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Ann Thorac Surg 2004;77:203-209
© 2004 The Society of Thoracic Surgeons

Original article: cardiovascular

Biomechanical comparison of median sternotomy closures

Julian E. Losanoff, MDa, Andrea D. Collier, BSc, Colette C. Wagner-Mann, DVM, PhDa, Bruce W. Richman, MAd, Harold Huff, MSc, Fu-hung Hsieh, PhDc, Alberto Diaz-Arias, MDb, James W. Jones, MD, PhDa*

a Department of Surgery, University of Missouri-Columbia, Columbia, Missouri, USA
b Department of Pathology, University of Missouri-Columbia, Columbia, Missouri, USA
c Department of Biological Engineering, University of Missouri-Columbia, Columbia, Missouri, USA
d Department of Psychiatry, University of Missouri-Columbia, Columbia, Missouri, USA

Accepted for publication July 29, 2003.

* Address reprint requests to Dr Jones, Department of Surgery, M580 Health Sciences Center, University of Missouri-Columbia School of Medicine, One Hospital Dr, Columbia, MO 65212, USA.
e-mail: jonesjw{at}health.missouri.edu


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
BACKGROUND: Poor healing of median sternotomy can significantly increase morbidity, mortality, and hospital costs. Effective union requires reliable sternal fixation. Although wire has proven the most reliable and widely used sternotomy closure material, no experimental studies have compared a large variety of wiring techniques in a human model. We developed an easily reproducible experimental model using cadaveric human sterna and compared several wiring methods to assess closure strength and stability.

METHODS: Fifty-three fresh adult human cadaveric sternal plates with adjacent ribs were fixed with specially designed spiked stainless steel clamps and attached to a texture analyzer. Single peristernal and transsternal, alternating single peristernal and transsternal, figure-eight peristernal, figure-eight pericostal, and Robicsek closures using no. 5 stainless steel wires were tested. We evaluated bone density, stiffness, and displacement using perpendicular, repetitive variable force loads of 800 Newtons cycling at a rate of 0.5 mm/s.

RESULTS: There were no significant differences in age, sex, or bone density in outcome measures of the sternal groups. No clamp failures or clamp damage to the specimens occurred. The single peristernal and alternating peristernal and transsternal closures proved superior in strength and stability (p < 0.001). The figure-eight peristernal, then the single transsternal, then the Robicsek were next stablest groups in decreasing order. The figure-eight pericostal closure had the highest failure rate (p < 0.001).

CONCLUSIONS: This novel model of sternotomy closure testing was reliable, inexpensive, and easily reproducible. The mechanical stability of peristernal and alternating peristernal and transsternal wires was significantly greater than that of the other tested methods. Pericostal figure-eight closures were not sufficiently stable to be considered a reliable method of primary sternotomy repair.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Healing complications after median sternotomy can include instability, nonunion, and infection. They occur in 0.3% to 5% of cases and are associated with a 14% to 47% mortality rate if mediastinitis supervenes [1, 2]. Such complications are best avoided by durable stability of the closure.

Many techniques for optimizing sternal closure have been in clinical use for more than 4 decades. Most studies of their effectiveness have been retrospective, with no statistical comparisons. The clinical trials were not preceded by experimental studies establishing the anatomic and biomechanical features of the particular closure methods tested.

The few experimental studies have used metallic jigs [3], bone analogue [4–6], animal bones [7–9], and a small number of human cadaveric sterna as models [10–14]. Although wire has proven the most reliable and widely used sternotomy closure material, only two studies [3, 8], neither using a human model, have compared a variety of wiring techniques. We developed an easily reproducible experimental model employing cadaveric human sterna, and used it to compare the closure strength and stability of several wiring methods.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
The study utilized a human cadaveric sternum model. No Institutional Review Board review for approval was required because federal regulations do not require human studies committee review of research on deceased individuals. The study was carried out in compliance with the protected health information of decedents.

Fresh autopsy sterna were stored at 2°C for 12 to 48 hours before the experiment. On the test day, the specimens were uniformly prepared for study at room temperature by using an electrical oscillating saw to perform midline sternotomies, with 4 cm of ribs left on either side.

A pair of clamps was fashioned from stainless steel blocks of equal size and designed to firmly grip the muscle, fascia, cartilage, and rib bone. Two longitudinal parallel rows of sharp 1-cm stainless steel nails were welded to the inside of each block at a 60-degree angle (Fig 1). Corresponding holes were drilled into both ends of each clamp to accommodate the bolts that held the clamp in place.



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  		Fig 1. Side-view of a clamped specimen showing the spikes penetrating tissue.

 
The sternal halves were approximated manually and no. 5 stainless steel monofilament wire sutures (Ethicon, Somerville, NJ) placed, consistent with the randomly selected specimens and sternotomy closure methods. Standard surgical needle drivers were used for closure. Fifty-three fresh adult human cadaveric sterna (median age 62.5 years) were used. Single peristernal and transsternal, alternating peristernal and transsternal, figure-eight peristernal, figure-eight pericostal, and Robicsek closures were tested (Fig 2). The number of specimens per testing group was determined by the level at which statistical significance was reached for any of the analyzed variables. Each manubrium was approximated with three single transsternal wires, except for the Robicsek closure, which consisted of a single perimanubrial wire loop. The transsternal and peristernal single wiring techniques used eight and four wire loops, respectively; the alternating technique used three peristernal and three transsternal wires, and the peristernal and pericostal figure-eight techniques used three wire loops each. The Robicsek technique used bilateral continuous pericostal weaves and a total of five overlying single peristernal wire loops [14].



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  		Fig 2. Schematic drawing illustrating the principles of sternotomy wiring techniques used in the study. Upper row: single transsternal, single peristernal, alternating trans- and peristernal; lower row: figure-eight peristernal, figure-eight pericostal, and Robicsek closures.

 
The clamps were placed on either side of the sternum, approximately 2.5 cm from the sternotomy, and secured with end bolts. The clamps were attached with bolts to the jigs of a TAHDi Texture Expert Exceed-Texture Analyzer (Stable Micro System; Texture Technologies Corporation, Scarsdale, NY). Biomechanical testing was performed with the sternotomy horizontally oriented (Fig 3). The specimen orientation was determined by the configuration of both the testing machine and jigs; there was no evidence that orientation affected the study results. The specimens were stressed with perpendicular, repetitive variable force loads of 0 to 800 Newtons cycling at 0.5 mm/s for 40 minutes. This uniaxial testing method was intended to reproduce the predominant lateral stresses on the sternum during breathing (moderate coughing), while remaining unaffected by minimal forces in the anterior-posterior and rostral-caudal directions. At the conclusion of the test, marked by failure of the closure or completion of the 40-minute period, the sternum was removed from the machine and a portion of the manubrium weighing 3 g to 4 g was cut away and cleaned of muscle for a density test. The sample was placed in a volumeter VM-100 (Horiba Instruments, Irvine, CA), which determines the volume and density of the bone using displacement in a container of constant volume with helium gas at constant pressure. The data were digitally stored for subsequent evaluation.



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  		Fig 3. Experimental setup with specimen attached to the biomechanical testing device.

 
Age, sex, bone density, stiffness, proportional limit load, displacement at various cycles, and permanent displacement after the first cycle were analyzed to identify differences among the techniques. Stiffness, measured in Newtons per millimeter, is defined as the slope of the linear portion of the first cycle of the force-displacement curve. This linear portion of the curve is referred to as linear elastic; the point at which the curve ceases to be linear is the proportional limit. The force (Newtons) at this limit is the proportional limit load. Bone density is a measure of the mass per unit volume of the sternal bone and is a measurement used to normalize the data. Bone density is measured to determine correlation between failure or high displacement in the sternal closure and low density bone. Displacement is observed at four points: at the peak (or greatest force) of cycle 1, cycle 10, cycle 25, and the final cycle of the test (40 minutes). This is based on the significant difference between the displacement in the respective intervals. Displacement is examined and recorded in millimeters; it is defined as the change in distance between the sternal halves as force is applied. Permanent displacement is defined as the part of the force-displacement curve after a cycle (or at the beginning of a new cycle) that shows a change in displacement without any apparent change in force. This measurement is examined after the first cycle.

All data are presented as mean ± SD. For age of individuals from whom the sterna were harvested, and for each of the measured variables (bone density, stiffness, and displacement), a one-way analysis of variance test or the Kruskal-Wallace analysis of variance on ranks test (when underlying conditions for parametric analysis were not met) was applied to determine whether there were differences among the closure groups. When significance was identified, an appropriate posthoc test was applied to identify differences between pairs of closure groups. Sex distribution among the four groups was compared using {chi}2 analysis. The Pearson product moment correlation was calculated to measure the strength of association between bone density and the permanent displacement at one cycle. The statistical software SigmaStat for Windows version 2.03 (SPSS, Chicago, IL) was used for all analyses, and the significance level was set at p less than 0.05.

To differentiate among the methods and determine a ranking from most stable to least stable, each closure method was assigned a score from 1 to 6 (1 best, 6 poorest) for each of 19 categories (there were no duplicate scores): the mean and median values for each method for each of the following variables: stiffness, proportional limit load, displacement at first cycle peak, displacement after 10 and 25 cycles, maximum displacement at the end of test, permanent displacement after the first, fifth and tenth cycles; and percent of catastrophic failures before each test's conclusion. The scores were compared among the six test methods and a total score for each method calculated.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
There were no significant differences detected in age, sex, and bone density in outcome measures of the sternal groups (see Table 1). No clamp slippage or clamp damage to the specimens occurred. Sternal fractures before or permanent sternal gape after the test were both considered evidence of technique failure (Fig 4). Sternotomy gaping at the incision's xiphoid end occurred first and uniformly in all techniques; in only the figure-eight pericostal technique was it greater than 1 cm after the first few cycles. Table 2 summarizes these data. The permanent gap became pronounced during the second half of the testing time. Close inspection of all specimens after they were removed from the testing machine and thoroughly cleaned of muscle and fascia revealed that the gap uniformly resulted from wires cutting through the bone.


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  		Table 1. Summary of Sex/Age, and Bone Density Data for Sterna in Each Study Group

 


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  		Fig 4. Macroscopic gaping at the conclusion of a test.

 

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  		Table 2. Summary of Failures (Sterna for Which One or More of Wires Cut Through Bone and Tension per Wire for Each Study Group

 
All of the objective data utilized to differentiate among the test groups are summarized in Table 3. Both the mean and median values for the listed variables were taken into consideration in differentiating the methods. These data demonstrate the consistency of the testing methodology applied, for each of the test groups. The final ratings of each of the six test groups are presented in Table 4. The two techniques rated first proved superior (p < 0.001) both in closure stiffness and displacement. The figure-eight pericostal closure had the highest failure rate (p < 0.001).


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  		Table 3. Mean and Median Values for Each Study Group for Indicated Variables

 

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  		Table 4. Summary of Sternotomy Group Ratings Based on Numerical Scoresa

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The standard closure of the sternum after sternotomy consists of five or more single transsternal monofilament surgical wires passed approximately 1 cm from each side [1]. The wires may easily cut through the bone causing transverse fragmentation and longitudinal separation, especially if the sternum is unusually narrow or osteoporotic, has been mishandled with sternal retractors, weakened by prolonged respirator treatment, or infected [1, 2]. The direction of the shearing forces resulting from longitudinal tension applied to the sternal halves is parallel to the wires, thus increasing the frontal pressure of the wire and promoting bone penetration. Modifications of the single transsternal suture used to prevent these complications have included single peristernal, figure-eight peristernal and transsternal, and pericostal closures [1, 2]. Most published series retrospectively analyze single closure methods, with no statistical comparison between the techniques. A number of experimental studies [3–15] have been done without resolution of the practical question of the best sternal closure. A review of all these studies demonstrates a wide variation among models, methods, and aims. Some of the conclusions suggested that sternal dehiscence occurs under physiologic loads and may be prevented by modified wire closures but only a few investigators attempted to compare multiple wire closures [3, 4]. None of these few studies used human sterna or a geometrically similar surrogate. The experimental design was based on the presumption that the human model is well suited for sternotomy closure research, provided that a large enough sample is available to statistically control for variations in demographics and specimen features, including bone density. We compared only wire closures because they are currently the most prominently utilized closure material among cardiothoracic surgeons worldwide [1, 2]. Recent research suggests that the use of standardized polyurethane foam sternal models is inexpensive, reduces variability between samples [6], and can be conducted under many different conditions, all apparent advantages over the use of biologic models. Only a detailed comparison between the human cadaveric and bone analogue models in a future large trial can show whether the polyurethane foam material approximates all aspects of the human sternal bone.

The use of whole sterna and high tension forces over long periods required a reliable specimen fixation. The reliability of the stainless steel spiked clamp was first validated in a porcine sternotomy study which demonstrated no tissue disruption resulting from the careful impalement at pulling forces averaging 730 to 916 N, and no clamp displacement even at closure failure loads [9]. Our previous [9] and present experiences with the clamp showed that it can be used for multiple measurements and experiments, conserving time and expense.

The uniaxial testing method used in our study has potential shortcomings. It has been shown that the anterior-posterior force needed to achieve 2.0 mm distraction was 263 ± 74 N, in comparison with 220 ± 40 N for a lateral force [13]. This emphasizes the importance of the former force, indicating that the variability of bone distraction in various sternal parts under different stresses must be considered. We used the property of bone density as a relatively reliable and measurable indicant of the specimens' susceptibility to sternotomy wiring failure. The thickness of the cortical layer might also have influenced the failure rate [15]. Our choice of bone density as a key indicator was primarily influenced by its availability to quantification in the clinical setting. The difficulty in measuring anterior-posterior and lateral forces and cortical thickness must be recognized as a study limitation.

Using the mathematical model derived by Casha and associates [3, 14] a reasonable estimate can be made of the forces across the sternotomy. The model's precision in force estimation was confirmed by a subsequent study [13], which determined the displacement of measured intrathoracic pressures. Casha's model assumes that all the forces will be exerted radially, which is reflected by the formula: T = rlP, where r is the radius of the chest, l is the length of the sternum, P is the pressure exerted on the chest walls, and T is the resultant force [3, 14]. Measuring our specimens, we determined that the average length of the sternum is approximately 20 cm. The average radial distance was noted to be approximately 15 cm. Using the given range of pressures (100 to 300 mm Hg), an estimate of the lateral forces across the sternotomy during coughing episodes is calculated to be approximately 400 to 1200 N, describing the average to maximum possible physiologic force produced by coughing. Because it is commonly asserted that a more rigid closure will deter sternal separation and displacement [1–13], we assumed that a reliable sternotomy closure should withstand at least twice the average force. The muscles that surround the thoracic cage tend to contract vigorously during coughing or other maneuvers that raise intrathoracic pressure. Data about the extent to which they increase the forces across the incision site are not available. We speculate that the increase is probably within the force limit tested; a higher force would have disrupted the sternotomy within a much shorter time, which is highly unlikely to occur in an actual patient. Our desired displacement force interval during testing was selected to be within the achievable physiologic load. Therefore 800 N was chosen as the testing force for this study, based on clinical reports that disruption occurs during sternal stress associated with sneezing or coughing.

The study's data analysis showed that the sternal closures tested behave differently during repetitive cycling loads. It should be acknowledged that the study did not compare the same number of wires in any of the methods tested nor the length of wire used for each closure. Instead we compared six completed clinical wire closures, each using specific number and configuration of wires to achieve integral sternal osteosynthesis. With respect to stiffness the two closure methods that utilized single peristernal wires (namely, single peristernal and combined peristernal and transsternal) were not statistically different from one another and were both superior to all the other methods, perhaps because in both methods loops passed over the thick cortical layer, inhibiting wires from cutting through bone. Interestingly the alternating peristernal and transsternal closure used one peristernal wire less than the peristernal single closure and three additional transsternal wires, with no significant impact on the closure's stability. Substituting four peristernal for eight transsternal wires in the multiple transsternal closure group significantly decreased the closure's stability. These findings suggest that a single peristernal wire adds more stability to the closure than two or three single transsternal wire loops. The statistically significant difference between the first two methods and the figure-eight peristernal closure may be attributable to longer wires used for figure-eight closure. Our findings demonstrated that the latter closure is not superior to the single peristernal method, contrary to our earlier report [1]. Like the single peristernal closure, the Robicsek method uses peristernal single wire loops placed over continuous pericostal weaves [16]. Its inferiority relative to the other single wire closures may be associated with the length of wires or with some of the limitations in the designed test. Soft tissue interposition between the weaves and sternum with progressively compressed tissue increasing the displacement is another, more remote, possibility. The value of the Robicsek method nevertheless remains unchallenged especially in advanced osteoporotic patients or those undergoing sternal reclosure [1, 2]. In this study the sterna were neither osteoporotic nor had pretesting mechanical defects so that the method's clinical advantages may not have been apparent. The figure-eight pericostal closure consistently showed the poorest performance contrary to expectations emerging from earlier studies [17, 18]. Our finding suggests that this method should be used only when all other closure alternatives have been exhausted and even then should be used only in combination with some of the superior closures.

The biomechanical behavior of the closure groups provides an important insight into the sternotomy separation. It suggests that the configuration and number of wires influences the closures' inherent stability or failure potential. Improved histomorphometric stability during the early healing stages is associated with more rigid sternal fixation [7], confirming our findings that a stable sternotomy is essential to complete and durable healing.

Our study suggests that the ex vivo human model using spiked clamps is valuable in comparing geometrically and mechanically varying closures using stainless steel wire. The model's low cost and easy reproducibility make it a promising foundation for future sternotomy closure research. Subsequent studies using this model will utilize a larger numbers of specimens, closure methods, and statistical comparisons to clarify the role and technique of wire configuration in improved sternotomy closures.

In conclusion, the model of sternotomy closure testing described here is reliable, cost-effective, and easily reproducible. The mechanical stability of peristernal single wire closure is significantly greater than that of figure eight peristernal and single transsternal closures. Pericostal figure-eight closures are not stable and should not be considered for primary sternotomy repair.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Losanoff J.E., Jones J.W., Richman B.W. Primary closure of median sternotomy: techniques and principles. Cardiovasc Surg 2002;10:102-110.[Medline]
  2. Losanoff J.E., Richman B.W., Jones J.W. Disruption and infection of median sternotomy: a comprehensive review. Eur J Cardiothorac Surg 2002;21:831-839.[Abstract/Free Full Text]
  3. Casha A.R., Yang L., Kay P.H., et al. A biomechanical study of median sternotomy closure techniques. Eur J Cardiothorac Surg 1999;15:365-369.[Abstract/Free Full Text]
  4. Hale JE, Anderson DD, Johnson GA, et al. An assessment of the pull-through strength and fatigue properties of a new sternal closure technique. 23rd Annual Meeting of the American Society of Biomechanics, University of Pittsburgh, Pittsburgh, Pennsylvania, October 21–23, 1999. Available at: http://asb-biomech.org/onlineabs/abstracts99/ACROBAT/ 134.PDF
  5. Cohen D.J., Griffin L.V. A biomechanical comparison of three sternotomy closure techniques. Ann Thorac Surg 2002;73:563-568.[Abstract/Free Full Text]
  6. Trumble D.R., McGregor W.E., Magovern J.A. Validation of a bone analog model for studies of sternal closure. Ann Thorac Surg 2002;74:739-745.[Abstract/Free Full Text]
  7. Sargent L.A., Seyfer A.E., Hollinger J., Hinson R.M., Graeber G.M. The healing sternum: a comparison of osseous healing with wire versus rigid fixation. Ann Thorac Surg 1991;52:490-494.[Abstract]
  8. Casha A.R., Gauci M., Yang L., et al. Fatigue testing median sternotomy closures. Eur J Cardiothorac Surg 2001;19:249-253.[Abstract/Free Full Text]
  9. Losanoff JE, Foerst JR, Huff H, et al. A biomechanical porcine model of median sternotomy closure. J Surg Res 2002;107:108–12
  10. Schade K., Greve H. Experimentelle Untersuchungen zur Stabilisierung der Refixation nach medianer Sternotomie. Langenbecks Arch Chir 1989;347:20-24.
  11. Cheng W., Cameron D.E., Warden K.E., et al. Biomechanical study of sternal closure techniques. Ann Thorac Surg 1993;55:737-740.[Abstract]
  12. Ozaki W., Buchman S.R., Iannettoni M.D., et al. Biomechanical study of sternal closure using rigid fixation technique in human cadavers. Ann Thorac Surg 1998;65:1160-1165.
  13. McGregor W.E., Trumble D.R., Magovern J.A. Mechanical analysis of midline sternotomy closure. J Thorac Cardiovasc Surg 1999;117:1144-1150.[Abstract/Free Full Text]
  14. Casha A.R., Yang L., Cooper G.J. Measurement of chest wall forces on coughing with the use of human cadavers. J Thorac Cardiovasc Surg 1999;118:1157-1158.[Free Full Text]
  15. Jutley R.S., Watson M.A., Shepherd D.E.T., Hukins D.W.L. Finite element analysis of stress around a sternum screw used to prevent sternal dehiscence after heart surgery. Proc Instn Mech Engrs Part H 2002;216:315-321.
  16. Robicsek F., Daugherty H.K., Cook J.W. The prevention and treatment of sternum separation following open-heart surgery. J Thorac Cardiovasc Surg 1977;73:267-268.[Abstract]
  17. Taber R.E., Madaras J. Prevention of sternotomy wound disruptions by use of figure-of-eight pericostal sutures. Ann Thorac Surg 1969;8:367-369.[Medline]
  18. Katz N. Pericostal sutures to reinforce sternal closure after cardiac surgery. J Card Surg 1997;12:277-281.[Medline]



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