Comparative analysis of celiac versus mesenteric artery outcomes after angioplasty and stenting

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1 From the Society for Clinical Vascular Surgery Comparative analysis of celiac versus mesenteric artery outcomes after angioplasty and stenting Sadaf S. Ahanchi, MD, Christopher L. Stout, MD, Tyler J. Dahl, BBmE, Rebecca L. Carty, MD, Cory A. Messerschmidt, BS, and Jean M. Panneton, MD, Norfolk, Va Background: Open bypass is the gold standard for treatment of mesenteric ischemia. With the refinement of endovascular therapy, visceral stenting is an attractive minimally invasive alternative, but the data are limited and which vessel responds best to stenting has not been addressed. This study compares the outcomes of superior mesenteric artery (SMA) and celiac artery (CA) stenting. Methods: All consecutive patients who underwent visceral stenting between January 2002 and May 2009 were reviewed. Standard statistical analyses, including Kaplan-Meier tests, were performed. Primary patency was defined as peak systolic velocities <350 cm/s for CAs and <450 cm/s for SMAs. Clinical patency was maintenance of either primary patency or the absence of recurrent symptoms. At arteriography, stenosis $70% was considered a loss of primary patency. Results: One hundred twenty-one patients received 140 visceral stents in the SMA (n [ 92; 65.7%), the CA (n [ 40; 28.6%), and the inferior mesenteric artery (n [ 8; 5.7%). Twenty-nine stents were placed in men (20.7%) and 111 stents were placed in women (79.3%) with a mean age of 72.9 years (range, ). The combined SMA/CA stent mean follow-up was 12.8 months. Technical success was 100% for all. Overall 30-day morbidity and mortality rates were 14% and 0.8%, respectively. One-year primary patency was significantly higher for SMA than for CA stents: 55% versus 18%, respectively (P <.0001). Six-month clinical patency was 86% for the SMA and 67% for the CA (P <.005). Loss of CA primary patency was associated with stent diameter <6 mm(p [.042) and age <50 years (two patients; P [.038). These factors did not correlate with loss of primary patency for SMA. Overall freedom from bypass was 93% at 4 years. Conclusions: Visceral stenting has an exceptionally high technical success rate with low procedural morbidity and mortality. Clinical primary patency and primary patency were significantly higher for the SMA group than for the CA group. Our data suggest that CA atherosclerotic lesions do not respond well to endovascular stenting, bringing into question its clinical utility. (J Vasc Surg 2013;57: ) Atherosclerosis, leading to stenosis and occlusion of the mesenteric arteries, is considered the leading cause of chronic mesenteric ischemia, which can lead to bowel necrosis and possibly death. 1 Open surgery has been the gold standard in the treatment of chronic mesenteric ischemia since its first success in With the introduction of endovascular procedures such as percutaneous transluminal angioplasty and stenting, the trend is shifting to more minimally invasive approaches. The literature suggests that symptomatic resolution is similar for open and endovascular revascularization. 3 The use of percutaneous transluminal angioplasty and stent placement has been shown to lead to favorable outcomes with primary and primary-assisted patency at 6 months ranging from 78.2 to 99%. 4,5 However, the issue of which vessel From the Division of Vascular Surgery, Eastern Virginia Medical School. Author conflict of interest: Dr Panneton has been paid a consulting fee by Medtronic and Spectronetics and is on their speakers bureau. Presented at the Thirty-eighth Annual Symposium of the Society for Clinical Vascular Surgery, Scottsdale, Ariz, April 7-10, Reprint requests: Sadaf S. Ahanchi, MD, Division of Vascular Surgery, Eastern Virginia Medical School, Sentara Heart Hospital, 600 Gresham Dr, Ste 8620, Norfolk, VA ( ahanchss@evms.edu). The editors and reviewers of this article have no relevant financial relationships to disclose per the JVS policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest /$36.00 Copyright Ó 2013 by the Society for Vascular Surgery. responds best to stenting has not been fully addressed. This study compares the outcomes of superior mesenteric artery (SMA) and celiac artery (CA) stenting. METHODS This is a retrospective review of all consecutive patients who underwent visceral stenting for visceral stenosis with the exclusion of vessel occlusions between January 2002 and May Records were reviewed for demographics, risk factors, preoperative and postoperative symptoms, and procedural and follow-up data including duplex ultrasound (DUS) findings. c 2 analysis was performed to identify factors that would impact stent patency. Kaplan-Meier estimates were used to determine patency and survival, with statistical significance based on log-rank. P <.05 was used to determine significance. All statistical analysis was performed using XLSTAT 1 (Addinsoft SARL, Andernach, Germany). Mesenteric procedures were performed under moderate sedation in our endovascular suite. Because we performed a retrospective review, the specifics of the procedure were at the discretion of the operating surgeon. Details of the procedure including sheaths, catheters, and type of stent varied based on the attending surgeon, but all visceral stents were balloon expandable. Visceral DUS was performed at 1, 6, and 12 months of follow-up. Mesenteric stents were considered free of in-stent restenosis if peak systolic velocity was <350 cm/s 1062

2 Volume 57, Number 4 Ahanchi et al 1063 Table I. Demographic and risk factor data for visceral stenting a Total CA/SMA (n ¼ 132) CA (n ¼ 40) SMA (n ¼ 92) P value Demographics Women 108 (82%) 32 (79%) 76 (83%).46 Men 24 (18%) 8 (21%) 16 (18%).46 Age 73 (21-94) 74 (46-90) 72 (21-94) Risk factor Hypertension 106 (80%) 32 (80%) 74 (80%).98 Hyperlipidemia 80 (61%) 27 (67%) 53 (58%).31 Diabetes 50 (38%) 19 (47%) 31 (34%).16 Tobacco use 107 (81%) 27 (67%) 80 (87%).59 Cerebral vascular disease 33 (25%) 8 (20%) 25 (27%).35 Coronary artery disease 72 (55%) 26 (65%) 46 (50%).12 Congestive heart failure 16 (12%) 5 (12%) 11 (12%).95 Peripheral vascular disease 77 (58%) 24 (60%) 53 (58%).85 Chronic obstructive pulmonary disease 35 (26%) 9 (22%) 26 (28%).46 End-stage renal disease 4 (3%) 1 (3%) 3 (3%).92 Chronic renal insufficiency b 11 (8%) 3 (7%) 8 (9%).65 CA, Celiac artery; SMA, superior mesenteric artery. a Values are given as the number of patients (%) or mean (range). b Defined as stage 2 or worse chronic kidney disease. for CAs and <450 cm/s for SMAs. 6 The values were internally validated in our peripheral vascular laboratory and correlated with an angiographic finding of $70% stent restenosis. Absence of any duplex or angiographic evidence of stenosis defined primary patency. Clinical patency was defined as either the absence of symptoms or maintenance of primary patency. Periprocedural morbidity and mortality were defined as any adverse event occurring within 30 days of the procedure regardless of relation to the procedure. Late mortality was verified by the Social Security database. This study was approved by the Eastern Virginia Medical School institutional review board. RESULTS Between January 2002 and May 2009, 121 patients, all with multivessel disease, received 140 visceral stents. Access was the femoral artery in 84% of patients and the left brachial artery in 15% of patients. If the CA, SMA, and inferior mesenteric artery (IMA) are combined, 29 (20.7%) stents were placed in men and 111 (79.3%) stents in women, with an overall mean age of 72.9 years (range, ). Medical comorbidities included hypertension (80.7%), hyperlipidemia (61.4%), tobacco use (87.9%), coronary artery disease (55%), and peripheral vascular disease (57.1%) (Table I). There was no significant difference in demographics between patients who received CA stents and those who received SMA stents (Table I). All patients underwent preprocedural DUS to diagnose visceral stenosis, which was confirmed with angiography. Anatomic location of the mesenteric stents included the SMA (n ¼ 92 stents; 65.7%), CA (n ¼ 40 stents; 28.6%), and IMA (n ¼ 8 stents; 5.7%). All isolated CA stents (n ¼ 22) were placed in individuals with multivessel visceral stenosis, with the CA presenting with the more severe stenosis on angiography. Nineteen patients had two vessels stented: 18 patients had both CA and SMA stents, and one patient had both SMA and IMA stents. Because of the small numbers, IMA stents were not included in the comparisons of outcomes. All visceral stents were placed in symptomatic patients with abdominal pain. Other common symptoms included weight loss (55%) and food fear (20%) (Table II). There was no significant difference in symptoms between patients who received CA stents and those who received SMA stents (Table II). Technical success was 100% as determined by angiographic evidence of <30% residual stenosis. The only significant procedural difference between the SMA and CA groups was mean stent length (SMA ¼ mm vs CA ¼ mm; P <.05). One patient in the CA group died of a gastrointestinal bleed on postoperative day 29, yielding an overall 30-day periprocedural mortality rate of 0.8%. Overall 30-day procedure-related morbidity rate was 14%, with a majority of complications being access related (three pseudoaneurysms, two femoral hematomas, one brachial artery repair), renal (one contrast-induced nephropathy and one acute renal failure), or gastrointestinal (one upper bleed caused by esophagitis and two lower bleeds caused by colonic ischemia), with no difference between the two groups. Overall mean follow-up was 12.8 months, with mean follow-up periods of 13.1 months (range, ) for the SMA group and 11.9 months (range, ) for the CA group. The overall clinical patency rate was 63% at 1 year. The SMA stent group had a significantly higher primary patency than the CA stent group, with a 1-year primary patency of 55% for the SMA stents and only 18% for the CA stents (P <.0001) (Fig 1). The SMA stents again demonstrated a statistically significant advantage in clinical patency when compared with CA stents, with

3 1064 Ahanchi et al April 2013 Table II. Symptomatology and laboratory values of patients who received celiac artery and superior mesenteric artery stents a Symptom Total CA/SMA (n ¼ 132) CA (n ¼ 40) SMA (n ¼ 92) P value Weight loss 73 (55%) 20 (50%) 43 (47%).78 Food fear 27 (20%) 9 (22%) 18 (47%).75 Nausea or emesis 58 (44%) 21 (52%) 37 (40%).22 Diarrhea 58 (44%) 18 (45%) 40 (43%).91 Hematochezia 16 (12%) 7 (17%) 9 (10%).35 Mean preoperative creatinine level (mg/dl) SMA, Superior mesenteric artery; CA, celiac artery. a Values are given as the number of patients (%) unless otherwise noted. Fig 2. Kaplan-Meier curves for clinical patency results for celiac artery versus superior mesenteric artery (SMA) stenting. a 6-month clinical patency of 86% for the SMA group versus 67% for the CA group (P <.005) (Fig 2). Thirty-two (34.8%) SMA stents and 12 (30%) CA stents required reintervention. Two CA stents required restenting; the remaining reinterventions involved angioplasty, with one cutting balloon angioplasty. Nine SMA stents required restenting; the remaining reinterventions were balloon angioplasties, 10 of which were cutting balloon angioplasties. Average time to reintervention was 5 months longer in the SMA group (14.1 months) than in the CA group (9.1 months) (P <.043). The overall survival of all patients at 1 year was 85%, with no additional gastrointestinal-related deaths and no difference between groups. Overall freedom from reintervention at 1year was 54%, and at 4 years, 18%. Overall freedom from open surgical bypass was 93% at 4 years, with one CA bypass at 13.2 months and three SMA bypasses at a mean of 11.9 months (range, ). The 1-year survival free from symptom recurrence for the SMA group was 63% versus 53% for the CA group (P ¼.07) Further analysis was performed to determine if any risk factor correlated with in-stent restenosis. CA artery in-stent restenosis was associated with congestive heart failure, coronary artery disease, hypertension, chronic renal insufficiency, age <50, and stent diameter <6 mm(p <.05 for all). No comorbidity or procedural factors were found to significantly impact SMA in-stent restenosis. Lastly, a comparison of combined two-vessel stenting of the CA and SMA with single CA and SMA stenting revealed no significant difference in rates of in-stent restenosis and no difference in survival free from symptom recurrence. Fig 1. Kaplan-Meier curves for primary patency results for celiac artery versus superior mesenteric artery (SMA) stenting. DISCUSSION The first described successful use of percutaneous angioplasty to treat mesenteric ischemia was in Further advancements in the treatment of CMI, principally percutaneous transluminal angioplasty and stenting, have changed the course of treatment. Endovascular treatment provides a potential improvement in the 5%- 30% morbidity rate and 2%-12% mortality rate of open repair. 3,8-12 Our low morbidity and mortality rates and high technical success rate (100%) are similar to those in the literature But controversy still exists as to the comparison of open and endovascular mesenteric revascularization, with some citing the superiority of open repair based on superior durability. 23 Yet the concept and the execution of visceral stenting have evolved to make it a beneficial therapy in high-risk patients not candidates for open revascularization. Unfortunately, the outcome of CA stenting versus that of SMA stenting has yet to be fully examined. A major finding in our study is the great discrepancy in clinical patency and freedom from in-stent restenosis/ primary patency between CA stenting and SMA stenting. The reason for the difference requires further investigation, but our proposed hypothesis is that the CA is in a poor anatomic location and the dynamic forces of respiration combined with the fixed ligament attachments of the diaphragm potentially influence the results of CA angioplasty and stenting. On examination of the CA group, stents with a diameter <6 mm were significantly more likely to lose primary patency earlier than larger-caliber stents. This could be due to the relationship between radius and resistance to

4 Volume 57, Number 4 Ahanchi et al 1065 flow through a vessel: as the radius decreases, resistance increases fourfold. A diameter of 6 mm may be a critical threshold below which stents should not be deployed in the CA, if any endovascular treatment must be used. All stents were balloon expandable, but it would be interesting to see if use of nitinol or covered stents improved results in the CA. It has been suggested that open operations for chronic mesenteric ischemia have an improved long-term success rate when bypasses to both the CA and SMA are performed. 24,25 Recent data also suggest that this may be true as well for endovascular management. 22 But the literature reports mixed results for single- versus two-vessel stenting. 1,22,26 We did compare the subgroup of patients who had combined SMA and CA stenting with the subgroup that had single mesenteric stenting and we found no significant difference in the rates of in-stent restenosis (as defined under Methods) or survival free from symptom recurrence, although our patient numbers were smaller. Currently, there is no consensus on the number of vessels requiring endovascular treatment in patients with multivessel mesenteric disease. Limitations to our study include the retrospective nature of the study, the relatively small number of combined SMA/CA stenting procedures, and the use of DUS to diagnose in-stent restenosis. DUS still has an undefined role in diagnosing in-stent restenosis. Using native vessel criteria for reintervention in in-stent restenosis, Morvay et al found that intervention based on ultrasound findings did not improve patency outcomes or prevent recurrence of symptoms. 27 Recently, in a hypothesis-seeking study, Mitchell et al concluded that DUS criteria for native SMA stenosis cannot be applied to stented SMA stenosis. 28 Early in our experience, angiograms would be performed based on the lower nonvalidated velocity criteria to confirm the diagnosis of in-stent restenosis. These were considered as reinterventions for this study, possibly lowering the patency rates. On the basis of a recent internal validation study in our vascular laboratory, we are now using higher peak systolic velocity (peak systolic velocity >350 cm/s for CAs and >450 cm/s for SMAs) before proceeding with a visceral angiogram for suspected in-stent restenosis. 6 CONCLUSIONS In comparison to open repair, there has been a dramatic increase in the use of percutaneous transluminal angioplasty and stenting for the treatment of chronic mesenteric ischemia in high-risk patients. The literature has not compared CA stenting with SMA stenting. Which vessels to consider for stenting is an important concept, as our study shows that regardless of the number of vessels endorevascularized, CA stenting has a very high in-stent restenosis rate, significantly poorer clinical patency rates, and a trend toward a higher reintervention rate. This retrospective study brings into question the utility of stenting the CA artery. AUTHOR CONTRIBUTIONS Conception and design: SA, CS, TD Analysis and interpretation: SA, TD Data collection: SA, TD, RC, TM Writing the article: SA, TD Critical revision of the article: SA, CS, JP Final approval of the article: SA, CS, JP Statistical analysis: SA, TD Obtained funding: Not applicable Overall responsibility: SA, CS REFERENCES 1. Sarac TP, Altinel O, Kashyap V, Bena J, Lyden S, Sruvastava S, et al. Endovascular treatment of stenotic and occluded visceral arteries for chronic merenteric ischemia. J Vasc Surg 2008;47: Shaw RS, Maynard EP III. Acute and chronic thrombosis of the mesenteric arteries associated with alabsorption. N Engl J Med 1958;258: Atkins MD, Kwolek CJ, LaMuraglia GM, Brewster DC, Chung TK, Cambria RP. Surgical revascularization versus endovascular therapy for chronic mesenteric ischemia: a comparative experience. J Vasc Surg 2007;45: Sharafuddin MJ, Olson CH, Sun S, Kresowik TF, Corson JD. 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