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Ann Thorac Surg 2005;79:1352-1357
© 2005 The Society of Thoracic Surgeons

Original articles: Cardiovascular

Sternal Nourishment in Various Conditions of Vascularization

Alexander A. Fokin, MD, PhD*, Francis Robicsek, MD, PhD, Thomas N. Masters, PhD, Alex Fokin, Jr, BS, Mark K. Reames, MD, James E. Anderson, Jr, MD

The Department of Thoracic and Cardiovascular Surgery, Heineman Medical Research Laboratories, Carolinas Medical Center, Charlotte, North Carolina

Accepted for publication August 5, 2004.

* Address reprint requests to Dr Robicsek, Carolinas Medical Center, 1001 Blythe Blvd, Charlotte, NC28203 (E-mail: frobicsek{at}sanger-clinic.com).

Presented at the Poster Session of the Fifty-first Annual Meeting of the Southern Thoracic Surgical Association, Cancun, Mexico, Nov 4–6, 2004.


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
BACKGROUND: Early changes in sternal perfusion were studied after midline sternotomy and different methods of mammary artery (MA) harvesting.

METHODS: Our observations were made in the swine model after midline sternotomy. In group 1 (6 animals), after unilateral skeletonized MA harvesting, 99mTc particles were injected intravenously. In group 2 (7 animals), after unilateral mammary artery and vein harvesting (semiskeletonized technique), 99mTc particles were injected intravenously. In group 3 (5 animals), after skeletonized bilateral MA harvesting, 99mTc particles were injected into the intercostal musculature lateral to the sternal border. In groups 1 to 3, sternal samples were analyzed using gamma counting. In group 4 (6 animals), unilateral skeletonized MA harvesting was performed. In group 5 (5 animals), the MA was harvested unilaterally using the semiskeletonized technique. In groups 4 and 5, sternal blood flow was assessed using thermography. Data were collected in all groups for 5 hours postoperatively.

RESULTS: Both radioactive and thermographic flow measurements showed a statistically significant decrease in sternal blood flow on the side of harvested mammary vessels, regardless of harvesting technique. Radioactivity of the devascularized hemisterni on the side of intramuscular particle injection was substantially higher than in the contralateral half, confirming the role of diffusion in sternal nourishment. The distal sternal segments were least perfused by the MA.

CONCLUSIONS: There is an acute reduction of sternal perfusion during the early postoperative period, even if collaterals are preserved by skeletonized MA harvesting. Diffusion plays an important role in sternal nourishment, particularly of the xiphoid, and even more so after MA harvesting.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 Acknowledgments
 References
 
The mammary vessels, principal providers of the sternal blood supply, are often harvested to serve as conduits for coronary bypass operations. This event is believed to contribute to the risk of postoperative complications such as sternal instability, necrosis, and infection [1, 2]. Analysis of sternal perfusion and the rate of complications after various techniques of mammary artery (MA) harvesting (pedicled, skeletonized, semiskeletonized) in different patient groups (diabetic, obese, geriatric) revealed varying results, ranging from a definitive decrease in sternal blood supply to unimpaired perfusion, even after bilateral MA mobilization [3–7]. Sternal perfusion has also often been addressed indirectly by observing the occurrence rate of complications (mediastinitis, dehiscence, etc), which are commonly a result of sternal ischemia [2, 8].

There are only a few publications related directly to the assessment of sternal blood flow during the first hours after midline sternotomy and MA mobilization. The conclusions from these publications remain controversial [9–11]. The role of diffusion in sternal nourishment has not been addressed. Our study was designed to investigate the initial impact of different techniques of MA harvesting after midline sternotomy on sternal blood flow, using radionuclear and thermographic methods for sternal perfusion assessment.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 Acknowledgments
 References
 
The experiments were performed on 29 female Yorkshire domestic cross pigs, weighing an average of 35 kg. The animals were premedicated with an intramuscular injection of Telazol (Wildlife Pharmaceuticals, Fort Collins, CO) (4.4 mg/kg), xylazine (1.5 mg/kg), and atropine (0.04 mg/kg). Once fully anesthetized, they were placed in a supine position, endotracheally intubated, and artificially ventilated using a Siemens ventilator (model E350E SV900D, Siemens, Erlangen, Germany). A deep anesthetic plane was maintained with isoflurane (1.25 to 2%). During the entire course of the observations, the animals received normal saline solution (50 to 75 mL/h) given intravenously to maintain hydration. They were handled according to the National Research Council "Guide for the Care and Use of Laboratory Animals" (National Academy Press, Washington, DC, 1996).

A midline sternotomy was performed in all animals. Mammary artery harvesting was done unilaterally or bilaterally either by the skeletonized (mammary artery only) or the semiskeletonized (both the mammary artery and vein) technique, as described by others [2, 4]. Sternal blood flow after sternotomy and MA harvesting was assessed either by injecting and monitoring the passage and retention of radioactive particles or by analyzing thermographic measurements.

In the radioactive flow studies, we applied 99mTc sulfur colloid microparticles (100 to 200 nm) with an activity of 5mCi (Mallincrodt Inc, St Louis, MO). The microparticles were sized by double filtering using MILLEX-GV 0.22 µm and MILLEX 0.1 µm filters (Millipore Corp, Bedford, MA). The free pertechnetate [99mTc0-], measured in each batch of sulfur colloid preparation by thin layer chromatography, was found to be 2% ± 1%. The microparticles (1 mL) were introduced into the animal's circulation either intravenously (through an ear vein), or into the intercostal muscle in the second intercostal space 3 cm lateral to the sternal border on the side with a harvested MA.

Tissue samples were obtained 5 hours after injection from the center of all segments of each sternal half and their radioactivity assessed using a gamma counter (model Cobra II, Packard Instrument Co, CT) for 30 minutes, expressed in counts per minute (CPM) per gram of tissues and corrected for the decay of 99mTc and for background activity. Before each experiment, the gamma counter was normalized and a constancy test performed to insure counter stability and reproducibility of data.

Thermographic studies were carried out using a thermographic camera (ThermaCAM S-60, FLIR Systems, Boston, MA) with a sensitivity of 0.06°C, mounted 70 cm above the sternal surface. In these animals, the pectoralis muscles on both sides were detached and retracted laterally to expose the surface of the sternum. This may possibly have altered the collateral circulation, which is why the data from these groups were analyzed separately from the radioactive particle groups. Measurements of both sternal halves were taken simultaneously at the beginning of the experiment (baseline), and at 2 and 5 hours after MA harvesting. Mean temperature was calculated across all sternal segments from an average of 192 points along the sternal halves using ThermaCAM Researcher Pro 2.7 software (FLIR Systems). The results of these studies [12] were compared to the findings obtained by the radioactive flow studies. The accumulation of radioactive particles in the tissues presented a primarily static assessment of sternal perfusion, while the temperature changes reflected dynamic flow changes.

Depending on the variables in surgical technique and methods of investigation, the animals were divided into the following groups. Sternal perfusion was assessed using radioactive measurements in groups 1 to 3 and by thermography in groups 4 to 5. In group 1 (6 animals), the MA was harvested unilaterally using the skeletonized technique. The injection of the microparticles was intravenous. In group 2 (7 animals), the MA was harvested unilaterally using the semiskeletonized technique. The injection of the microparticles was intravenous. In group 3 (5 animals) the MA were harvested bilaterally using the skeletonized technique. The microparticles were injected into the intercostal musculature. In group 4 (6 animals), the MA was harvested unilaterally using the skeletonized technique. In group 5 (5 animals), the MA was harvested unilaterally using the semiskeletonized technique. In all groups, the side with harvested vessels or in which intramuscular injection was performed was considered experimental, while the contralateral side served as a control.

The blood flow in the proximal MA before harvesting was on average 26 mL/min, as measured by ultrasonic flowmeter (Animal Research Flow Meter, model T206, Transonic Systems, Inc, Ithaca, NY). The mean blood pressure was maintained in the vicinity of 65 mm Hg. All values in all groups were expressed as the mean ± standard error. Student's paired t test was applied for comparison of mean values (SigmaPlot 2001 for Windows, Version 7.101, SPSS Inc, Chicago, IL), and p less than 0.05 was considered significant.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 Acknowledgments
 References
 
The results of the experiments are shown in Figures 1 to 5 and Tables 1 and 2 and may be summarized as follows. In groups 1 to 2, radioactivity of the sternal halves on the harvested side was about half as compared to the side with intact blood supply, regardless of the harvesting technique employed (Fig 1). Segmental distribution of the 99mTc microparticles always revealed lower levels of radioactivity in the devascularized sternal half, also regardless of the harvesting technique (Fig 2). Diffusion from the neighboring tissues contributed to nourishment of the devascularized sternum (Fig 3). The ratio of radioactivity between normal and devascularized sternal halves after the semiskeletonized technique (group 2) was lower in comparison to the skeletonized technique (group 1), thus reflecting a retention of particle matter after venous drainage impairment (Figs 1, 2).



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  		Fig 1. Radioactivity of the sternal halves after unilateral mammary artery harvesting using skeletonized (group 1) and semiskeletonized (group 2) methods and intravenous injection of 99mTc microparticles. *The value of radioactivity on the control side was statistically significantly higher in comparison with the experimental side in each group. (CPM = counts per minute.)

 

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  		Table 1. Temperature Changes of Sternal Halves in Group 1 (Mean Values in °C)
 


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  		Fig 2. Radioactivity of sternal segments (mean CPM/g) after midline sternotomy and intravenous injection of 99mTc microparticles. Control versus experimental side. (A) Mammary artery harvested on the experimental side (group 1). (B) Mammary artery and vein harvested on the experimental side (group 2). (e = exponent.)

 


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  		Fig 3. Radioactivity of the sternal halves after bilateral mammary artery harvesting and unilateral intramuscular injection of 99mTc microparticles (group 3). (CPM = counts per minute.)

 
The temperature drop in the sternal halves with harvested mammary vessels (groups 4 and 5) was more pronounced as compared to the contralateral (control) halves, regardless of the harvesting technique. These changes were observed at 2 and 5 hours after harvesting (Tables 1, 2, Figs 4, 5). Both methods of perfusion assessment found the xiphoid process to be the sternal segment least perfused by the MA (Figs 2, 4).



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  		Fig 4. Thermographic images of sternal halves. Temperature scale is on the right. Lines drawn along sternal halves were used for temperature calculations. (A) Both sternal halves exhibit similar temperatures with the xiphoid being the coolest sternal segment. (B) Five hours after midline sternotomy and mammary artery harvesting. Lower temperature of the experimental sternal half as compared to the control sternal half.

 

   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
Acknowledgments
 References
 
The use of radiolabelled markers for sternal perfusion assessment is an established method that has been used in different clinical and experimental settings [4, 7, 13]. Thermography is also a recognized technique for the evaluation of changes in blood flow [14–17]. It has been successfully used in numerous clinical studies related to the cardiovascular system, ranging from the diagnosis of sternal wound infections to the identification of atherosclerotic plaques in the coronary arteries [18–20]. Recent refinements in the accuracy of this method, combined with its noninvasiveness and relative simplicity make thermography a valuable tool in blood flow measurements [21, 22].

Our findings show that MA harvesting produced an acute decrease in perfusion of the affected sternal half, even utilizing the skeletonized approach, and that this effect lasted for at least 5 hours. These data are in accordance with the reports that, after removal of the main source of sternal blood supply and disruption of the cross-anastomoses between the periosteal plexus by median sternotomy, the collateral flow from intercostal and segmental branches cannot immediately substitute for the missing MA [1, 9, 13]. Our results contradict the findings of Bahn and Holloway [11], who did not find a reduction in sternal blood supply immediately after MA harvesting. Korbmacher and colleagues [6] and Rivas and colleagues [7] also did not find a decrease in sternal blood supply at 12, or even 7 days after MA or bilateral MA harvesting using the pedicled technique. Other authors reported that an acute reduction in blood flow occurs only in diabetic and obese patients [2, 23]. There are publications that show the bilateral skeletonized MA mobilization in patients with diabetes reduces the risk of sternal infection as compared to the conventional pedicled technique [3, 24, 25]; however, the rate of sternal infection in obese diabetic women is high enough to advocate the use of a single MA as opposed to a bilateral MA graft [26]. Lorberboym and colleagues [4] described sternal ischemia 6 days after surgery only after pedicled MA harvesting, not after the skeletonized or semiskeletonized methods. According to literary data, sternal ischemia lasts for about a week and is usually resolved by the end of a month [27]. The transient nature of sternal ischemia was partly explained by intramedullary and periosteal blood flow from the contralateral side when only one MA had been harvested or from intercostal arteries [27]. Recovery of sternal perfusion after skeletonized or semiskeletonized harvesting should occur faster than after the conventional pedicled technique, due to less trauma during harvesting and preservation of more collateral vessels. Skeletonization also adds extra length to the graft, though employing this method increases harvesting time and may induce more severe spasm [25].

Questions have been raised concerning possible damage to the structural integrity of the MA wall during skeletonization. The incidence of injury to the MA during skeletonization was reported at 0.7% [28]. However, it was shown recently that the vasa vasorum count, endothelial function, innervation, etc, were similar after the pedicled and skeletonized techniques [29, 30]. In addition, it has been reported that the MA is nourished by luminal diffusion, therefore it is less susceptible to external injury [31]. There are also some concerns that the pedicled or semiskeletonized techniques may potentially cause some blood stagnation [4]. Taking into account the usual abundance of venous vessels, this passive congestion should not be a long-lasting phenomenon. Lorberboym and colleagues [4] expressed the view that increased sternal ischemia is probably not due to passive venous congestion, but rather to injury of several arterial channels.

Another interesting aspect of the physiology of the chest after deprivation of mammary blood flow is that the sternum may not only act as a devascularized bone graft, but that diffusion from neighboring tissues could contribute to its "survival." It has also been confirmed that midline sternotomy alone did not affect sternal blood perfusion. The latter is in compliance with previous reports that there is no significant difference between presternotomy and poststernotomy flows [9, 13].

The cartilaginous xiphoid process was found to be the sternal segment least perfused by the MA, therefore less susceptible to flow changes after MA removal. This also suggests a relatively higher importance of diffusion in its nourishment. These findings are in agreement with anatomical and clinical observations that point out the reduced blood supply to the xiphoid and that sternal dehiscence often starts from the distal part of the sternum [1, 32, 33].

Limitations of the Study
This study was designed to address only the early changes in sternal blood supply that occur after midline sternotomy and harvesting of the mammary vessels. Such early measurements of blood flow, however, preclude any interference by inflammation and the healing process, which may influence the assessment.

Sternal perfusion has been studied in different laboratory animals (in vivo experiments) [9, 10, 13, 29]. We considered the swine model appropriate because its large, broad, flat sternum with defined segments and mammary vessels is similar to that of a human. The size of the pigs also assured circulation very similar to that of human patients.

We accept the assumption that unilateral MA harvest has minimal or no effect on the blood supply of the contralateral hemisternum. We also assumed that midline sternotomy had a comparable effect on both sternal halves. If these postulates are valid indeed, then it was appropriate to use the contralateral sternal half as a control for the sternal half with harvested mammary vessels [4]. The recirculation of the radioactive marker and its delivery to sternal tissues through the preserved collaterals after MA harvesting and intramuscular injection was considered to be similar for both sternal halves.

Conclusions
Harvesting the MA either alone or together with the mammary vein acutely reduces the blood flow to the affected sternal half. This effect lasts for at least 5 hours and was not affected by preservation of collaterals with skeletonized or semiskeletonized harvesting. Sternal blood supply is not affected by midline sternotomy. Diffusion after sternal devascularization appeared to play an important role in sternal nourishment.



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  		Fig 5. Example of a graph showing temperature along the length of the sternum. (A) Baseline control ({circ}) and experimental (•) temperatures are similar. (B) Five hours after mammary artery harvesting, temperature of the sternal half on the experimental side ({blacktriangleup}) is substantially lower in comparison to the control ({triangleup}).

 

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  		Table 2. Temperature Changes of Sternal Halves in Group 2 (Mean Values in °C)
 

   Acknowledgments
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
References
 
This study was supported by grants from the Heineman Foundation for Research, Educational, Charitable and Scientific Purposes, Inc, New York, NY, and Heineman Medical Research, Inc, Charlotte, NC.


   References
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
 Acknowledgments
 References
 

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