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Ann Thorac Surg 2001;72:810-815
© 2001 The Society of Thoracic Surgeons

Original article: cardiovascular

Arterial balloon catheter: a new atraumatic device for dilating arterial grafts

Hugues Jeanmart, MDa, Louis P. Perrault, MD, PhDa, Nathalie Desjardins, BSa, Olivier Chavanon, MDa, Michel Carrier, MDa, James D. Fonger, MDb

a Research Center and Department of Surgery, Montreal Heart Institute, Montreal, Quebec, Canada
b Adventist Hospital, Washington, DC, USA

Accepted for publication May 17, 2001.

Address reprint requests to Dr Perrault, Research Center, Montreal Heart Institute, 5000 Belanger St East, Montreal, Quebec, HIT 1C8, Canada
e-mail: lpperrau{at}icm.umontreal.ca


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. Harvesting of the internal mammary artery (IMA) for use in myocardial revascularization may result in spasm, which can impair early graft flow. Hydrostatic and mechanical dilatation can exert an intraluminal shear force, causing denudation of the IMA endothelium. A new long balloon dilatation technique (LB) has been developed to mechanically increase IMA diameter and flow without exerting any shear force on the endothelium.

Methods. Vascular rings of porcine IMA were divided into four groups: no manipulation (control), metal dilators (MD), short balloon (SB), or LB intraluminal dilation. In situ flows after dilation and percentage of intact endothelium after silver nitrate staining were determined. Endothelium-dependent contractions with arachidonic acid, relaxations with acetylcholine, endothelium-independent contractions with norepinephrine, and relaxation with sodium nitroprusside were recorded in organ chamber experiments.

Results. Increases in IMA flows were similar in all dilated groups. Endothelium-independent contractions and relaxations of IMA smooth muscle were unaffected by any type of mechanical dilation. However, endothelium-dependent contractions and relaxations were significantly impaired after MD and SB but preserved after LB dilation compared with control. Silver nitrate staining showed a greater preservation of the endothelial coverage after LB dilation.

Conclusions. IMA dilatation with the novel arterial LB catheter increases IMA flow and preserves endothelial cell integrity, making it an effective and atraumatic method to relieve IMA spasm before use for coronary artery bypass grafting.


   Introduction
Top
 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Coronary artery bypass surgery now routinely involves the use of the internal mammary artery (IMA). Its harvesting may result in spasm, which may decrease early graft flow. Different methods have been described to prevent and treat IMA spasm: application of external vasodilators (papaverine) on the pedicle, hydrostatic or mechanical dilation, and perivascular or intraluminal injection of papaverine [1, 2]. Hydrostatic dilatation with papaverine may disrupt the internal elastic lamina with the risk of dissection or subsequent intimal proliferation. Mechanical dilatations by either short balloon catheters (SB) or metal dilators (MD) can exert an intraluminal shear force that denudes the IMA endothelium. A new long arterial balloon dilatation catheter (LB) has been developed to mechanically increase IMA diameter and flow without exerting any shear force on the endothelium, to ensure preservation of its integrity and function. The long arterial balloon has the advantage of distributing the pressure applied to the arterial wall to minimize the trauma as compared with the dilatation by a short balloon catheter.

The central role of the endothelial cell in the regulation of arterial relaxation and vascular wall homeostasis has been recognized since 1980 [3]. Relaxation of arteries such as the IMA occurs through both endothelium-dependent and endothelium-independent pathways [4, 5]. Endothelium-dependent IMA relaxation requires both the presence and functional integrity of the endothelial cells. This endothelial cell monolayer is easily damaged by mechanical manipulation. Removal or damage of the endothelial cells impairs endothelium-dependent relaxations, and may promote the apparition of intimal hyperplasia because regenerated endothelium is dysfunctional with impaired relaxations, affecting mostly the Gi-protein pathway leading to a decrease in endothelium-derived nitric oxide (NO) release [6]. NO has an inhibitory effect on platelet and leukocyte adhesion to the endothelium and acts (synergically with prostacyclin) to inhibit platelets aggregation to prevent thrombosis and smooth muscle cell proliferation [7–10].

The aim of this study was to compare the effect of two commonly used dilatation techniques and the new technique using a long arterial balloon catheter (ABC) on IMA flow and on the vasoactive properties of the IMA endothelium in an acute porcine model.


   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Surgical protocol
The swines (90 kg) were anesthetized in a supine position and the distal IMA was exposed by a left median sternotomy incision. The long ABC is a 15-cm balloon of specially designed latex (Applied Medical, Irvine, CA) that inflates symetrically to a precise diameter (Fig 1). All the devices were introduced into the IMA through the distal end and inflated for 1 minute at 30 g (shear pressure applied to the arterial wall by the catheter) and then deflated for the short and long balloon, and simply passed through for the metal dilator. The inflated diameter of the balloon was chosen depending upon the size of the vessel; diameters ranging from 2.0 to 4.5 mm. IMA flow was measured by quantification of the volume of blood expelled into a recipient jar in 1 minute immediately after insertion of the devices. The animals were sacrified immediately after the procedure.



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  		Fig 1. Arterial balloon catheter. (A) Inflated; (B) deflated.

 
Vascular reactivity
After the sacrifice, the left and right IMAs were dissected and immediately transported to the laboratory in Krebs bicarbonate solution at room temperature. The periadventitial fat was removed carefully and completely dissected from the IMA before division into vascular rings of 4 mm in length. The endothelial function of the different rings were studied in organ chambers filled with oxygenated Krebs bicarbonate solution at 37°C (composition in mmol/L: NaCl, 118.3; KCl, 4.7; MgSO4, 1.2; KH2PO4, 1.2; glucose, 11.1; CaCl2, 2.5; NaHCO3, 25; and calcium ethylenediaminotetraacetic acid, 0.026: control solution). Oxygenation was ensured using a carbogen mixture (95% O2 and 5% CO2). The rings were suspended between two metal stirrups, one of which was connected to an isometric force transducer for isometric tension recording (EMKA, Paris, France).

The rings were stretched progressively in 1-g increments to a final resting tension of 5 g. The rings were allowed to equilibrate for 10 minutes after each 1-g increase. At 5 g, the rings were equilibrated for an additional 45 minutes before testing. We had previously found a final resting tension of 5 g for similar diameter IMA rings to produce the maximal contraction when stimulated with high-dose potassium (40 mEq/L). The chart baseline value was brought down to zero before norepinephrine (an alpha adrenergic receptor agonist [NE], 10-7 mol/L) was given to obtain a contraction between 50% and 80% of the maximal contraction (with KCI 40 mEq/L). Once a contraction plateau was reached at this dose, testing of IMA ring relaxation was begun.

Endothelium-dependent relaxations were studied using increasing concentrations of acetylcholine (ACh, 10-8 to 10-5 mol/L). Endothelium-independent relaxations were studied using increasing concentrations of sodium nitroprusside (SNP, 10-8 to 10-4 mol/L). After the last dose, a washout of the organ chambers was done and the rings were allowed to equilibrate for 45 minutes before NE 3 x 10-8 mol/L was added to the chambers to start the second part of the experiment. Once a contraction plateau was reached at this dose, the testing of IMA ring contractions were begun. Endothelium-dependent contractions were studied using increasing concentrations of arachidonic acid (AA, 10-8 to 10-5 mol/L). Endothelium-independent contractions were studied using increasing concentrations of norepinephrine (NE, 10-9 to 10-5 mol/L).

Silver nitrate staining
Specimens of the IMA from each group were used for fresh silver nitrate staining of the endothelial cell lining. Rings from each group were prepared as outlined in the section on functional testing. Instead of placing the rings in organ chambers, these rings were opened along their folded edge and silver stained to visualize the remaining intact endothelium. Specimens for silver nitrate staining were pinned to the surface of a dish coated with silicon. The rings first were treated for 30 seconds with 0.25% silver nitrate followed by a 30-second 5% glucose wash. This was followed by a 2-minute treatment with 3% bromine and another 30-second 5% glucose wash. The final treatment was 10 minutes of 4% formaldehyde followed by a 30-second 5% glucose wash. The stained specimens were mounted whole on glass slides and labeled for subsequent pathologic review.

The silver-stained rings were reviewed by a vascular pathologist blinded as to the treatment group of each ring. The percent surface area covered by intact endothelium was visually estimated to the nearest 10%.

Statistical analysis
Values from all rings at each concentration and in each group were averaged. The contractions are expressed as the percentage of maximal contraction (final percentage relaxation) for each group. The final percentage relaxation in each group for acetylcholine (ACh) and sodium nitroprusside (SNP), and the maximal percentage contraction after arachidonic acid (AA) and norepinephrine (NE), were compared by the Kruska-Wallis nonparametric test followed by the Wilcoxon signed-rank test when differences were identified. Results of the analysis of the silver nitrate studies were compiled by group and compared with the Wilcoxon signed-rank test; n refers to the number of IMA used.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
Flow rate of IMA
The increase in IMA flow was statistically significant after each method of dilatation compared with baseline, but there was no statistical difference between the three methods (control, 221 cc/min; LB, 287 cc/min; SB, 296 cc/min; MD (2.5 mm), 245 cc/min; MD (3.0 mm), 302 cc/min) (Fig 2). The blood pressure was constant throughout the experiments (data not shown), and there were no significant differences between groups.



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  		Fig 2. Internal mammary artery increases in flow rate before and after application of 2.5- and 3.0-mm metal dilators and long and short balloon. Results are presented as: (A) increase in mL/min of flow rate, and (B) increase in percentage of flow rate compared with control. Results are presented as mean ± standard error of the mean (* vs short balloon, p is nonsignificant).

 
Contraction studies
There was a statistically significant decrease of the maximal contraction to AA after MB and SB (30% and 35%, respectively, p < 0.001 vs LB and control) compared with the LB dilatation group (100%). There was no statistically significant difference in the maximal contraction to AA between the LB and the control group (110%) (Fig 3).



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  		Fig 3. Cumulative concentration-response curve to arachidonic acid in rings of porcine internal mammary artery with endothelium. Responses are given as a percentage of maximal contraction (final percentage relaxation). Results are presented as mean ± standard error of the mean.

 
There was no statistically significant difference in the maximal contraction to NE between groups (data not shown).

Endothelium-dependent relaxations
There was a statistically significant decrease in the maximal relaxation to ACh in the MB and SB groups (20% and 15%, respectively, p < 0.005 vs LB) compared with the control (85%) and LB groups (65%). There was no statistically significant difference in the maximal relaxation to ACh after LB dilatation compared with the control (Fig 4).



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  		Fig 4. Cumulative concentration-response curve to acetylcholine in rings of porcine internal mammary artery with endothelium. Responses are given as a percentage of maximal relaxation (final percentage contraction). Results are presented as mean ± standard error of the mean.

 
Endothelium-independent relaxations
There was no significant difference in endothelium-independent relaxations of IMA with SNP in the three methods of mechanical dilatation (Fig 5).



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  		Fig 5. Cumulative concentration-response curve to sodium nitroprusside in rings of porcine internal mammary artery with endothelium. Responses are given as a percentage of maximal relaxation (final percentage contraction). Results are presented as mean ± standard error of the mean.

 
Silver nitrate staining study
IMA rings submitted to LB dilatation exhibited a statistically significant greater preservation of endothelial cells (66%, p < 0.05 vs control 83%) than vascular rings exposed to MD and SB techniques (17% and 15%, p < 0.001 vs LB) (Fig 6A). A representative photograph of the intact endothelial lining in the IMA after dilatation with the long balloon catheter is shown is Figure 6B.



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  		Fig 6. (A) Percentage of endothelial coverage assessed by silver nitrate staining. Results are presented as mean ± standard error of the mean (* vs control p < 0.05; ** vs long balloon p < 0.001). (B) Representative photograph of the intact endothelial lining in the internal mammary artery after dilatation with the arterial balloon catheter.

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
The major findings of this study are: the LB is efficacious in augmenting the IMA flow; and it is associated with a better preservation of endothelium-dependent relaxations and of the cellular coverage.

The IMA is the conduit of choice for coronary artery bypass surgery because of its superior long-term patency rate compared with saphenous vein grafts, and it improves the survival of patients when the left IMA is grafted to the LAD [11–13]. The IMA is a pharmacologically active vessel that releases more NO than veins, which could explain its resistance to the development of atherosclerosis compared with native coronary arteries and other conduits [14] and its superior long-term patency [15]. Anatomical factors of the IMA including a thinner media, a more elastic than muscular artery, and fenestration in the internal elastic lamina could also contribute to this better long-term patency. The surgical preparation of the IMA may cause vasospasm of the artery and a decrease in arterial flow. This can lead to an increase in perioperative morbidity and even mortality in high-risk patients [1, 16–18]. Several technical steps have been tried to prevent injury to the graft, such as minimizing the contact with the IMA by keeping a thick and wide pedicule, and transecting the IMA at least 3 cm proximal to its bifurcation to allow resection of the muscular segment of the IMA [19].

Ultrasonic dissection has been proposed as an alternative to current techniques of dissection using cautery, which may cause thermal injury to the vascular wall. Tissues with a high water content are fragmented and aspirated (ie, fat); the tissues with high elastin and collagen contents, for example blood vessels, are spared. The main advantage of this technique is the limited area exposed to the mechanical energy produced (100 µmol/L of the tip of the handpiece). One study showed the safety of this approach by demonstrating no statistical difference between the endothelial function of the IMA after its dissection with this system or with a standard dissection technique [20].

Saline injection between the costal cartilages and adjacent tissue for separating the IMA from the chest wall is another technique described by John and colleagues [21]. One variant of this technique is the use of papaverine instead of a saline solution, to dilate pharmacologically the IMA and its branches, thus offering a better working field. Visualization and division of the IMA is easier and may reduce the time needed for dissection [22].

The skeletonization technique was first described in 1987 by Keeley as a means to increase graft length [23]. Removal of the endothoracic fascia allows dilatation of the IMA, so that the free flow in skeletonized arteries is superior to that of pedicled conduits [24, 25]. This increased flow could be secondary to the local sympathetectomy that occurs during skeletonization. Different studies have demonstrated that skeletonization has no detrimental effects on the morphology, histology, and tissue viability of the IMA [26, 27]. A recent study has evaluated the integrity of the endothelial cell layer after surgical preparation. Transmission electron microscopic examination and immunohistochemical studies have demonstrated the integrity of the endothelial cell layer in skeletonized IMA (same as the pedicled conduit) [27]. Although, a study of Deja and colleagues did not demonstrate any statistically significant difference between the endothelial function of skeletonized IMAs and pedicled conduit after dissection [25], but further investigation is warranted to evaluate the long-term endothelial function and patency of this graft. The use of bipolar cauterization allows precise control of the current and avoids random spraying of heat [23], and has been advised for the skeletonization of the IMA. This approach may limit damage to the vessel wall [28]. Many surgeons fear injury to the IMA during skeletonization, which would affect the early and late results of the surgery [28, 29], and use of bipolar cautery could improve the safety of this approach.

Numerous pharmacological interventions may be used to prevent IMA spasm. Different studies have shown an increase in the human IMA flow after wrapping in a swab soaked with papaverine, nifedipine, glyceryl trinitrate, or sodium nitroprusside [2, 6]. Only one study has showed spontaneous relaxation of the IMA if the time between dissection and grafting was over 30 minutes, leaving the use of pharmacological agent only for specific cases of IMA spasm before grafting [30].

Intraluminal injection of papaverine to prevent IMA spasm [1] has yielded results comparable with those with wrapping of the IMA in a sodium nitroprusside-soaked swab, but the vasodilatation may be due to stretching of the smooth muscle cells of the media and not to the pharmacological effect of the papaverine itself on the endothelium and vascular smooth muscle.

Mechanical dilatation with a metallic probe has been tested on canine IMA [31]. The increase in IMA flow obtained was associated with a loss of endothelial cells. This loss was responsible for impaired relaxation to prostacyclin and the endothelium-derived relaxing factor (NO). Those mediators are important modulators of vasomotor tone and inhibitors of platelet adhesion and aggregation, and smooth muscle cell proliferation. A decreased release of these factors may predispose to postoperative spasm and early thrombosis of the graft, as well as premature development of intimal hyperplasia. Intraluminal manipulation is similar to the technique used in physiological experiments to remove the endothelium, which involves rubbing of the endoluminal surface of the vessel with radial pressure.

The use of a balloon catheter is an alternative to treat IMA spasm. The effect of dilation with a Fogarty IMA balloon catheter on the integrity of the endothelial cell layer has been studied. The balloon catheter was inflated at a tension of 20 or 30 g and then was withdrawn slowly. Scanning electron microscopy revealed severe, tension-dependent alterations of the endothelium (extensive zone of denudation with platelet attachment). Endothelial injury occurred simply by inflation of the catheter without shearing by the inflated balloon [32]. The zone of denudation offers a thrombotic surface that could lead to early graft occlusion or later to the development of intimal hyperplasia.

Overdistension of the saphenous vein (> 150 to 300 mm Hg) is known to cause a loss of endothelial coverage, adhesion of platelets and leucocytes, and a decrease in early graft patency [33]. Histological examination of the distended segment showed that the zone denuded of endothelium was the preferential site of platelet and leukocyte aggregation. Increased platelet adhesion is associated with an increase in degranulation, which produces a greater local production of platelet-derived growth factor (PDGF), which could be associated with a greater degree of myointimal hyperplasia [34].

The present study suggests that the use of the long balloon (LB) for IMA dilatation is a superior alternative to augment IMA flow and prevent IMA spasm. This technique offers the same result as other mechanical dilatators but has the advantage of ensuring better preservation of the contractile and endothelial function of the IMA. As discussed above, preservation of the integrity of the endothelium is associated with less platelet adhesion and aggregation, due to the preservation of the protective effects of endothelium-derived relaxing factors produced by the vessel wall, which may potentially be followed by a better long-term graft patency.

Limitations
The limitations of this study include the use of normal swine IMA, which might not respond in the same way as the IMA of patients with diffuse atherosclerosis, whom already may have generalized endothelial dysfunction, which might tolerate dilatation as well. Also, this acute study does not address the long-term effect on endothelial function and graft patency of this new technique but is relevant to the immediate intraoperative and postoperative period.

Also, of paramount importance is the study of the effect of dilatation techniques in different types of arterial conduits elastic arteries (IMA, gastroepiploic artery [GEA]) versus muscular arteries (inferior epigastric artery [IEA], radials). Chronic studies on the same porcine model have shown that arterial long balloon dilatation is not detrimental to the endothelial cell function chronically (30 days) and is therefore an effective and atraumatic method to relieve IMA spasm before coronary bypass grafting [35].

Conclusion
In summary, the long balloon ABC catheter dilatation technique is a superior method of IMA dilatation because no shear forces are exerted on the endothelium, and therefore it prevents injuries to the vascular wall, which could translate into better clinical results.


   References
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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Related Article

Invited commentary
Guo-Wei He
Ann. Thorac. Surg. 2001 72: 816. [Extract] [Full Text] [PDF]




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