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Ann Thorac Surg 1998;65:1660-1665
© 1998 The Society of Thoracic Surgeons

Original articles: general thoracic

Biomechanical Study of Sternal Closure Using Rigid Fixation Techniques in Human Cadavers

Wayne Ozaki, MDa, Steven R. Buchman, MDa, Mark D. Iannettoni, MDb, Elizabeth P. Frankenburg, BSc

a Section of Plastic and Reconstructive Surgery, University of Michigan Medical Center, Ann Arbor, Michigan, USA
b Section of Cardiothoracic Surgery, Department of Surgery, University of Michigan Medical Center, Ann Arbor, Michigan, USA
c Orthopedic Research Laboratory, University of Michigan Medical Center, Ann Arbor, Michigan, USA

Accepted for publication January 30, 1998.

Address reprint requests to Dr Buchman, Section of Plastic and Reconstructive Surgery, University of Michigan Medical Center, F7859 Mott Hospital, 1500 E Medical Center Dr, Ann Arbor, MI 48109-8063


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Background. We believe rigid plate fixation may be superior to wire fixation in sternal closure, as rigid fixation used in the craniofacial skeleton has shown greater stability, lower postoperative pain, and accelerated bone healing. We hypothesize that sterna fixed with titanium plates are more stable mechanically than sterna fixed with wires.

Methods. The sterna from human cadavers were used in this two-phased study. Phase I compared wires to four-hole titanium straight plates. Phase II compared wires to four-hole titanium custom H plates. The sterna were tested biomechanically using all fixation methods.

Results. Phase I showed no statistically significant difference in the stiffness or lateral displacement between the wired and straight plated sterna. Phase II showed a statistically significant greater stiffness (p < 0.05) and less lateral displacement (p < 0.05) in the custom plated sterna over the wired sterna.

Conclusions. Our results showed that custom titanium H plates were superior to wire fixation. Furthermore, our results established the importance of plate configuration in sternal fixation. Our study may have beneficial clinical implications, as decreased motion at the sternotomy site could mean less postoperative pain, a decreased incidence of infection, and accelerated bone healing.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 Acknowledgments
 References
 
Stainless steel cerclage wires are currently the standard method of median sternotomy closure in cardiothoracic surgery. Sternal wire fixation was first used to close a median sternotomy by Milton in 1897 [1] and was later popularized by Julian and colleagues in 1957 [2]. At the time, wire fixation techniques were inexpensive, rapidly performed, and relatively safe, and therefore, seemed to be the most effective method of sternotomy closure. In fact, previous studies have shown the efficacy and even the superiority of sternal wiring over other nonrigid methods of median sternotomy closure [3, 4]. Sternal wire fixation, despite its widespread use, was still associated with known morbidity and even occasional cases of mortality [5, 6]. The potential complications of sternal wire fixation included infection, wound dehiscence, mediastinitis, and sternal nonunion. In addition, increased motion at the sternotomy site can worsen a patient’s postoperative sternal pain, which may lead to atelectasis and pneumonia secondary to a decreased inspiratory effort. In an attempt to reduce the risk of these complications, clinicians and researchers continue to search for improved closure techniques.

Similar to the practice of cardiothoracic surgeons, who currently use wires to close sternal osteotomies, historically, craniomaxillofacial and orthopedic surgeons have also used wires for bone fixation. Morbidity and complications associated with wire fixation in the craniofacial and axial skeleton were similar to those found by cardiothoracic surgeons in sternotomy closures. These complications included infection, separation, instability, motion, nonunion, and delayed healing. To reduce these complications, researchers developed rigid fixation techniques that were able to decrease motion at the osteotomy or fracture site, lower postoperative pain, and improve the rate of primary bone healing. Indeed, since the introduction of rigid fixation techniques with titanium plates and screws, the bone healing complication rates have been significantly reduced in craniomaxillofacial and orthopedic surgery [7–10]. These specialties have been able to reduce hospitalization days and have seen their patients benefit from an earlier return to normal functioning [8, 11]. In fact, the overwhelming benefits of rigid fixation has led to the near-complete replacement of wire fixation in orthopedic, craniomaxillofacial, otolaryngologic, oral, and most recently in neurologic surgery.

Extending the technological advances of rigid plate fixation to sternal osteotomy closure seems to be the next logical step for the use of rigid fixation and a reasonable method to potentially reduce sternal closure complications. Sternal plates have been used anecdotally in secondary sternal reconstruction [12, 13]. Our belief is that the sound principles of rigid fixation, used in craniomaxillofacial, orthopedic, and other surgical specialties, can be applied to cardiothoracic operations with potentially equal success. To realize these improvements, modifications and adaptations of the currently used plating systems will be required to take full advantage of the benefits of rigid fixation techniques. Our hypothesis is that rigid sternal fixation with titanium plates will display greater stiffness, less lateral motion, and have fewer failures than sterna fixed with stainless steel cerclage wires. Our specific aim is to develop a rigid sternal plate with the appropriate design refinements, which will be able to withstand biomechanical forces that simulate physiologic conditions. To test directly our hypothesis, a rigorous biomechanical analysis will be performed, which compares our rigid sternal plate fixation system to conventional stainless steel wire fixation in human cadaver sterna. Our hope is that rigid fixation of the sterna will allow cardiothoracic surgeons to achieve faster primary bone healing, lower postoperative pain, and an earlier return to normal functioning, thereby reducing the risks of sternal complications.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 Acknowledgments
 References
 
The sterna and surrounding ribs from fresh human cadavers were used in this two-phased study. The first phase tested 10 human cadaver sterna and the second phase tested 11 human cadaver sterna. Phase I compared biomechanically the fixation strength of No. 5 stainless steel cerclage wires (Ethicon, Inc, Somerville, NJ) to four-hole, titanium straight plates (KLS-Martin L.P., Jacksonville, FL) (Fig 1A). Phase II, compared biomechanically the fixation strength of No. 5 stainless steel cerclage wires to customized four-hole, titanium H plates designed by us and manufactured by KLS-Martin L.P. (Fig 1B).



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  		Fig 1. (A) 2.3-mm, four-hole titanium alloy straight plate (KLS-Martin L.P., Jacksonville, FL). (B) Customized 2.3-mm, four-hole titanium alloy H (KLS-Martin L.P., Jacksonville, FL).

 
All sterna, manubria, and surrounding ribs (two through six) were obtained en bloc from fresh human cadaver specimens. The mean age of the cadavers was 79 years (range, 45 to 91 years). Of the 18 cadavers used in this study 11 were female and 7 were male. The sterna and ribs were surgically prepared by cutting the ribs to a length of approximately 10 cm and then drilling the ends with Kirschner pins. The ribs and sterna were subsequently "potted." Potting the sterna entailed placing the rib ends into rectangular aluminum molds, then filling the molds with chemically cured polymethyl methacrylate to a level that was 1 cm lateral to the internal mammary arteries. After potting, all specimens underwent median sternotomies using a reciprocating saw. Each of 10 sterna used in phase I was fixed using six, No. 5 stainless steel wires. The wires were placed through the manubrium and circumferentially around the sternum in the same sternal closure technique used clinically by one of the coauthors. The potted and wired sterna were then mechanically tested using the uniaxial servohydraulic testing machine (MTS model 810, Minneapolis, MN) (Fig 2). Each test consisted of repetitive loading for 10 ten-second cycles using a 22.5-kg load. A 22.5-kg load was used to "stress" the fixation with forces that were greater than those typically achieved during normal breathing. Cyclic loading was performed in an attempt to reproduce the normal breathing motion. Maximum load, sternal displacement, load curves, and displacement curves were acquired from a clip gauge and processed through an analog-to-digital converter. Stiffness measurements were calculated from the average slope of the load versus displacement curves. Stiffness data for each cycle were recorded and analyzed. In addition, a strain gauge was used to measure lateral sternal displacement across the median sternotomy. Once tested, the wires were removed and each sternum was plated with three four-hole titanium alloy plates (KLS-Martin L.P.). Each plate was approximately 22 mm long and 1.5 mm thick. All plates were secured with four titanium alloy screws that were 10 to 12 mm in length and 2.3 mm in diameter. The sternal edges were held together using manual pressure as the plates were applied. The drill holes were made using a power drill and a 1.5-mm drill bit. Cold irrigation was used to prevent overheating of the bone during the drilling process. Each screw was placed with a manual screw driver and tightened using gentle finger pressure. One plate was placed across the manubrium and two plates were placed across the sternum. Each sternal plate was placed approximately one-third the distance from the sternal end. The same mechanical testing that was performed on each of the wired sterna was repeated on the plated sterna.



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  		Fig 2. Potted sternum undergoing compression by the uniaxial servohydraulic testing machine (MTS model 810, Minneapolis, MN). The strain gauge is beneath the sternum.

 
Upon completion of phase I, study design changes were made before beginning phase II. In phase I, three of the sterna sustained rib fractures. To reduce the risk of this occurring in phase II, the sterna were potted closer to the lateral sternal border at the level of the internal mammary arteries. All damaged sterna from phase I were discarded. Phase II of this study tested 11 sterna (8 new sterna and 3 undamaged sterna from phase I). These 11 sterna were fixed with No. 5 stainless steel wires and biomechanically tested by the same technique used in phase I. The stiffness and displacement data obtained from the three retested wire-fixed sterna in phase II were nearly identical to that found in phase I. This enabled us to include these three reused sterna in phase II of our study. Once tested, the wires were removed from each of the sterna in phase II and the sterna were plated subsequently using custom four-hole titanium alloy H plates (18 mm long, 10 mm wide, and 1.5 mm thick). The plated sterna were again biomechanically tested by the same technique used in phase I.

Statistical analysis
The statistical analysis used in this study was a univariate paired t test. Stiffness was calculated as the average slope of the stress/strain curve measured as a numeric value/100 mm ± standard deviation. Lateral displacement was measured in millimeters ± standard deviation as the maximum lateral displacement during an entire compression cycle. Failures were determined by the criteria set forth in the methods section. Three sterna sustained rib fractures that were unrelated to the integrity of the sternal fixation. These sterna were removed from the study and were not counted as failures toward either group. A p value of less than 0.05 was considered statistically significant in this study.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 Acknowledgments
 References
 
Ten sterna were tested in phase I, which compared biomechanically wire fixation to straight plate fixation. Phase I testing was complicated by rib fractures in 3 of the 10 sterna, necessitating their removal from the study. Of the seven remaining sterna, there was one wired sternum failure and there were three plated sterna failures. Complete failure was defined as wire breakage or complete wire pull-through, plate fracture, screw pull-out, or a sternal displacement greater than 1 in. Our results showed that the wired sterna in phase I trended toward a greater stiffness (3.61 ± 3.6) over the plated sterna (3.37 ± 3.0). The wired sterna (3.41 ± 2.5) also trended toward a lower sternal separation over the plated sterna (4.66 ± 4.8). Neither of these differences, however, proved to be statistically significant (p = 0.68 and p = 0.48, respectively) (Fig 3).



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  		Fig 3. Phase I: four-hole straight plate versus wire fixation. Lateral displacement is measured in millimeters, stiffness is measured in millimeter-1, and failures are calculated from a total of seven plates.

 
After phase I, a thorough inspection of the plated sterna showed that the screw holes closest to the midline sternotomy tended to break through the adjacent bone (Figs 4 and 5). The fractures in this bone caused the screws to lose a significant amount of their bone purchase, which weakened the entire fixation and led to eventual failure of the plated sterna. These observations led us to believe that fixation screws placed too close to the midline sternotomy would increase the risk for failure. We believed that a new plate design, which could assure rigid fixation in adequate bone stock, would also prove to be stiffer and exhibit lower lateral motion at the sternotomy site than wired sterna. The plates were redesigned to an H configuration from a straight configuration, which placed the two screw holes on each side of the midline sternotomy in a superior and inferior position instead of a side-to-side position. This design capitalized on the principle that screws placed into the stronger central bone would be better secured and less likely to fail than screws placed into the weaker peripheral bone (Fig 6). Phase II testing resulted in no rib fractures. The decreased rate of rib fractures most likely occurred because the sterna in phase II were potted closer to the sternal border. Phase II results showed one wired sternal failure, but no custom plated sternal failures. The plated sterna (5.88 ± 3.4) had an overall greater stiffness than the wired sterna (5.02 ± 2.6) (Fig 7). In addition, the plated sterna (1.48 ± 1.5) had less lateral displacement than the wired sterna (2.46 ± 2.7). We found both these differences to be statistically significant (p < 0.05).



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  		Fig 4. Failed four-hole titanium alloy straight plate sternal testing. Wide sternal separation seen.

 


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  		Fig 5. Failed wired sternal testing. Wires seem to be pulling through the sternum.

 


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  		Fig 6. Successful custom four-holed H plate sternal testing.

 


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  		Fig 7. Phase II: four-hole straight plate versus wire fixation. Lateral displacement is measured in millimeters, stiffness is measured in millimeters-1, and failures are calculated from a total of eleven plates.

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
Acknowledgments
 References
 
For many years stainless steel cerclage wires have been the most commonly used approach for median sternotomy closure in cardiothoracic operations. The superiority of wire fixation has been confirmed by several investigators [3, 4] who found that the biomechanical stability of sternal closures with stainless steel wires exceeded the stability of many other nonrigid fixation methods, including merceline ribbons and steel bands. Despite their widespread use, routine sternal closure with stainless steel cerclage wires still carries a 0.5% to 4% wound healing complication rate [5, 6]. The sequelae of sternal wire failure can contribute to an increased rate of infection, wound dehiscence, mediastinitis, and sternal nonunion. Failure of wire fixation can also lead to sternal separation and increase motion at the sternotomy site, which could increase sternal pain. Potentially this can reduce a patient’s respiratory effort and increase the risk of atelectasis and pneumonia. Furthermore, there is a significant mortality associated with sternal complications. Cheung [14] in 1985 and Milano [15] in 1995 and their colleagues found an increase in mortality in patients who developed infected sterna. Although wire fixation of median sternotomies is currently the most widely accepted method of sternal closure, the pain and morbidity associated with nonrigid wire fixation have prompted clinicians and researchers to continue to search for improved closure techniques.

Rigid fixation techniques are currently widely used in the fields of craniomaxillofacial and orthopedic surgery. The advantages of rigid fixation techniques over wire fixation techniques in these specialties include accelerated primary bone healing, lower incidence of wound infection and dehiscence, and an earlier return to normal function [7–11]. The success of rigid fixation in fracture repair and osteotomy stabilization led us to believe that rigid fixation technology could be extended to the fixation of median sternotomies. Our failure to demonstrate an improvement of the standard titanium straight plates over wire fixation techniques in phase I of our study, however, convinced us that achieving rigid fixation of the sterna was more difficult than suspected initially. In fact, we believe that our inability to achieve rigid fixation in phase I precluded us from attaining the maximum benefits from plate and screw fixation.

The plates used in phase I were linear and did not optimize rigid fixation techniques. Rigid bony fixation not only depends on the use of rigid plates and screws, but is also influenced by the bone under the plates into which the screws are being placed. To achieve rigid fixation, the holes must be properly drilled with adequate irrigation, the appropriately sized screws must be used, and the screws must be placed into the thickest and densest possible bone. A careful inspection of our failed plated sterna demonstrated that the screws in phase I were not being placed into the best possible bone. Poorly placed titanium screws into the sternal bone edges caused small bone fractures to develop in the areas closest to the midline sternotomy. These bony fractures caused the screws to lose their purchase, which led to complete plate failure. The plate fixation failures convinced us of the need for a plate design modification, which placed the screw holes further away from the bone edges. By redesigning the rigid titanium plates, we were able to take advantage of the unique characteristics of the sternal osteotomy site. The H plate configuration placed the screw holes in an inferior and superior position instead of a side-to-side position, which achieved our goal of rigid fixation by placing the screw holes further away from the sternal edge. The H configuration significantly reduced bone breakage and prevented plate fixation failures. In phase II of our study, the screws were definitely secured into better bone stock and clinically seemed to have greater bone purchase. After phase II of our study, the expected results were realized and the plated sterna had a statistically significant greater sternal stiffness, less sternal motion, and fewer failures than the wired sterna. The success of phase II confirmed our belief that rigid titanium plate fixation was important for sternal stability and that rigid fixation could only be achieved through proper plate design.

Rigid fixation improves sternal stability over wire fixation and it may also be a safer sternal closure method. Cerclage wiring can potentially disrupt the sternal blood supply during their placement either around or through the sternum. The blood vessels at risk for compression or damage include the internal mammary arteries, perforating branches of the internal mammary arteries, and the posterior intercostal arteries. Disruption of these blood vessels can have the serious consequences of sternal ischemia, delayed wound healing, and an increased sternal complication rate [16, 17]. Rigid plate fixation, however, does not circumferentially compress the sternum and, therefore, affords a lower risk of damaging the local sternal blood supply. By reducing the risk of damaging the sternal blood supply, we believe that rigid fixation may lower the risk of sternal complications.

Rigid titanium plate fixation of the sterna carries a higher operative cost than wire fixation. The cost of six sternal wires is approximately $40, whereas the cost of three titanium plates and 12 titanium screws is approximately $500. The overall expense of thoracic procedures, however, which includes the hospital, surgical, and patient recovery costs, can potentially be reduced in patients receiving rigid fixation. The overall cost savings attributed to rigid plate fixation has already been demonstrated clinically in craniomaxillofacial operations [11]. The higher cost of rigid plate fixation may also be merited if significant patient benefit can be shown. Our study demonstrated decreased motion across the osteotomy site. If decreased motion could be reproduced clinically, as it has been shown clinically for maxillofacial fracture repair, potentially this could translate into lower postoperative pain. A decrease in the patient’s postoperative pain, may allow him or her to breathe more deeply, thereby reducing pulmonary complications and postoperative recovery time. Rigid fixation may also speed primary bone healing and lower the risks of bone healing complications. The higher initial costs often associated with rigid plates and screws, therefore, may be offset by fewer hospitalization days, an improved quality of life, and an earlier return to normal function.

Our custom rigid titanium plates were designed with the potential need for emergency chest reentry in mind. Clinicians may believe that removal of rigid titanium plates would be more difficult than removing wires during such emergencies. We, however, were able to readily cut through both the standard and custom titanium plates (approximately 1.5 mm thick) using standard wire cutters that are in emergency carts on cardiothoracic wards. Furthermore, we used twice as many wires as we used plates, which lengthened the wire fixation reentry time. Although wire cutters can be used to cut through plates, the use of a screwdriver is the preferred method of plate removal. If plates and screw fixation becomes more commonplace, then screwdrivers would also become standard equipment on cardiac "crash" carts, eliminating this problem.

During the placement of sternal plates, there may be a concern with potentially passing a drill beyond the sternum and damaging important underlying structures. Over-drilling can be avoided in three ways. First, the sternal thickness could be measured and a prepackaged, guarded drill bit could be used. Second, a malleable retractor could be passed beneath the sternum to protect the underlying structures. Finally, KLS-Martin, L.P. has developed screws for facial fracture repair that can be placed without predrilling a hole. Adaptation of these self-drilling screws to sternal closures would eliminate completely the hazards of drilling screw holes.

Excessive plate projection has been of concern to craniomaxillofacial surgeons who worry about palpating or visualizing rigid fixation plates through the skin. These concerns have forced plate manufacturing companies to create thinner and stronger plates. The rigid titanium plates used in our study are approximately 1.5 mm thick and were originally made to repair mandibular fractures. These plates are approximately the same thickness as sternal wires and their twisted ends. In addition, the rigid plates were smooth and flat, and the wire ends were irregular and sharp.

In our study we found a greater stiffness and a lower lateral displacement in sterna fixed with rigid custom titanium H plates when compared with sterna fixed with stainless steel cerclage wires. In addition, there were fewer failures in sterna fixed with our custom plates than in sterna fixed with cerclage wires. Our results support our belief that plate configuration is of critical importance and that the fixation screws must be placed into solid bone to achieve true rigid fixation. We have proven our hypothesis by showing statistically significant reduced motion at the median sternotomy site in sterna fixed with titanium custom H plates compared with sterna fixed by stainless steel cerclage wires. Our results may have beneficial clinical implications, as greater stiffness and decreased motion at the sternotomy site could mean less postoperative pain, a decreased incidence of wound infection and sternal dehiscence, faster primary bone healing, and an earlier return to normal functioning. These benefits have been shown clinically in both the craniomaxillofacial and orthopedic literature. Our future plans are to use rigid plate fixation in animal studies to test these biomechanical properties in vivo and to determine the benefits of rigid fixation on primary bone healing. If rigid fixation in animal studies proves to be beneficial, limited trials in humans will be attempted. This study has enhanced our knowledge of the biomechanics of rigid sternal fixation. In addition, this study has led to the development of a rigid sternal plating system that is biomechanically superior to wire fixation. It is our hope that use of such a system will enable cardiothoracic surgeons to enjoy the same benefits of rigid fixation that is already being enjoyed by craniomaxillofacial, orthopedic surgeons, and other surgical specialists.


   Acknowledgments
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
References
 
This project was supported in part by grants from the UM-MAC, NIH P60-AR20557 and KLS-Martin L.P., Jacksonville, FL.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 Acknowledgments
 References
 

  1. Milton AF, cited by Kirschner M. Tratatad de tecnica operatoria general y especial. Barcelona: Editorial Labor, 1944;4:756–60.
  2. Julian O.C., Lopez-Belio M., Dye W.S., Javid H., Grove W.J. Appraisal of progress in surgical therapy. Surgery 1957;42:753-761.[Medline]
  3. Cheng W., Cameron D.E., Warden K.E., Fonger J.D., Gott V.L. Biomechanical study of sternal closure techniques. Ann Thorac Surg 1993;55:737-740.[Abstract]
  4. Sanfelippo P.M., Danielson G.K. Nylon bands for closure of median sternotomy incisions. Ann Thorac Surg 1972;13:404-406.[Medline]
  5. Grossi E.A., Culliford A.T., Krieger K.H., et al. A survey of 77 major infectious complications of median sternotomy: a review of 7,949 consecutive operative procedures. Ann Thorac Surg 1985;40:214-223.[Abstract]
  6. Ottino G., De Paulis R., Pansini S., et al. Major sternal wound infection after open-heart surgery: a multivariate analysis of risk factors in 2,579 consecutive operative procedures. Ann Thorac Surg 1987;44:173-179.[Abstract]
  7. Rohrich R.J., Watumull D. Comparison of rigid plate versus wire fixation in the management of zygoma fractures: a long-term follow-up clinical study. Plast Reconstr Surg 1995;96:570-576.[Medline]
  8. Hoffman W.Y., Barton R.M., Price M., Mathes S.J. Rigid internal fixation vs. traditional techniques for the treatment of mandible fractures. J Trauma 1990;30:1032-1036.[Medline]
  9. Zachariades N., Papademetriuo I., Rallis G. Complications associated with rigid internal fixation of facial bone fractures. J Oral Maxillofac Surg 1993;51:275-278.[Medline]
  10. Melone C.P., Jr Rigid fixation of phalangeal and metacarpal fractures. Orthop Clin North Am 1986;17:421-425.[Medline]
  11. Thaller S.R., Reavie D., Danniler A. Rigid internal fixation with miniplates and screws: a cost-effective technique for treating mandible fractures?. Ann Plast Surg 1990;24:469-474.[Medline]
  12. Sherman J.E., Salzberg A., Raskin N.M., Beattie E.J. Chest wall stabilization using plate fixation. Ann Thorac Surg 1988;46:467-469.[Abstract]
  13. Hendrickson S.C., Koger K.E., Morea C.J., Aponte R.L., Smith P.K., Levin L.S. Sternal plating for the treatment of sternal nonunion. Ann Thorac Surg 1996;62:512-518.[Abstract/Free Full Text]
  14. Cheung E.H., Craver J.M., Jones E.L., Murphy D.A., Hatcher C.R., Jr, Guyton R.A. Mediastinitis after cardiac valve operations: impact upon survival. J Thorac Cardiovasc Surg 1985;90:517-522.[Abstract]
  15. Milano C.A., Kesler K., Archibald N., Sexton D.J., Jones R.H. Mediastinitis after coronary artery bypass graft surgery: risk factors and long-term survival. Circulation 1995;92:2245-2251.[Abstract/Free Full Text]
  16. Arnold M. The surgical anatomy of sternal blood supply. J Thorac Cardiovasc Surg 1972;64:596-610.[Medline]
  17. Seyfer A.E., Shriver C.D., Miller T.R., Graeber G.M. Sternal blood flow after median sternotomy and mobilization of the internal mammary arteries. Surgery 1988;104:899-904.[Medline]



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ANN THORAC SURG ASIAN CARDIOVASC THORAC ANN EUR J CARDIOTHORAC SURG
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