wide specimen was removed, consisting of all tissues from the skin to the anterior mediastinum, including the full length of the sternum and the first seven costal cartilages on each side. The skin, subcutaneous tissue, and pectoralis major muscles were dissected off the anterior aspect of the specimen. The anterior mediastinal tissues and the transversus thoracis muscles were carefully dissected off the posterior aspect of the specimen. These tissues were discarded.

The specimen was placed in a bath of 2% potassium hydroxide at room temperature for 3 weeks; the bath was changed every 3 to 4 days. The specimen was then transferred to 50%, 70%, 100%, and again 100% glycerol, with 3-day intervals between transfers. This rendered the soft tissues almost transparent.

Using a Zeiss operating microscope (x4 to x25) and standard microsurgical instruments, a careful dissection was made of both internal thoracic arteries and all their branches, from the first to the sixth intercostal space. Each branch, and its branches, were followed to their destinations, and the destinations were recorded. A detailed vessel map was drawn for each specimen, and each completed dissection was photographed. Figure 1Go indicates the appearance of a typical specimen upon completion of the dissection. Vessel diameters were measured at specific points, described below, by visual comparison with a set of steel rods ranging in diameter from 0.2 mm to 2.0 mm, in 0.2-mm increments. Distances between certain critical points, described below, were measured with calipers.



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Fig. 1. . Posterior view of a typical injected, cleared sternal specimen on completion of microdissection.

 
In recording the results, we kept in mind the fact that after a midline thoracotomy, the two halves of the sternum have no vascular connection to each other. Therefore, in counting vessels each specimen was considered as consisting of two separate hemisternal specimens.


    Results
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Six types of vessels were found. Five arise from the ITA; one runs close to it. Of the six vessel types, three have the potential to act as conduits for collateral flow to the sternum; the other three do not. Figure 2Go shows the vessel types diagrammatically and shows the points at which measurements were made.



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Fig 2. . The six vessel types identified in this study. Vessel diameters ({downarrow}) and surgically important distances (< >) were measured where indicated by arrows. (ITA = internal thoracic artery.)

 
Noncollateral Vessels
The three noncollateral vessel types are the three classically described ITA branch types: sternal, intercostal, and perforating. They typically arise respectively from the medial, lateral, and anterior aspects of the ITA. Noncollateral vessels outnumber collateral vessels by approximately 5:2. Their frequency and diameter range are shown in Table 1Go.


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Table 1. . Frequency and Diameter of Noncollateral Vesselsa
 
Collateral Vessels
Two of the collateral vessel types are branches of the ITA that arise by a common trunk then divide to supply both the sternum and an adjoining area, either the adjoining intercostal space or the adjoining anterior soft tissue. We refer to these as sternal/intercostal (S/I) branches and sternal/perforating (S/P) branches. The third type of collateral vessel is a rare persistent posterior intercostal artery that reaches the sternum, bypassing the ITA without anastomosing with it. Figure 3Go shows examples of each type of collateral vessel. The frequency and diameter of collateral vessels are given in Table 2Go.



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Fig 3. . Examples of the three types of sternal collateral vessels identified in this study. The sternum is to the right, except in (B). (A, B) A sternal/perforating branch (arrow), posterior view (A), and anterior view (B). Circle indicates the perforating sub-branch, seen end-on, which passes forward and enters the pectoralis major muscle. (C, D) A sternal/intercostal branch (arrow), with the internal thoracic artery in situ (C) and retracted laterally (D). The common trunk is unusually long. (E, F) A persistent posterior intercostal artery (arrow). The internal thoracic artery is retracted laterally (E) and medially (F) to show lack of any connection between it and the persistent posterior intercostal artery.

 

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Table 2. . Frequency and Diameter of Collateral Vesselsa
 
STERNAL/INTERCOSTAL ITA BRANCHES.
An S/I branch arises from the anterior or lateral aspect of the ITA and within a short distance divides into sternal and intercostal sub-branches. These run in opposite directions. The sternal sub-branch typically divides to supply both anterior and posterior aspects of the sternum.

After mobilization of the ITA, collateral blood flow could reach the sternum by way of an S/I ITA branch (Fig 4AGo). For this to occur, the point of division of the S/I branch into its sternal and intercostal sub-branches must be protected from surgical damage. The length of the common trunk of the S/I branches ranged from 1 to 12 mm, with a mean of 4.1 mm. The distance was less than 5 mm in 67% of cases and less than 10 mm in 95% of cases.



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Fig 4. . Presumed route of collateral flow to the sternum after mobilization of the internal thoracic artery: (A) via sternal/perforating branches and (B) via sternal/intercostal branches.

 
STERNAL/PERFORATING ITA BRANCHES.
An S/P branch arises from the medial or anterior aspect of the ITA. Passing anteriorly toward the pectoralis major muscle it gives off a sub-branch to the posterior aspect of the sternum and usually another to the anterior aspect. Collateral blood flow could reach the sternum by way of an S/P ITA branch (Fig 4BGo). For this to occur the points of origin of its sternal sub-branches must be protected from surgical damage. The posterior sternal sub-branches are vulnerable. The distance between the origin of an S/P branch from the ITA and the origin of its posterior sternal sub-branch ranged from 0 to 16 mm, with a mean of 5.2 mm. The distance was less than 5 mm in 51% of instances, and less than 10 mm in 84% of instances.

The point of origin of the anterior sternal sub-branch is located more anteriorly within the thickness of the intercostal muscle and does not appear to be vulnerable to surgical damage.

Sternal/perforating branches could be damaged not only during ITA dissection, but also at wound closure by the passage of cerclage wires. The distance between the lateral edge of the sternum and the perforator component of an S/P branch ranged from 0 to 16 mm, with a mean of 5.4 mm. The distance was less than 5 mm in 44% of instances and less than 10 mm in 72% of instances.

PERSISTENT POSTERIOR INTERCOSTAL ARTERIES.
A small number of posterior intercostal arteries were found which passed all the way to the sternum without anastomosing with an ITA branch. In doing so, they passed close to the ITA and anterior to it. The proximity of a persistent posterior intercostal artery to the ITA makes it vulnerable. At the point where the vessels cross, the distance between the persistent posterior intercostal artery and the ITA ranged from 2 to 10 mm, with a mean of 4.5 mm. The distance was less than 5 mm in 59% of instances and less than 10 mm in 90% of instances.

Collective Observations Concerning Collateral Vessels and Their Distribution
The number of collateral vessels per hemisternum ranged from 3 to 12 with a mean of 5.8. The number of collateral vessels in each interspace ranged from 0 to 4 with a mean of 1.02. The number of collateral vessels varied as widely between the right and left sides of a specimen as it did between individual specimens.

The number of interspaces in each hemisternum in which there was no collateral vessel ranged from zero to four, with a mean of 1.9. In 5 of the 20 hemisternal specimens there were two adjacent interspaces that had no collateral vessel. In a further 2 specimens there were three adjacent interspaces with no collateral vessel.

The vertical distribution of the three types of collateral vessel is shown in Table 3Go. There were many fewer collateral vessels in the lower three interspaces than in the upper three.


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Table 3. . Mean Frequency of Occurrence of Each Type of Collateral Vessel in Each Intercostal Space, Per Hemisternum
 
EXTENT OF SURGICAL DAMAGE TO COLLATERAL VESSELS.
By examination of the vessel map of each specimen, determinations were made of the number of collateral vessels that would have been damaged in that specimen if the ITA had been surgically mobilized. Two surgical techniques were envisioned, the first relatively careful, the second relatively destructive. In the first technique all branches of the ITA would be ligated 5 mm from the trunk of the ITA, and all persistent posterior intercostal arteries would be spared. In the second technique all branches of the ITA would be divided 10 mm from the trunk of the ITA and all persistent posterior intercostal arteries lying less than 5 mm from the ITA trunk would be destroyed.

With the first technique 51% of all S/I branches and 67% of all S/P branches would cease to function as collateral vessels because they would be ligated beyond their point of division.

In the second technique 95% of all S/I branches and 84% of all S/P branches would cease to function as collateral vessels. In addition, 59% of persistent posterior intercostal vessels would be destroyed.

A determination also was made of the number of intercostal spaces that would be left without any collateral vessel using each technique. In this regard the effect of operation would be more serious for the posterior than for the anterior aspect of the sternum. This is because, in the case of S/P branches, the sub-branch to the posterior aspect of the sternum is prone to damage whereas the sub-branch to the anterior aspect is not.

Before the imagined operation the mean number of intercostal spaces having no collateral vessel was 1.9 per hemisternum. With the first technique, this number would rise to 2.2 on the anterior aspect and 3.6 on the posterior aspect. With the second technique, the number of interspaces having no collateral vessel would rise to 4.6 on the anterior aspect and to 5.1 on the posterior aspect.


    Comment
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Our findings show that vessels exist that have the potential to carry blood to the sternum from sources other than the ITA. These collateral vessels exist mainly in the form of ITA branches that serve two destinations. One destination is the sternum; the other is either the adjacent intercostal space or the adjacent anterior chest wall. Collateral channels also exist, less commonly, in the form of persistent posterior intercostal arteries. All three types of collateral vessel are prone to damage when the ITA is being mobilized.

Of the three types of collateral vessels that we identified only one, the S/I ITA branch, was described by Green [7]; Green's description of S/I branches was made on the basis of operative findings. Our account of these branches corresponds with Green's except that we find that they do not occur as regularly as Green states.

Arnold [10], in a study based on anteroposterior, two-dimensional arteriography, failed to identify any of the three types of collateral vessels that are readily apparent upon dissection of the cleared tissue. This attests to the limitations of two-dimensional arteriography. The radiologic shadow of the ITA would obscure, in each collateral vessel type, an essential anatomic feature. For S/I and S/P branches the essential feature is the common trunk of origin. For persistent posterior intercostal vessels the essential feature is the vessel's separateness from the ITA.

We encountered wide variation between individuals in the number of collateral vessels that were present. An individual endowed with few collateral vessels would be at greater risk of serious devascularization than an individual with many. The collateral blood supply of the lower half of the sternum appears to be especially precarious. The lower three interspaces possessed only 30% of all the observed collateral vessels. The lower two possessed only 14%.

Our anatomic findings strongly reinforce the recommendation that all ITA branches should be ligated as close as possible to the main vessel trunk to minimize damage to the collateral blood supply of the sternum.

Collateral vessels to the sternum are prone to damage not only when the ITA is being mobilized, but also when the sternal wound is being closed. The use of cerclage wires to approximate the two halves of the sternum could readily occlude sternal/perforating collateral vessels. The distance between these vessels and the sternal edge varied in our series from 0 to 16 mm. The branch lay less than 5 mm from the sternal edge in 44% of instances. The only practical recommendation that our findings support in this regard is that cerclage wires should be placed as close as possible to the edge of the sternum. Our observations do not support any particular recommendation regarding the vertical placement of wires, either high, low, or centrally in the interspace. On average, we found collateral vessels to be distributed evenly among the upper, lower, and central thirds of each interspace.

Cerclage wires also may harm the sternal circulation in another way: by interrupting the vertically running vessels of the anterior and posterior periosteal plexus. The periosteal plexi probably play an important role in sustaining the viability of the sternum after operation, particularly in those segments where the adjoining interspaces have lost their collateral vessels. Although cerclage wires have mechanical advantages, it would seem preferable in terms of sternal blood supply for a sternal closure device to go into the sternum rather than around it.


    Acknowledgments
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Facilities for this research were provided through the generosity of the Jewish Hospital Foundation. This work was carried out in the Fresh Tissue Dissection Laboratory in the Department of Anatomical Sciences and Neurobiology, University of Louisville.


    Footnotes
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
Presented at the Eleventh Annual Meeting of the American Association of Clinical Anatomists, Galveston, TX, June 14–17, 1994.

Address reprint requests to Dr Acland, University of Louisville, 324 MDR Building, Louisville, KY 40292.


    References
 Top
 Footnotes
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Culliford AT, Cunningham JN, Zeff RH, Isom OW, Teiko P, Spencer FC. Sternal and costochondral infections following open-heart surgery. J Thorac Cardiovasc Surg 1976;72: 714–25.[Abstract]
  2. Grossi EA, Culliford AT, Krieger KH, et al. A survey of 77 major infectious complications of median sternotomy: a review of 7,949 consecutive operative procedures. Ann Thorac Surg 1985;40:214–23.[Abstract]
  3. Hazelrigg SR, Wellons HA, Schneider JA, Kolm P. Wound complications after median sternotomy. J Thorac Cardiovasc Surg 1989;98:1096–9.[Abstract]
  4. Loop FD, Lytle BW, Cosgrove DM, et al. Sternal wound complications after isolated coronary artery bypass grafting: early and late mortality, morbidity, and cost of care. Ann Thorac Surg 1990;49:179–87.[Abstract]
  5. Kouchoukos NT, Wareing TH, Murphy SF, Pelate C, Marshall WC. Risks of bilateral internal mammary artery bypass grafting. Ann Thorac Surg 1990;49:210–9.[Abstract]
  6. Carrier M, Gregoire J, Trone F, Cartier R, Leclerc Y, Pelletier L. Effect of internal mammary artery dissection on sternal vascularization. Ann Thorac Surg 1992;53:115–9.[Abstract]
  7. Green GE. Sternotomy incision, mobilization, and routing of ITA grafts. In: Green GE, Singh RN, and Sosa JA (eds.). Surgical revascularization of the heart: the internal thoracic arteries. New York: Igaku-Shoin Medical Publisher, 1991:119–27.
  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. Williams PL, Warwick R, Dyson M, Bannister LH, eds. Gray's anatomy, 37th ed. New York: Churchill Livingstone, 1989:754–5.
  10. Arnold M. The surgical anatomy of sternal blood supply. J Thorac Cardiovasc Surg 1972;64:596–610.[Medline]



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M. Sousa Uva, E. Braunberger, M. Fisher, Y. Fromes, P. H. Deleuze, J. A. Celestin, and O. M. Bical
Does bilateral internal thoracic artery grafting increase surgical risk in diabetic patients?
Ann. Thorac. Surg., December 1, 1998; 66(6): 2051 - 2055.
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S. Pagni, E. J. Salloum, G. R. Tobin, D. J. VanHimbergen, and P. A. Spence
Serious wound infections after minimally invasive coronary bypass procedures
Ann. Thorac. Surg., July 1, 1998; 66(1): 92 - 94.
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A. El Gamel, N. A. Yonan, R. Hassan, M. T. Jones, C. S. Campbell, A. K. Deiraniya, and R. A. M. Lawson
Treatment of Mediastinitis: Early Modified Robicsek Closure and Pectoralis Major Advancement Flaps
Ann. Thorac. Surg., January 1, 1998; 65(1): 41 - 46.
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J. A. Henriquez-Pino, W. J. Gomes, J. C. Prates, and E. Buffolo
Surgical Anatomy of the Internal Thoracic Artery
Ann. Thorac. Surg., October 1, 1997; 64(4): 1041 - 1045.
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I. A. Nicholson and H. S. Paterson
Modified T Graft for Triple-Vessel Disease
Ann. Thorac. Surg., August 1, 1997; 64(2): 451 - 453.
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S. C. Hendrickson, K. E. Koger, C. J. Morea, R. L. Aponte, P. K. Smith, and L. S. Levin
Sternal Plating for the Treatment of Sternal Nonunion
Ann. Thorac. Surg., August 1, 1996; 62(2): 512 - 518.
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