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Vasa Vasorum Changes Following Stent Placement in Experimental Arterial Stenoses
I
From the Laboratory
Vasa Vasorum Changes Following Stent placement in Experimental Arterial Stenosesl Joio Martins Pisco. MD, PhD Miguel Correia, MD, PhD Jose A. Esperanga-Pina, MD. PhD Luis Aires de Sousa, MD, PhD
-
Index terms: Arteries, grafts and prostheses, 9*.1268,9*.1282 Blood vessels, foreign bodies, 9*.1268,9*.1282 Stents, 9*.1268
JVIR 1993; 4269-273
PURPOSE: Experimental stenoses were created in canine aortae to compare the effects of stent placement and balloon angioplasty on the vasa vasorum. MATERIALS AND METHODS: A balloon-expandablePalmaz stent was placed in the proximal stenosis, and angioplasty was performed in the distal stenosis in each of eight dogs. Two dogs were killed at 4,8,12, and 18 months, respectively. Specimenswere studied by means of microangiography, histology, scanning electronic microscopy, and Spalteholz technique. RESULTS: At up to 12 months, there was proliferation of the vasa vasorum and a rich plexus formed in each of the animals at each treated site. More vasa vasorum were seen after stent placement than after angioplasty. The new vessels were mainly venules located in the media. At 18 months, there was regression of the venules and the vasa vasorum distribution returned to baseline. CONCLUSION: The authors conclude that the effects of stents on the vasa vasorum are temporary.
vasorum are the small vessels that supply the vessel wall. The arterial wall is vascularized only beyond a depth of 0.5 mm. The intima and inner two-thirds of the media are avascular and are nourished from the vessel lumen by means of diffusion of nutrients. The vasa vasorum arise from branches of the abdominal aorta, particularly from the lumbar arteries, and form a plexus in the adventitia. The arterioles that reach the outer third of the media originate from the inner surface of that plexus. In normal dog aortae we found that precapillary arterioles, 0.03-0.01 mm in caliber, arise from the inner surface of those arterioles and are situated a t the junction of the external and middle third of the media (1). Since stent placement produces neointima formation and atrophy of the media (2,3), it is r,easonable to assume that it may also damage the vasa vasorum. However, to our knowledge, the changes of the vasa vasorum produced by stents have not been studied. VAsA
From the Department of Radiology, Sta Marta Hospital, Rua de Sta Marta, 1100 Lisboa, Portugal (J.P.),and the Departments of Anatomy (M.C., J.A.E.P.) and Radiology (L.A.d.S.j, New University of Lisbon, Portugal. From the 1991 SCVIR annual meeting. Received August 13, 1992; revision requested October 8; revision received November 17; accepted November 25. Address reprint requests to J.P.
" SCVIR, 1993
To evaluate the effect of stents and percutaneous transluminal angioplasty on vasa vasorum of stenotic arteries, artificial stenoses were created in the abdominal aortae of dogs. Subsequently, a Palmaz stent was placed a t this level.
MATERIALS AND METHODS This study was performed on eight dogs of both sexes that weighed between 15 and 20 kg. After general anesthesia was administered intravenously, a midline laparotomy was performed to create two focal stenoses in the abdominal aorta, 5 and 10 cm above the aortic bifurcation. The stenoses were created by placing a 310 resorbable chromic catgut suture that was passed twice around the aorta. To achieve uniform slack in the suture, a piece of 10-F Teflon tubing was placed alongside the aorta, before the suture was applied. Six weeks after creation of the focal stenosis, abdominal aortography was
270
Journal of Vascular and Interventional Radiology
March-April 1993
performed through the right femoral artery to document the stenosis. Six weeks was the time required for the suture material to be completely replaced by fibrous tissue. The diameter of the normal aorta as measured below the renal arteries was between 8 and 12 mm. At the stenosis, the diameter was 3.5 mm. Immediately after angiography, one balloon-exanda able intraluminal Pdmaz stent was placed in the most cephalic stenosis and the caudal stenosis was dilated with use of a polyethylene balloon catheter. The diameter of the balloon used for stent deployment was eaual to that of the balloon used for angioplasty and was also the equal to that of the aorta proximal to the stenosis. The balloons were inflated at a Dressure of 6 atm. The diameters of the stent site, the angioplasty site, and the adjacent proximal portion of the aorta were all equal. Two dogs were killed a t 4,8, 12, and 18 months, respectively, after the ~rocedure.Before the animals were killed, 10,000 IU of heparin was administered intravenously and abdominal aortography was performed with injection of contrast material through an 8-F pigtail catheter. At this time the angiographic appearance a t the level of the stent and the dilated segment was the same as that of normal aorta. After complete exsanguination, the aorta was flushed with normal saline solution at 37°C under 100 mm Hg pressure until clear saline was obtained. At that time, the aorta was ligated above the renal arteries and was filled with a mixture of Micropaque (Nicholas) and gelatin at 100 mm Hg. The aortic specimen was fixed with 10% formalin for 48 hours. Cross sections were obtained from the zones where stents were placed and zones that were dilated with balloon catheters. These sections were prepared for histologic study, micro&-q$ography, and s i n n i n g electron microscopy. The remainder of the specimens was initially placed in a mixture of equal parts of hydrochloridic acid and 5% sodium hypoclorite for 72 hours. This mixture was re-
a.
b.
Figure 1. Images of the abdominal aorta obtained 4 months after stent placement with use of the Spalteholz technique (original magnification, x 70). (a)In longitudinal section, precapillary arterioles (arrows) surround the stent. (b)In longitudinal section, new precapillary arterioles (arrow) arise from the outer media but do not reach the stent ( S ) (Fig 1continues).
Figure 1 (continued). ( c ) Scanning electron microscopic image of the transition zone under the stent (US) (right) and without the stent (WS) (left). Normal endothelium is seen on left, neointima without endothelium on right.
c.
newed every 24 hours. The specimens were then dehydrated with increasing concentrations of ethanol-60%,
80%, and 100% ethanol-for 24 hours in each concentration. Afterward, the specimens were placed in
Pisco et a1
271
Volume 4 Number 2
vasorum was still increasing. Once again the new vessels arose from the outer third-middle third junction of the media and reached the stent struts (Fig 3). In addition, a new venular plexus formed. These venules arose from the intima and converged to form larger tributaries that drained toward the media. Also a t 12 months, the neointimal layer was slightly thicker and the endothelium was normal. At 18 months the vasa vasorum distribution was normal. The thickness of the neointimal layer decreased, and the endothelium continued to appear normal. At all times, the zone of the aorta dilated with the balloon showed less proliferation of the vasa vasorum than that observed a t the areas in which the stent was placed, and the new vessels did not reach the inner third of the media. Figure 2. Abdominal aortic images obtained with Spalteholz technique 8 months after Palmaz stent placement. (a)On longitudinal section, more new vessels (arrows)are . On cross section, more shown close to the stent (S) (original magnification, ~ 6 0 )(b) new vessels (arrow)arise from the junction of the outer and middle third of the media that almost reach the stent (S).
acetone in a vacuum for 48 hours and then in a mixture of benzyl benzoate and methyl salicylate in equal parts, according to the Spalteholz technique, to obtain good transparency (4). The Spalteholz method is a technique that provides more detailed information concerning the morphologic changes of the vasa vasorum (4).
RESULTS Four months following stent placement there was earlv ~roliferationof the precapillary artiribles in the involved segment. These vessels extended medially from the junction of the outer and middle thirds of the media but did not reach the stent (Fig 1). Under normal circumstances, such as in controls studied previously, the arterioles are not distrib-
uted inside of the outer third of the media. At 4 months there was neointima formation without significant thickening in these experimental aortae, and no endothelium. Some medial atrophy was seen at the site of contact with the stent struts. By 8 months more new vessels were visible, and they were closer to the stent struts. By means of the clearing technique, it was shown that some of these vessels arose from the precapillary arterioles a t the junction of the outer and middle thirds of the media and they almost reached the stents (Fig 2). At this time endothelial cells lining the luminal surface of the stent were present. The inward extension of the precapillary arterioles continued up to 12 months. Similarly, the thickness of the neointimal layer increased up to 12 months. At 12 months the number of vasa
DISCUSSION In this experimental model, studies of balloon angioplasty have shown interruption of the vasa vasorum and rupture of elastic and muscle fibers at the site of the suture ligature (1). To our knowledge, changes in the vasa vasorum following stent placement have not yet been reported. The neovascular proliferation that follows balloon angioplasty and stent placement may be the result of hypoxia of the arterial wall due to impairment of the blood flow in the vasa vasorum (5). This may be due to temporary compression from the inside toward the outside that is caused by balloon inflation or by permanent compression due to a stent (6).The intimal hyperplasia induced by these treatments and the thickness of the stent strut may also cause increased oxygen demand and thus further stimulate the proliferation of the vasa vasorum. In normal arteries the intima and the inner third of the media are avascular and their nourishment comes directly from the main lumen. Geiringer found that beyond the critical depth of 0.5 mm, the lay-
272
Journal of Vascular and Interventional Radiology
March-April 1993
c. d. Figure 3. Abdominal aortic images obtained 12 months after Palmaz stent placement. (a)Longitudinal view obtained with Spalteholz technique shows that the number of vasa vasorum (arrows) close to the stent strut has increased (original magnification, ~ 5 0 ) . (b)Cross-sectional view obtained with Spalteholz technique shows that the new vessels reach the stent. ( c ) Scanning electron microscopic image shows venules (arrowhead) arising from the intima converging toward larger vessels (arrow) that drain toward the . Cross-sectional view obtained with Spalteholz technique after angioplasty of the caudal media (original magnification, ~ 6 5 0 )(d) stenosis shows some proliferation of the vasa vasorum (arrow) invading the media. This proliferation was less than that after stent placement (original magnification, x 50).
ers are vascularized and there is a correlation between intimal hyperplasia and vasa vasorum formation (7). Decreased diffusion of nutrients owing to mural thrombus deposition following stent placement may be another mechanism inducing neovascular proliferation. In the present study, the plexus of new vessels in the media was more prominent after stent placement than after angioplasty. Although we
have no direct proof, we postulate that this difference is due to longterm hypoxia as a result of prolonged compression of the vasa vasorum. The number of vasa vasorum and the thickness of the intima increased up to 12 months. Following that time there was a decrease in the number of vasa vasorum as well as in the thickness of the neointima. Complete endothelialization of the
inner surface of the balloon-expandable intraluminal stent has been described as early as 3 weeks after implantation in dogs (8,9). Palmaz et a1 found that at 8 weeks following stent placement, the endothelial surface under a scanning electron microscope appeared smoothly continuous with that of the adjacent vessel and had an orderly orientation in the direction of flow (2).
Pisco et a1
273
Volume 4 Number 2
In our study, a t 4 months following stent placement t h e neointima had a n irregular surface without endothelium. At 8 months endothelial cells were present. The growth of the endothelium is probably due to remaining patches of surviving endothelial cells between struts extending over t h e fibrin-covered metal after stent placement (10).At 18 months t h e endothelium and the vascular supply to the arterial wall were normal. I t was shown t h a t there was formation of new venules arising from t h e intima t h a t converged to form larger tributary vessels that drained toward t h e media. Although the vascular changes of improved arterial vascularization and venous return caused by t h e mechanical effects of stents were temporary, they may have a significant role in determining long-term patency, because they support the metabolic exchange in the arterial wall.
Acknowledgments: We thank Wilfrido Castaneda-Zuniga,MD, and Thomas Sos, MD, for thoughtful review of the manuscript and editorial suggestions; Carlos Lopes for technical expertise; and Paulo Alves for manuscript preparation. References 1. Pisco JM, Correia M, Pina JAF, de Sousa LA. Vasa vasorum changes following angioplasty and stenting. In: Castaneda-ZunigaWR, ed. Percutaneous revascularization techniques. New York: Thieme, 1993; 64-69. 2. Palmaz JC, Sibbit RR, Reuter SR, Tio FO, Rice WJ. Expandable intraluminal graft: a preliminary study. Radiology 1985; 156:73-77. 3. Palmaz JC, Windelar SA, Tio FO, Sibbit RR, Reuter SR. Balloon-expandable intraluminal grafting of atherosclerotic aortas. Radiology 1986; 160:723-726. 4. Spalteholz W. Das durchsichtigrnachen als biologische arbeistsmethode handbuch der biologischen: Arbeistsmethoden 1927; 8:409-432.
5. Zollikofer CL, Redha FH, Bruhlmann WF', et al. Acute and longterm effects of massive balloon dilation on the aortic wall and vasa vasorum. Radiology 1987; 164:14&149. 6. Pisco JM, Correia M, EsperangaPina JA, et al. Changes of the vasa vasorum after percutaneous transluminal angioplasty and stent placement in experimental arterial stenosis (abstr). Radiology 1989; 173(P): 386. 7. Geiringer E. Intimal vascularization and atherosclerosis.J Path Bact 1951; 63:201-211. 8. Palmaz JC, Kopp DT, Hayashi H, et al. Normal and stenotic renal arteries: experimental balloon-expandable intraluminal stenting. Radiology 1987; 164:705-708. 9. Schatz RA, Palmaz JC, Tio FO, Garcia 0,Reuter SR. Balloon-expandable intracoronary stents in the adult dog. Circulation 1987; 76:45@457. 10. Palmaz JC. Balloon-expandable intravascular stent. AJR 1988; 150: 1263-1269.
From the Laboratory
Vasa Vasorum Changes Following Stent placement in Experimental Arterial Stenosesl Joio Martins Pisco. MD, PhD Miguel Correia, MD, PhD Jose A. Esperanga-Pina, MD. PhD Luis Aires de Sousa, MD, PhD
-
Index terms: Arteries, grafts and prostheses, 9*.1268,9*.1282 Blood vessels, foreign bodies, 9*.1268,9*.1282 Stents, 9*.1268
JVIR 1993; 4269-273
PURPOSE: Experimental stenoses were created in canine aortae to compare the effects of stent placement and balloon angioplasty on the vasa vasorum. MATERIALS AND METHODS: A balloon-expandablePalmaz stent was placed in the proximal stenosis, and angioplasty was performed in the distal stenosis in each of eight dogs. Two dogs were killed at 4,8,12, and 18 months, respectively. Specimenswere studied by means of microangiography, histology, scanning electronic microscopy, and Spalteholz technique. RESULTS: At up to 12 months, there was proliferation of the vasa vasorum and a rich plexus formed in each of the animals at each treated site. More vasa vasorum were seen after stent placement than after angioplasty. The new vessels were mainly venules located in the media. At 18 months, there was regression of the venules and the vasa vasorum distribution returned to baseline. CONCLUSION: The authors conclude that the effects of stents on the vasa vasorum are temporary.
vasorum are the small vessels that supply the vessel wall. The arterial wall is vascularized only beyond a depth of 0.5 mm. The intima and inner two-thirds of the media are avascular and are nourished from the vessel lumen by means of diffusion of nutrients. The vasa vasorum arise from branches of the abdominal aorta, particularly from the lumbar arteries, and form a plexus in the adventitia. The arterioles that reach the outer third of the media originate from the inner surface of that plexus. In normal dog aortae we found that precapillary arterioles, 0.03-0.01 mm in caliber, arise from the inner surface of those arterioles and are situated a t the junction of the external and middle third of the media (1). Since stent placement produces neointima formation and atrophy of the media (2,3), it is r,easonable to assume that it may also damage the vasa vasorum. However, to our knowledge, the changes of the vasa vasorum produced by stents have not been studied. VAsA
From the Department of Radiology, Sta Marta Hospital, Rua de Sta Marta, 1100 Lisboa, Portugal (J.P.),and the Departments of Anatomy (M.C., J.A.E.P.) and Radiology (L.A.d.S.j, New University of Lisbon, Portugal. From the 1991 SCVIR annual meeting. Received August 13, 1992; revision requested October 8; revision received November 17; accepted November 25. Address reprint requests to J.P.
" SCVIR, 1993
To evaluate the effect of stents and percutaneous transluminal angioplasty on vasa vasorum of stenotic arteries, artificial stenoses were created in the abdominal aortae of dogs. Subsequently, a Palmaz stent was placed a t this level.
MATERIALS AND METHODS This study was performed on eight dogs of both sexes that weighed between 15 and 20 kg. After general anesthesia was administered intravenously, a midline laparotomy was performed to create two focal stenoses in the abdominal aorta, 5 and 10 cm above the aortic bifurcation. The stenoses were created by placing a 310 resorbable chromic catgut suture that was passed twice around the aorta. To achieve uniform slack in the suture, a piece of 10-F Teflon tubing was placed alongside the aorta, before the suture was applied. Six weeks after creation of the focal stenosis, abdominal aortography was
270
Journal of Vascular and Interventional Radiology
March-April 1993
performed through the right femoral artery to document the stenosis. Six weeks was the time required for the suture material to be completely replaced by fibrous tissue. The diameter of the normal aorta as measured below the renal arteries was between 8 and 12 mm. At the stenosis, the diameter was 3.5 mm. Immediately after angiography, one balloon-exanda able intraluminal Pdmaz stent was placed in the most cephalic stenosis and the caudal stenosis was dilated with use of a polyethylene balloon catheter. The diameter of the balloon used for stent deployment was eaual to that of the balloon used for angioplasty and was also the equal to that of the aorta proximal to the stenosis. The balloons were inflated at a Dressure of 6 atm. The diameters of the stent site, the angioplasty site, and the adjacent proximal portion of the aorta were all equal. Two dogs were killed a t 4,8, 12, and 18 months, respectively, after the ~rocedure.Before the animals were killed, 10,000 IU of heparin was administered intravenously and abdominal aortography was performed with injection of contrast material through an 8-F pigtail catheter. At this time the angiographic appearance a t the level of the stent and the dilated segment was the same as that of normal aorta. After complete exsanguination, the aorta was flushed with normal saline solution at 37°C under 100 mm Hg pressure until clear saline was obtained. At that time, the aorta was ligated above the renal arteries and was filled with a mixture of Micropaque (Nicholas) and gelatin at 100 mm Hg. The aortic specimen was fixed with 10% formalin for 48 hours. Cross sections were obtained from the zones where stents were placed and zones that were dilated with balloon catheters. These sections were prepared for histologic study, micro&-q$ography, and s i n n i n g electron microscopy. The remainder of the specimens was initially placed in a mixture of equal parts of hydrochloridic acid and 5% sodium hypoclorite for 72 hours. This mixture was re-
a.
b.
Figure 1. Images of the abdominal aorta obtained 4 months after stent placement with use of the Spalteholz technique (original magnification, x 70). (a)In longitudinal section, precapillary arterioles (arrows) surround the stent. (b)In longitudinal section, new precapillary arterioles (arrow) arise from the outer media but do not reach the stent ( S ) (Fig 1continues).
Figure 1 (continued). ( c ) Scanning electron microscopic image of the transition zone under the stent (US) (right) and without the stent (WS) (left). Normal endothelium is seen on left, neointima without endothelium on right.
c.
newed every 24 hours. The specimens were then dehydrated with increasing concentrations of ethanol-60%,
80%, and 100% ethanol-for 24 hours in each concentration. Afterward, the specimens were placed in
Pisco et a1
271
Volume 4 Number 2
vasorum was still increasing. Once again the new vessels arose from the outer third-middle third junction of the media and reached the stent struts (Fig 3). In addition, a new venular plexus formed. These venules arose from the intima and converged to form larger tributaries that drained toward the media. Also a t 12 months, the neointimal layer was slightly thicker and the endothelium was normal. At 18 months the vasa vasorum distribution was normal. The thickness of the neointimal layer decreased, and the endothelium continued to appear normal. At all times, the zone of the aorta dilated with the balloon showed less proliferation of the vasa vasorum than that observed a t the areas in which the stent was placed, and the new vessels did not reach the inner third of the media. Figure 2. Abdominal aortic images obtained with Spalteholz technique 8 months after Palmaz stent placement. (a)On longitudinal section, more new vessels (arrows)are . On cross section, more shown close to the stent (S) (original magnification, ~ 6 0 )(b) new vessels (arrow)arise from the junction of the outer and middle third of the media that almost reach the stent (S).
acetone in a vacuum for 48 hours and then in a mixture of benzyl benzoate and methyl salicylate in equal parts, according to the Spalteholz technique, to obtain good transparency (4). The Spalteholz method is a technique that provides more detailed information concerning the morphologic changes of the vasa vasorum (4).
RESULTS Four months following stent placement there was earlv ~roliferationof the precapillary artiribles in the involved segment. These vessels extended medially from the junction of the outer and middle thirds of the media but did not reach the stent (Fig 1). Under normal circumstances, such as in controls studied previously, the arterioles are not distrib-
uted inside of the outer third of the media. At 4 months there was neointima formation without significant thickening in these experimental aortae, and no endothelium. Some medial atrophy was seen at the site of contact with the stent struts. By 8 months more new vessels were visible, and they were closer to the stent struts. By means of the clearing technique, it was shown that some of these vessels arose from the precapillary arterioles a t the junction of the outer and middle thirds of the media and they almost reached the stents (Fig 2). At this time endothelial cells lining the luminal surface of the stent were present. The inward extension of the precapillary arterioles continued up to 12 months. Similarly, the thickness of the neointimal layer increased up to 12 months. At 12 months the number of vasa
DISCUSSION In this experimental model, studies of balloon angioplasty have shown interruption of the vasa vasorum and rupture of elastic and muscle fibers at the site of the suture ligature (1). To our knowledge, changes in the vasa vasorum following stent placement have not yet been reported. The neovascular proliferation that follows balloon angioplasty and stent placement may be the result of hypoxia of the arterial wall due to impairment of the blood flow in the vasa vasorum (5). This may be due to temporary compression from the inside toward the outside that is caused by balloon inflation or by permanent compression due to a stent (6).The intimal hyperplasia induced by these treatments and the thickness of the stent strut may also cause increased oxygen demand and thus further stimulate the proliferation of the vasa vasorum. In normal arteries the intima and the inner third of the media are avascular and their nourishment comes directly from the main lumen. Geiringer found that beyond the critical depth of 0.5 mm, the lay-
272
Journal of Vascular and Interventional Radiology
March-April 1993
c. d. Figure 3. Abdominal aortic images obtained 12 months after Palmaz stent placement. (a)Longitudinal view obtained with Spalteholz technique shows that the number of vasa vasorum (arrows) close to the stent strut has increased (original magnification, ~ 5 0 ) . (b)Cross-sectional view obtained with Spalteholz technique shows that the new vessels reach the stent. ( c ) Scanning electron microscopic image shows venules (arrowhead) arising from the intima converging toward larger vessels (arrow) that drain toward the . Cross-sectional view obtained with Spalteholz technique after angioplasty of the caudal media (original magnification, ~ 6 5 0 )(d) stenosis shows some proliferation of the vasa vasorum (arrow) invading the media. This proliferation was less than that after stent placement (original magnification, x 50).
ers are vascularized and there is a correlation between intimal hyperplasia and vasa vasorum formation (7). Decreased diffusion of nutrients owing to mural thrombus deposition following stent placement may be another mechanism inducing neovascular proliferation. In the present study, the plexus of new vessels in the media was more prominent after stent placement than after angioplasty. Although we
have no direct proof, we postulate that this difference is due to longterm hypoxia as a result of prolonged compression of the vasa vasorum. The number of vasa vasorum and the thickness of the intima increased up to 12 months. Following that time there was a decrease in the number of vasa vasorum as well as in the thickness of the neointima. Complete endothelialization of the
inner surface of the balloon-expandable intraluminal stent has been described as early as 3 weeks after implantation in dogs (8,9). Palmaz et a1 found that at 8 weeks following stent placement, the endothelial surface under a scanning electron microscope appeared smoothly continuous with that of the adjacent vessel and had an orderly orientation in the direction of flow (2).
Pisco et a1
273
Volume 4 Number 2
In our study, a t 4 months following stent placement t h e neointima had a n irregular surface without endothelium. At 8 months endothelial cells were present. The growth of the endothelium is probably due to remaining patches of surviving endothelial cells between struts extending over t h e fibrin-covered metal after stent placement (10).At 18 months t h e endothelium and the vascular supply to the arterial wall were normal. I t was shown t h a t there was formation of new venules arising from t h e intima t h a t converged to form larger tributary vessels that drained toward t h e media. Although the vascular changes of improved arterial vascularization and venous return caused by t h e mechanical effects of stents were temporary, they may have a significant role in determining long-term patency, because they support the metabolic exchange in the arterial wall.
Acknowledgments: We thank Wilfrido Castaneda-Zuniga,MD, and Thomas Sos, MD, for thoughtful review of the manuscript and editorial suggestions; Carlos Lopes for technical expertise; and Paulo Alves for manuscript preparation. References 1. Pisco JM, Correia M, Pina JAF, de Sousa LA. Vasa vasorum changes following angioplasty and stenting. In: Castaneda-ZunigaWR, ed. Percutaneous revascularization techniques. New York: Thieme, 1993; 64-69. 2. Palmaz JC, Sibbit RR, Reuter SR, Tio FO, Rice WJ. Expandable intraluminal graft: a preliminary study. Radiology 1985; 156:73-77. 3. Palmaz JC, Windelar SA, Tio FO, Sibbit RR, Reuter SR. Balloon-expandable intraluminal grafting of atherosclerotic aortas. Radiology 1986; 160:723-726. 4. Spalteholz W. Das durchsichtigrnachen als biologische arbeistsmethode handbuch der biologischen: Arbeistsmethoden 1927; 8:409-432.
5. Zollikofer CL, Redha FH, Bruhlmann WF', et al. Acute and longterm effects of massive balloon dilation on the aortic wall and vasa vasorum. Radiology 1987; 164:14&149. 6. Pisco JM, Correia M, EsperangaPina JA, et al. Changes of the vasa vasorum after percutaneous transluminal angioplasty and stent placement in experimental arterial stenosis (abstr). Radiology 1989; 173(P): 386. 7. Geiringer E. Intimal vascularization and atherosclerosis.J Path Bact 1951; 63:201-211. 8. Palmaz JC, Kopp DT, Hayashi H, et al. Normal and stenotic renal arteries: experimental balloon-expandable intraluminal stenting. Radiology 1987; 164:705-708. 9. Schatz RA, Palmaz JC, Tio FO, Garcia 0,Reuter SR. Balloon-expandable intracoronary stents in the adult dog. Circulation 1987; 76:45@457. 10. Palmaz JC. Balloon-expandable intravascular stent. AJR 1988; 150: 1263-1269.