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Ann Thorac Surg 2004;77:1262-1265
© 2004 The Society of Thoracic Surgeons


Original article: cardiovascular

Robotic skeletonizing of the internal thoracic artery: is it safe?

Gil Bolotin, MD, PhDa*, Walter W. Scott, Jr, MDa, Trevor C. Austina, Patrick J. Charlanda, Alan P. Kypson, MDa, L. Wiley Nifong, MDa, Kenneth Salleng, DVMa, W. Randolph Chitwood, Jr, MDa

a Division of Cardiothoracic Surgery, Brody School of Medicine at East Carolina University, Greenville, North Carolina USA

Accepted for publication September 23, 2003.

* Address reprint requests to Dr Bolotin, Department of Surgery, Tel Aviv Medical Center, 6 Weizman St, Tel Aviv, Israel
e-mail: bolotin{at}tasmc.health.gov.il


    Abstract
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
BACKGROUND: The advantages of internal thoracic artery skeletonization include early high blood flow, a longer conduit, and less bleeding than pedicle internal thoracic artery grafts. Longer conduits are needed for complete endoscopic arterial revascularization. Therefore this study was designed to determine the feasibility and safety of internal thoracic artery skeletonization using the da Vinci robotic system (Intuitive Surgical, Sunnyvale, CA).

METHODS: Nine dogs underwent bilateral robotic internal thoracic artery harvesting through three ports placed in the left chest. One internal thoracic artery was harvested as a pedicle in each dog, and the other was skeletonized. Internal thoracic artery blood flow was measured in each graft, and comparative endothelial histologic studies were performed. Data are mean ± the standard error of the mean.

RESULTS: All 18 internal thoracic arteries were harvested successfully. Skeletonized internal thoracic artery harvests required more time (48.0 minutes ± 1.8) than pedicle internal thoracic artery harvests (39.0 minutes ± 1.4; p < 0.05). Internal thoracic artery flows during the final intervals were similar (skeletonized = 30.0 mL/min ± 2.4 vs pedicle = 31.5 mL/min ± 1.8; p = 0.9). Free internal thoracic artery bleeding flow was similar in both groups (skeletonized = 162.0 mL/min ± 3.0 vs pedicle = 189.0 mL/min ± 2.4; p = 0.4). Histologically, both groups were similar with minimal endothelial damage.

CONCLUSIONS: Robotically skeletonized harvesting is safe, but it requires more time (48.0 minutes ± 1.8) than pedicle internal thoracic artery harvesting. Despite muted tactile feedback with robotics, neither technique was associated with histologic or functional damage. These encouraging results may represent an advantage for complete arterial revascularization in robotic coronary bypass patients.


    Introduction
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
The advantages of internal thoracic artery (ITA) skeletonization were reported to include early high blood flow, a longer conduit, and less bleeding than pedicle ITA grafts [13]. Longer conduits are needed for complete endoscopic arterial revascularization. The combination of potentially more distal anastomosis with the use of off-pump technology may represent a future advantage of the skeletonized technique in robotic-assisted totally arterial multivessel off-pump surgery [4, 5]. Therefore this study was designed to determine the feasibility and safety of ITA skeletonizing using the da Vinci robotic system (Intuitive Surgical, Sunnyvale, CA).


    Material and methods
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
Nine mongrel dogs weighing 22 to 36 kg were used for this study. All animals underwent bilateral internal thoracic artery harvesting through three ports in the left chest using the da Vinci robotic system (Intuitive Surgical). Each animal underwent one pedicled internal thoracic artery harvesting and one skeletonized harvesting. The experiments were performed in accordance with the "Guide for the Care and Use of Laboratory Animals" [6].

All animals were anesthesized with intravenous sodium thiopental (Pentothal, 15 mg/kg; Abbott SPA, Rome, Italy), intubated, and maintained with 1% to 2% isoflurane and O2 and N2O (1:2 mixture). Throughout the experiments, lung ventilation was achieved using a positive-pressure respirator (MDS [Matrx, Orchard Park, NY]). Arterial invasive blood pressure using the Hewlett Packard 78534C, GMBH (Hamburg, Germany), electrocardiogram using the Hewlett Packard 78534C, GMBH (Hamburg, Germany), and pulse oximeter using the Escort 20401 (Arleta, CA) were monitored throughout the experiment. Body temperature was kept constant using a heating blanket.

Internal thoracic artery harvesting surgical technique
The animals were positioned on their side with the left chest up. The first port for the robotic camera (12 mm) was placed in the fourth intercostal space at the midaxillary line. CO2 insufflation was used to maintain an insufflation pressure between 6 to 10 mm Hg before introducing the endoscope by using a high-flow laparoflator (Linvatec, Largo FL) connected to the camera port. After adequate visualization of the pleural cavity was achieved, the two instrument ports (5 mm) were placed under endoscopic vision in the second and sixth intercostal spaces, two centimeters posterior to the camera port. The right internal thoracic artery was harvested first through the left chest, followed by the left internal thoracic artery harvesting through the same ports. To avoid internal thoracic side bias, five procedures were started with skeletonizing the right internal thoracic, followed by pediculated harvesting of the left internal thoracic artery, whereas the other four procedures were started with pediculated right side internal thoracic artery harvesting. Two surgeons performed the experiments. The harvesting technique was similar to the open clinical technique; mainly the cautery dissection was used in the pedicled group and the blunt dissection with clip division of the arterial branches was used in the skeletonized group. There was no use of papaverine during the harvesting procedures.

Instrumentation and data collection
A Doppler flow probe (Transonic Systems, NY) was introduced into the chest through the first intercostal space and placed around each internal thoracic artery using the robotic arms. The flow in the internal thoracic artery was monitored before and during the harvesting (every 10 minutes), at the end of the harvesting, and 5 minutes later. Free internal thoracic bleeding was measured at the end of each experiment. Surface electrocardiogram, invasive blood pressure, blood saturation, and systemic temperature were monitored continuously throughout the experiments.

The histologic examination
Vessels were fixed in 10% neutral buffered formalin. Cross-sections for evaluation were obtained sequentially every 10 mm. Tissues were routinely processed, and 4-micron sections were stained with hematoxylin and eosin. Sections were evaluated by a pathologist who was blinded to the harvesting techniques. Each section was evaluated semiquantitatively on a scale from 0 to 4 (0 = none, 1 = minimal, 2 = mild, 3 = moderate, and 4 = severe) for the following criteria: vacuolation of the tunica media, loss of endothelium, margination of white blood cells, loss of the internal elastic lamina, splitting of the internal elastic lamina, thrombosis, adventitial hemorrhage, periadventitial hemorrhage, vasa vasorum heat-associated damage, vasa vasorum thrombosis, and vasa vasorum margination of white blood cells.

Data and statistical analysis
Hemodynamic data were gathered on a personal computer using Sonosoft 3.1.3 (Sono Metrics, Ontario, Canada) software. Robotic pedicled internal thoracic artery harvesting was compared with skeletonized harvesting using the Student's paired t test. Results are expressed as mean ± standard deviation. Differences were considered significant at a p value less than 0.05.


    Results
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
All 18 ITAs were harvested successfully and were found to be patent at the end of the experiments. For the skeletonized harvesting, a mean of 12.4 ± 0.3 clips were used for each internal thoracic as compared with 3.1 ± 0.2 clips in the pediculated group (p = 0.004).

Skeletonized ITA harvests required more time (46.6 ± 1 minute) than pediculated ITA harvests (35.5 ± 1 minute; p = 0.005). No learning curve was observed regarding the time needed to harvest the internal thoracic artery in either technique. There was no significant difference between the two surgeons; surgeon 1 required 45.8 ± 2 minutes for the skeletonization and 37.5 ± 2 minutes for the pedicle, whereas surgeon 2 required 47.4 ± 2 minutes for the skeletonization and 34.0 ± 3 for the pedicle (p = 0.74 and p = 0.86, respectively).

Internal thoracic artery blood flow at 5 minutes after harvesting was found to be similar when comparing the two techniques (skeletonized = 33.0 ± 1.4 mL/min vs pediculed = 36.1 ± 1.6 mL/min; p = 0.97). Free ITA bleeding flow was similar in both groups (skeletonized = 171.1 ± 10 mL/min vs pediculed = 187.5 ± 9 mL/min; p = 0.43).

There was a trend toward higher flow in the skeletonized group at the first part of the harvesting process (10 and 20 minutes) and a trend toward reduction in flow at the second half of the harvesting process (30 and 40 minutes) (Fig 1). However, these differences did not reach statistical significance, and 5 minutes after the completion of the harvesting process the flow between the two groups was found to be similar.



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Fig 1. Flow in the internal thoracic artery during the harvesting procedure and at the end of it as measured by transonic flow probe. {diamondsuit} = pediculated; {blacksquare} = skeletonized. (pre = preoperative.)

 
Histologic assessment of the 18 internal thoracic arteries yielded 32 specimens in the nine pedicled ITAs. Those were compared with 40 histologic specimens generated from the nine skeletonized internal thoracic arteries. The difference in specimen number is a result of the longer length achieved with the skeletonization method (25% longer). In the pedicled specimens there is still abundant periadventitial loose connective tissue and adipose tissue attached to the tunica adventitia with numerous small blood vessels (Fig 2A), whereas in the skeletonized specimens the outer layer is the tunica adventitia with intact smaller nourishing blood vessels (Fig 2B). Generally the damage was found to be minimal and similar between the two groups. The endothelial loss was found to be low and similar in both groups, 0.7 ± 0.8 in the pedicled group as compared with 0.9 ± 0.8 in the skeletonized group (p = 0.589). Thrombosis in the vessel lumen was extremely rare and similar (0.03 ± 0.2 in the pedicled group as compared with 0.03 ± 0.2 in the skeletonized group [p = 0.326]). Adventitial hemorrhage was 0.6 ± 1.1 in the pedicled group as compared with 0.9 ± 1.3 in the skeletonized group (p = 0.364).



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Fig 2. Histology cross sections (x20 magnification) of (A) a pediculed internal thoracic artery and (B) a skeletonized internal thoracic artery. (a = tunica media, b = tunica adventitia; L = arterial lumen.)

 
There was a trend toward more damage in the vasa vasorum of the skeletonized group, with heat changes of 0.4 ± 0.8 in the pedicled group versus 0.6 ± 1.0 in the skeletonized group (p = 0.08). There was no thrombosis 0.0 ± 0.0 of the vasa vasorum in the pedicled group versus 0.1 ± 0.3 in the skeletonized group (p = 0.08). However, the trend was opposite in the vasa vasorum margination (0.5 ± 0.1 in the pedicled group versus 0.2 ± 1.0 in the skeletonized group [p = 0.14]).


    Comment
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 
In the current study, skeletonized harvesting of the internal thoracic artery using a robotic system was found to be feasible and safe. Pedicled robotic internal thoracic harvesting has been reported by several authors [7, 8]. Practice with a phantom model and subsequent animal experiments allowed the surgeon to gain sufficient experience for application to the clinical setting [7], and after a steep learning curve, internal thoracic artery takedown was performed in less than 40 minutes [8]. Robotic harvesting of the internal thoracic artery is the first step toward a totally endoscopic coronary artery bypass grafting on either an arrested or a beating heart [8, 9]. Though some diversity in harvesting techniques exists between the clinical groups [10], skeletonized robotic internal thoracic artery harvesting was not reported.

Skeletonization of the internal thoracic artery was reported by Keeley [1] in order to achieve graft lengthening and potential use for sequential anastomosis. Other authors have reported an increased graft length as well as higher immediate blood flow in the skeletonized internal thoracic group as compared with the pedicled group, and also a larger anastomotic diameter in the skeletonized group [2, 3]. This higher immediate blood flow may increase the safety of arterial revascularization by reducing the risk of internal thoracic hypoperfusion syndrome [11]. Other groups have reported an improvement in pulmonary function tests and deep sternal wound infections in the elderly, diabetic patients with the routine use of bilateral skeletonized internal thoracic arteries [12, 13]. Calafiore and coworkers [14] reported the clinical advantages of bilateral skeletonized internal thoracic grafting in regard to the increased number of distal anastomosis and lower sternal wound complications as compared with bilateral pedicled internal thoracic artery grafting. This combination of potentially more distal anastomosis with the use of off-pump technology may represent a future advantage of the skeletonized technique in robotic-assisted totally arterial multivessel off-pump surgery [4, 5].

In the current study, robotic skeletonization was found to be more time consuming than robotic pediculed ITA harvesting. A difference of 11 minutes between the two techniques may be of importance, because totally endoscopic coronary artery bypass procedures are generally more time consuming. No learning curve was demonstrated in our study, probably because of the small number of procedures as compared with the clinical reports [15].

The minimal and comparable histologic damage is similar to previous reports comparing the two harvesting techniques in median sternotomy patients [16, 17]. The trend toward more vasa vasorum damage (heat changes and vasa vasorum thrombosis) in the skeletonized group may represent a potential hazard toward long-term changes. However, the overall number is quite low (0.1and 0.6, less than minimal) and therefore should probably not represent clinical significance.

The dog is a well-accepted animal model for ITA harvesting; however, several anatomical differences make the dog's ITAs easier to harvest. The major differences include the following: the first third of the dog's ITA is loosely in the mesentery, there are fewer side branches in the dog's ITA in the latter two thirds, and the vessel is covered mainly by muscle. Therefore clinical robotic harvesting is needed to verify our results.

In conclusion, based on our animal model, robotic skeletonization of the internal thoracic artery is feasible and safe, and it may represent a future advantage for total arterial robotic coronary artery bypass grafting.


    References
 Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

  1. Keeley S.B. The skeletonized internal mammary artery. Ann Thorac Surg 1987;44:324-325.[Abstract]
  2. Deja M.A., Wos S., Golba K.S., et al. Intraoperative and laboratory evaluation of skeletonized versus pedicled internal thoracic artery. Ann Thorac Surg 1999;68:2164-2168.[Abstract/Free Full Text]
  3. Takami Y., Ina H. Effects of skeletonization on intraoperative flow and anastomosis diameter of internal thoracic arteries in coronary artery bypass grafting. Ann Thorac Surg 2002;73:1441-1445.[Abstract/Free Full Text]
  4. Cartier R., Leacche M., Couture P. Changing pattern in beating heart operations: use of skeletonized internal thoracic artery. Ann Thorac Surg 2002;74:1548-1552.[Abstract/Free Full Text]
  5. Kappert U., Cichon R., Gulielmos V., et al. Robotic-enhanced Dresden technique for minimally invasive bilateral internal mammary artery grafting. Heart Surg Forum 2000;3(4):319-321.[Medline]
  6. National Academy of Sciences. Guide for the Care and Use of Laboratory Animals. DHHS Publication, NIH No. 85–23, revised 1985
  7. Boehm D.H., Reichenspurner H., Gulbins H., et al. Early experience with robotic technology for coronary artery surgery. Ann Thorac Surg 1999;68:1542-1546.[Abstract/Free Full Text]
  8. Mohr F.W., Falk V., Diegeler A., et al. Computer-enhanced "robotic" cardiac surgery: experience in 148 patients. J Thorac Cardiovasc Surg 2001;121:842-853.[Abstract/Free Full Text]
  9. Kappert U., Cichon R., Schneider J., et al. Technique of closed chest coronary artery surgery on the beating heart. Eur J Cardiothorac Surg 2001;20:765-769.[Abstract/Free Full Text]
  10. Jacobs S., Falk V. Pearls and pitfalls: lessons learned in endoscopic robotic surgery—the da Vinci experience. Heart Surg Forum 2001;4(4):307-310.[Medline]
  11. Wendler O., Tscholl D., Huang Q., Schafers H.J. Free flow capacity of skeletonized versus pedicled internal thoracic artery grafts in coronary artery bypass grafts. Eur J Cardiothorac Surg 1999;15:247-250.[Abstract/Free Full Text]
  12. Matsumoto M., Konishi Y., Miwa S., Minakata K. Effect of different methods of internal thoracic artery harvest on pulmonary function. Ann Thorac Surg 1997;63:653-655.[Abstract/Free Full Text]
  13. Gurevitch J., Paz Y., Shapira I., et al. Routine use of bilateral skeletonized internal mammary arteries for myocardial revascularization. Ann Thorac Surg 1999;68:406-411.[Abstract/Free Full Text]
  14. Calafiore A.M., Vitolla G., Iaco A.L., et al. Bilateral internal mammary artery grafting: midterm results of pedicled versus skeletonized conduits. Ann Thorac Surg 1999;67:1637-1642.[Abstract/Free Full Text]
  15. Vassiliades T.A., Jr Technical aids to performing thoracoscopic robotically-assisted internal mammary artery harvesting. Heart Surg Forum 2002;5(2):119-124.[Medline]
  16. Gaudino M., Toesca A., Nori S.L., Glieca F., Possati G. Effect of skeletonization of the internal thoracic artery on vessel wall integrity. Ann Thorac Surg 1999;68:1623-1627.[Abstract/Free Full Text]
  17. Sasajima T., Wu M.H., Shi Q., Hayashida N., Sauvage L.R. Effect of skeletonizing dissection on the internal thoracic artery. Ann Thorac Surg 1998;65:1009-1013.[Abstract/Free Full Text]



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