Annals of Vascular Surgery
Volume 23, Issue 6 , Pages 770-777, November 2009

The Impact of Aortic Clamping Site on Glomerular Filtration Rate after Juxtarenal Aneurysm Repair

  • Massimiliano M. Marrocco-Trischitta

      Affiliations

    • Department of Vascular Surgery, San Raffaele Scientific Institute, Università Vita-Salute, San Raffaele, Milan, Italy
    • Corresponding Author InformationCorrespondence to: Massimiliano M. Marrocco-Trischitta, MD, PhD, Vascular Surgery, San Raffaele Scientific Institute, Via Olgettina, 60, 20132 Milan, Italy
  • ,
  • Germano Melissano

      Affiliations

    • Department of Vascular Surgery, San Raffaele Scientific Institute, Università Vita-Salute, San Raffaele, Milan, Italy
  • ,
  • Andrea Kahlberg

      Affiliations

    • Department of Vascular Surgery, San Raffaele Scientific Institute, Università Vita-Salute, San Raffaele, Milan, Italy
  • ,
  • Giuseppe Vezzoli

      Affiliations

    • Department of Nephrology and Dialysis Unit, San Raffaele Scientific Institute, Università Vita-Salute, San Raffaele, Milan, Italy
  • ,
  • Giliola Calori

      Affiliations

    • Statistical Unit, San Raffaele Scientific Institute, Università Vita-Salute, San Raffaele, Milan, Italy
  • ,
  • Roberto Chiesa

      Affiliations

    • Department of Vascular Surgery, San Raffaele Scientific Institute, Università Vita-Salute, San Raffaele, Milan, Italy

published online 21 July 2009.

Article Outline

Background

Open repair of juxtarenal abdominal aortic aneurysms (JAAAs), which necessitates clamping above one (interrenal clamping, interRC) or both renal arteries (suprarenal clamping, supraRC), is associated with an increased risk of perioperative renal derangements. We reviewed our experience to investigate the impact of aortic clamping site during JAAA repair on peri- and postoperative glomerular filtration rate (GFR).

Methods

Between January 2001 and March 2006, 32 patients (28 male, four female; mean age 70.5±5.6 years) were submitted to elective open repair of JAAA. SupraRC was required in 12 patients and performed with cold renal perfusion (CRP) in five cases; interRC was required in 20 and performed with CRP in eight. GFRs were estimated through postoperative day 4 using the Cockcroft-Gault equation and compared to those of concurrent controls undergoing infrarenal AAA repair, matched 1:1 by gender, age, aneurysm size, preoperative GFR, and left renal vein management. GFR values were also evaluated and compared between groups at a mean follow-up of 29.0±23.7 months. Renal dysfunction was defined as a decrease of GFR ≥20%. Statistics were determined as appropriate for the variables of interest.

Results

No perioperative mortality was recorded and no differences in major complication rates were observed between groups (p=0.16). Operative time was longer in JAAA patients (154±47 vs. 132±41min, p=0.019). Mean renal ischemia time was 16.7±7.7min. Postoperatively, GFR values up to day 4 were significantly worse in JAAA patients compared to controls (p=0.0007), with a fourfold risk of renal dysfunction at postoperative day 4 (34% vs. 9%, odds ratio [OR]=4.44, 95% confidence interval [CI] 1.1-18.1; p=0.029). At univariate analysis, supraRC was found to be the only factor associated with perioperative renal dysfunction (OR=11.3, 95% CI 2.0-63.1; p=0.003). At follow-up, two patients with supraRC died and another two required dialysis permanently. When compared to those with interRC or infrarenal clamping, patients with supraRC showed a persistent renal dysfunction at follow-up (p=0.005).

Conclusion

Elective JAAA repair with renal ischemia time ≤30min is safe, but supraRC entails a significant perioperative and mid-term GFR reduction. In contrast, interRC provides results similar to those obtained after infrarenal AAA repair, allowing postoperative recovery of renal function to preoperative values.

 

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Introduction 

Juxtarenal abdominal aortic aneurysms (JAAAs) are defined as those that extend up to, without including, the renal arteries but require clamping above one or both renal arteries during surgical repair.1 However, in the endovascular era, JAAAs are most commonly described as infrarenal aneurysms (AAAs) with an inadequate proximal neck for stent-graft exclusion.2 Endovascular repair of JAAA has been reported to be feasible with fenestrated customized devices.3 Nevertheless, until the encouraging initial results obtained by a few centers4 are reproduced in common clinical practice, open surgery remains the treatment of choice.

JAAA repair is associated with increased mortality and morbidity rates, with renal failure being the most common complication.1 Proximal clamping time and location have been previously investigated as determinants of postoperative outcome,1, 5, 6, 7, 8, 9 but controversial results have been reported due to methodological differences among the studies, including patient and control selection and the choice of the renal failure definition10 and index. Dialysis requirement is an inaccurate end point due to its low incidence rate,6 and serum creatinine, though specific, is in fact an insensitive marker of renal deterioration, particularly in cases of mild to moderate degrees of renal dysfunction that may remain unrevealed.11 Glomerular filtration rate (GFR) is the best overall measure of kidney function currently available12 and was found to be a much more powerful prognostic factor than serum creatinine alone in patients with abdominal11 and thoracic aortic aneurysmal disease.13

During JAAA elective repair, an aortic clamp level distal to the origin of the superior mesenteric artery (suprarenal clamping, supraRC) has been associated with significant decreases in mortality and renal morbidity rates compared to supravisceral clamping.1, 5 Yet, even in such a setting, postoperative renal insufficiency rates remain as high as 28.3%, with an incidence of permanent dialysis dependence of 5.8%.5

Theoretically, whenever technically feasible, an even lower level for aortic cross-clamping—namely between the renal arteries (interrenal clamping, interRC)—should further reduce the risk of postoperative renal derangements, providing the maintenance of blood perfusion to one kidney. In fact, this maneuver has been reported to increase the risk of renal complications, possibly due to renal atheroembolization.14 Also, the clamp may cause a mechanical distortion of the aorta, compromising the flow through the more proximal renal artery. The aim of our study was to analyze the impact of proximal aortic clamping level on peri- and postoperative GFR after elective JAAA open repair.

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Methods 

A retrospective analysis was conducted on a prospectively compiled computerized database of all patients submitted to abdominal aortic surgery at our center between January 2001 and March 2006. A total of 32 patients underwent elective open repair of a JAAA. There were 28 men and four women, with a mean age of 70.5±5.6 years. Surgery was performed through a transperitoneal approach, and intravenous heparin (70IU/kg) was administered before perirenal aortic dissection. Selective clamping of the renal arteries was performed in all cases prior to aortic clamp placement, to reduce the risk of embolization. Mannitol and furosemide were administrated intravenously before renal cross-clamping and upon reperfusion. SupraRC was performed in 12 cases and interRC in 20. Proximal clamping site was decided based on both preoperative computed tomographic (CT) assessment and intraoperative findings. Renal perfusion with a cold crystalloid solution (mannitol 18% 70mL and 6-methylprednisolone 500mg in Ringer 4°C 500mL) employing 9F balloon-tip Pruitt irrigation catheters15 was instituted in five of the former and eight of the latter. This procedure was performed at the discretion of the surgeon. Aortic reconstruction was performed with Dacron graft interposition, and proximal and distal anastomoses were made in an end-to-end fashion. Twenty-seven patients had an aortoaortic, four had an aortobi-iliac, and one had an aortobifemoral reconstruction. In order to improve proximal exposure, left renal vein (LRV) division was performed in six cases (18.8%); and in one patient it was found to be occluded. In the other five patients, the LRV was reconstructed by direct reanastomosis after the aortic anastomoses were completed and clamps were released. Collateral branches were preserved during LRV mobilization and retraction. Thirty-two matched controls were randomly identified from the database among concurrent 1,189 patients submitted to infrarenal AAA open repair. Matching was by gender, age (±5 years), AAA diameter (±5mm), preoperative GFR (±10mL/dL/1.73m2), type of aortic reconstruction, and management of the LRV (five cases of division and reconstruction and one case of division of an occluded vein16).

Patient groups were stratified by preoperative risk factors including diabetes, tobacco use, hypertension, and hyperlipidemia using a simplified grading system according to the Society for Vascular Surgery Suggested Reporting Standards;17 by perioperative cardiac risk, according to the Goldman's Revised Cardiac Risk Index (RCRI);18 and by stages of chronic kidney disease (CKD), according to the National Kidney Foundation guidelines19 (Table 1).

Table 1. Comparison of patient demographics and preoperative risk factors
JAAA, n (%)Controls, n (%)pa
Overall3232
Gender
Male28 (87.5)28 (87.5)1.0
Age (years), mean±SD70.4±5.670.8±6.00.82
AAA diameter, mean±SD (mm)59.1±15.159.7±16.00.96
Preoperative serum creatinine, mean±SD (mg/dL)1.14±0.441.22±0.400.21
Preoperative GFR, mean±SD (mL/dL/1.73m2)b65.9±23.767.9±20.70.72
Stage 1 (GFR ≥90)5 (15.6)3 (9.4)0.64
Stage 2 (GFR 60-89)14 (43.8)16 (50.0)
Stage 3 (GFR 30-59)12 (37.5)13 (40.6)
Stage 4 (GFR 15-29)1 (3.1)0 (0.0)
Stage 5 (GFR <15 or dialysis)0 (0.0)0 (0.0)
Body mass index, mean±SD26.8±3.128.3±3.30.07
Revised Cardiac Risk Indexc
I (0.5%)0 (0.0)0 (0.0)0.77
II (1.3%)17 (53.1)19 (59.4)
III (3.6%)9 (28.1)9 (28.1)
IV (9.1%)6 (18.8)4 (12.5)
Hypertension
0 (diastolic <90mm Hg)5 (15.6)5 (15.6)0.95
1 (easily controlled, single drug)9 (28.1)11 (34.4)
2 (requires two drugs)13 (40.7)12 (37.5)
3 (more than two drugs or uncontrolled)5 (15.6)4 (12.5)
Diabetes
0 (none)24 (74.0)25 (78.1)0.25
1 (adult onset, no insulin)5 (15.6)6 (18.8)
2 (adult onset, insulin-controlled)3 (9.4)0 (0.0)
3 (juvenile onset)0 (0.0)1 (3.1)
Smoking
0 (none or abstinence >10 years)9 (28.1)9 (28.1)0.78
1 (none currently, abstinence 1-10 years)12 (37.5)15 (46.9)
2 (current, <1 pack/day or abstinence >1 year)7 (21.9)6 (18.7)
3 (current 1 ≥ pack/day)4 (12.5)2 (6.3)
Hyperlipidemia
0 (cholesterol and triglycerides within normal limits for age)21 (65.6)24 (75.0)0.46
1 (mild elevation, diet-controlled)1 (3.1)2 (6.3)
2 (type II, III, or IV requiring strict diet control)0 (0.0)0 (0.0)
3 (requires drug control)10 (31.3)6 (18.7)
Pulmonary statusd
022 (68.7)21 (65.6)0.73
17 (21.9)9 (28.1)
22 (6.3)2 (6.3)
31 (3.1)0 (1.8)

aFisher's exact test or χ2 test for categorical data, unpaired t-test or Mann-Whitney test for continuous data.

bStages of chronic kidney disease: 1, kidney damage with normal or↑GFR; 2, kidney damage with mild ↓GFR; 3, moderate ↓GFR; 4, severe ↓GFR; 5, kidney failure.

cMajor cardiac complication rates.

dPulmonary status (PFTs=pulmonary function tests; VC=vital capacity; FEV1,=forced expiratory volume in 1 sec): 0, asymptomatic, normal chest X-ray film, PFTs 20%; 1, mild dyspnea on exertion or mild X-ray parenchymal changes, PFTs 65-80%; 2, between 1 and 3; 3, VC <1.85, L, FEV1<1.2 L or <35%, pCO2>45mm Hg, pulmonary hypertension.

Morbidity and mortality were recorded. Normal serum creatinine was defined as ≤1.5mg/dL. Myocardial infarction was suggested by electrocardiographic changes and confirmed by elevation of cardiac enzymes, regardless of symptoms. Respiratory failure was defined as ventilator dependence of >72hr, need for postoperative reintubation, clinical data or culture confirmation of pneumonia, or the need for tracheostomy.1 Ileus was defined as a delay in gut motility lasting >72hr after surgery.

Operative times, estimated blood loss, and hospital length of stay were recorded. Clinical follow-up, including serum creatinine and weight measurements, was performed after 6 months and thereafter annually.

GFR was estimated by using the Cockcroft-Gault equation:19, 20 (140 - age)×weight/72 × serum creatinine (where age is in years, actual body weight is in kilograms, and serum creatinine is in milligrams per deciliter; for women, the equation is multiplied by 0.85).

Patients with JAAA were first analyzed and compared to matched controls with infrarenal AAA in terms of demographics and preoperative risk factors (Table 1), perioperative variables (Table 2), and perioperative renal dysfunction, defined as a decrease >20% in GFR (Table 3). GFR values and trend up to day 4 after surgery were also calculated and compared (Fig. 1). Among JAAA patients, supraRC and interRC subgroups were also comparable in terms of pre- and perioperative risk factors and specifically renal clamping time (15.8±8.2 vs. 18.1±6.7min, p=0.435).

Table 2. Comparison of perioperative variables of interest
JAAA, n (%)Controls, n (%)pa
Total operative time, mean±SD (min)154.5±46.8132.2±41.40.019
Aortic proximal clamping time, mean±SD (min)16.7±7.715.1±5.90.346
Estimated blood loss, mean±SD (mL)117.5±191.2150.6±214.90.806
Hospital length of stay, mean±SD (days)6.8±3.15.7±1.40.390
Major complications
Total12 (37.5)6 (18.7)0.164
Renal insufficiencyb3 (9.4)2 (6.3)
Myocardial infarction3 (9.4)0 (0.0)
Respiratory failure4 (12.5)4 (12.5)
Bleeding1 (3.1)0 (0.0)
Ileus1 (3.1)0 (0.0)

aFisher's exact test or χ2 test for categorical data, unpaired t-test or Mann-Whitney test for continuous data.

bSerum creatinine increase >30% or >2.0mg/dL.

Table 3. Perioperative renal dysfunction after JAAA vs. AAA repair
JAAA, n (%)AAA, n (%)OR95% CIpa
Renal dysfunctionb11 (34.4)3 (9.4)4.41.1-18.10.029

aFisher's exact test.

bDecrease >20% in GFR at postoperative day 4.

  • View full-size image.
  • Fig. 1 

    Variations of GFR values at different postoperative (P.O.) times. Within-factor effect (time) F4,59=7.15, p<0.0001; between-factor effect (group) F1,62=3.30, p=0.074; group × time interaction F4,59=5.58, p=0.0007.

In JAAA patients the influence of supraRC vs. interRC on perioperative renal dysfunction was investigated, along with other risk factors including preoperative GFR, renal ischemia time, and renal cold perfusion (Table 4).

Table 4. Univariate analysis of risk factors for perioperative renal dysfunctiona in patients with JAAA
VariablePatients, n (%)Renal dysfunction (%)OR95% CIpb
Overall32 (100.0)11 (34.4)
Preoperative GFR (mL/dL/1.73m2)
<6013 (40.6)5 (38.5)1.30.3-5.90.687
6019 (59.4)6 (31.6)
Renal ischemia time (min)
1516 (50.0)6 (37.5)1.30.3-5.70.710
<1516 (50.0)5 (31.3)
Renal cold perfusion
Yes13 (40.6)7 (63.6)4.40.9-20.60.124
No19 (59.4)4 (36.4)
Clamping site
Suprarenal12 (37.5)8 (66.7)11.32.0-63.10.003
Interrenal20 (62.5)3 (15.0)

aDecrease >20% in GFR at postoperative day 4.

bχ2 test or Fisher's exact test.

Finally, GFR variations at follow-up associated with supraRC, interRC, and infraRC were compared (Table 5).

Table 5. Impact of proximal aortic clamping site on GFR variations at follow-up
SuprarenalInterrenalInfrarenalp
ΔGFRa at follow-up
Median % (I, III quartile)−31.6 (−48.9, −22.7)−3.7 (−12.9, +8.0)−6.5 (−17.6, +13.0)0.005
Suprarenal vs. infrarenal <0.05b
Suprarenal vs. interrenal <0.05b
Interrenal vs. infrarenal NSb

aΔGFR, variation of glomerular filtration rate expressed as percent decrease of preoperative value.

bDunn's test.

Statistical Analysis 

Results were analyzed using Fisher's exact test or χ2 test for categorical data, unpaired t-test or Mann-Whitney test for continuous data as appropriate. Perioperative GFR trend with time was compared between JAAA patients and controls using two-way analysis of variance for repeated measures with one within-factor and one between-factor (respectively, time and group), as previously described elsewhere.16 Only in the study group (i.e., JAAA) were standard univariate analyses performed to produce frequency distributions for the variables of interest and to estimate cumulative incidence of the risk of a decrease >20% in GFR at postoperative day 4 versus preoperative values. Variation of GFR between follow-up and preoperative values, expressed as a percentage of the latter, were calculated and compared between three groups (supraRC, interRC, and infraRC) using the Kruskal-Wallis test. Dunn's test was then used for post-hoc analysis. All analyses were run using the software SAS System 8.02 (SAS Institute, Cary, NC).

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Results 

Analysis of demographics and risk factors not included among the matching criteria showed JAAA patients and controls to be overall comparable (Table 1).

No perioperative mortality was recorded in JAAA or AAA patients, and no differences in major complication rates were observed between the groups (Table 2). Operative time was longer in JAAA patients (154±47 vs. 132±41min, p=0.019). Mean renal ischemia time was 16.7±7.7min.

At postoperative day 4, mean GFR variation compared to baseline was -12.1±24.9% in JAAA patients and +3.7±19.1% (p=0.006) in controls. The trend of GFR up to postoperative day 4 was significantly different in the two groups (p=0.0007, Fig. 1), with a fourfold risk of renal dysfunction at postoperative day 4 in the JAAA group (p=0.029, Table 3).

In JAAA patients, at univariate analysis (Table 4), only supraRC was found to be a significant predictor of perioperative renal dysfunction (odds ratio [OR]=11.3, 95% confidence interval [CI] 2.0-63.1; p=0.003).

At a mean follow-up of 29.0±23.7 months, overall survival was 95.3% (61/64). No aneurysm-related death was recorded. Two patients of the study group, with 59 and 55mm aneurysms, respectively, required dialysis permanently. Both had a preoperative GFR <60mL/dL/1.73m2, required a supraRC with renal cold perfusion, had relatively longer renal ischemia time (29 and 30min, respectively), and developed a severe perioperative renal dysfunction, with GFR reductions at day 4 of 65.7% and 70.3%, respectively. LRV was left intact in both cases.

GFR values were available in 55 of the survivors. Comparison of relative GFR decrease at follow-up (Table 5) revealed a significant impact of proximal clamping site (p=0.005). At post-hoc analysis, patients with supraRC showed a greater decrease compared to those with interRC (p<0.05) and infraRC (p<0.05), whereas patients with interRC did not differ from those with infraRC.

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Discussion 

Our results confirm the safety of elective JAAA repair in terms of perioperative morbidity and mortality when associated with proximal clamping time <30min.5, 6, 7 However, the impact of aortic clamping site was of paramount importance. SupraRC was confirmed to be associated with an increased risk of perioperative renal dysfunction. Even more importantly, at mid-term follow-up patients with supraRC showed a persistent and significant reduction of GFR values, whereas those with interRC had no permanent deterioration of renal function, similar to patients submitted to infrarenal AAA repair. Hence, in contrast to previous findings,14 our results imply that interRC can safely maintain an adequate intraoperative renal perfusion, even though no direct assessment of contralateral renal artery patency or atheroembolism was performed in this study.

In an elective setting, interRC can be planned preoperatively by means of an adequate diagnostic work-up, and it was found to be feasible intraoperatively in a considerable number of patients. Anatomical studies based on spiral CT showed that the renal arteries do not originate from the aorta at the same level in 50% of cases, with a mean distance between the two ostia of 8mm and a maximum distance of 54mm.21 Also, the right renal artery usually originates from the anterolateral aorta, with an angle that varies from -10° to 55° (mean +24°); and the left arises from the posterolateral aorta, with an angle that varies from +30 to -55 (mean -11°).21 Importantly, however, the presence of significant thrombus should be held as a contraindication to interRC. In this respect, for adequate and consistent grading we believe that the score proposed by Chaikof et al.22 for endovascular aneurysm repair could be also used in surgical patients.

In patients undergoing JAAA repair, preoperative abnormal renal function is also a well-known determinant of postoperative insufficiency.5, 6, 7 In our series, however, preoperative GFR did not reach statistical significance, possibly due to the low incidence rate of renal derangements (type II error).

During elective surgery, we do not routinely employ supravisceral clamping to avoid the associated hemostatic23 and cardiac24 alterations and the risk of visceral ischemia, unless its use is mandated by the involvement of perirenal aorta with significant atherosclerosis and thrombus or the proximity of the superior mesenteric artery.5, 7 Supravisceral clamping has been initially recommended and even found safer than supraRC in terms of renal morbidity;8, 9, 14 however, later studies have concluded the opposite.5, 7 This disagreement, in addition to some methodological bias in the former reports,7 is likely related to more accurate and safer planning of surgical exposure and aortic clamping level allowed by the recent improvements of preoperative imaging modalities.5 The lesson learned from Green et al.8 is that incorrect selection of proximal clamping site and intraoperative repositioning of the clamp entail greater risk of atheroembolic complications.7 To avoid such complications, we also routinely clamp the renal arteries before proximal suprarenal cross-clamping.

A debated issue in the surgical management of JAAA is the use of renal hypothermia. This has been shown to reduced the incidence of renal complications during thoracoabdominal aortic aneurysm repair.25 However, in patients with JAAA a selective rather than routine use of cold renal perfusion has been suggested in cases of either preoperative renal insufficiency or expected renal ischemia >30min.26 Of note, this maneuver is not without risks and may cause renal artery dissection and embolization. We suggest its use only if renal artery cannulation appears to be easily and rapidly feasible as an expeditious completion of proximal anastomosis appears of even greater importance. In our series, renal hypothermia did not result in improved postoperative renal function. However, no thorough conclusions can be drawn due to the limited renal ischemia time, which did not exceed 30min in any case, and the selection bias in the use of cold perfusions.

Finally, controversies persist regarding the management of the LRV.16 Some authors showed a significant renal detriment from LRV ligation,1, 27, 28 whereas others reported a low incidence of postoperative renal derangements and therefore found routine LRV reanastomosis unnecessary in case of adequate collateral circulation.29, 30 We believe that, whenever deemed useful, deliberate LRV division allows a safer proximal aortic control, particularly during interRC. As the occurrence of renal venous hypertension seems unpredictable, we find it unnecessary to take the chance and suggest a routine reconstitution of LRV anatomical continuity, by either direct reanastomosis or interposition of an expanded polytetrafluoroethylene graft. We previously showed this maneuver to be feasible without significantly lengthening operative time or increasing complication rates.16

We recognize several limitations of our study, including the use of GFR estimations related to the retrospective fashion of the study. However, previous studies showed that GFR calculated with the Cockcroft-Gault equation using the preoperative patient weight represents a surrogate measure of perioperative renal function that can be used in clinical trials.31, 32 Also, our study presents a relatively small number of patients, which accounts for some wide confidence intervals in the statistical tests. Yet, our analysis provided useful information that led us to modify our current surgical strategy.

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Conclusions 

In an elective setting, supraRC appears safe when associated with reduced renal ischemia (<30min) but entails a permanent renal detriment that warrants an ad-hoc long-term follow-up. InterRC maintains preoperative renal function and provides results similar to those obtained after infrarenal AAA repair. Hence, we recommend a routine, accurate preoperative imaging study of the perirenal aorta to assess whether this maneuver is technically feasible, particularly in patients with renal insufficiency. LRV division and reconstruction should be held as a safe maneuver to improve proximal aortic neck exposure. Selective clamping of the renal arteries prior to aortic clamp placement may reduce the risk of embolization.

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 Presented at the XXII Annual Meeting of the Societè de Chirurgie Vasculaire de Lingue Francaise, Lyon, France, June 2-5, 2007.

PII: S0890-5096(09)00086-7

doi:10.1016/j.avsg.2009.04.002

Annals of Vascular Surgery
Volume 23, Issue 6 , Pages 770-777, November 2009