Impact of Obesity on Robot-Assisted Distal Pancreatectomy

Abstract

Background:

Obesity has been steadily increasing in the United States. The effect of body mass index (BMI) on surgical outcomes in pancreatic surgery is still controversial. Currently, there is no report related to obesity and robotic pancreatic surgery. The purpose of this study was to evaluate the impact of BMI on the surgical outcomes of both nonobese and obese patients undergoing robot-assisted distal pancreatectomy (RADP).

Methods:

A prospectively collected database for RADP was retrieved for analysis. Patients were categorized as obese (BMI ≥30 kg/m²) and nonobese (BMI <30 kg/m²). Demographics, perioperative data, American Society of Anesthesiologists score, diagnosis, conversion rate, morbidity, surgical mortality, pancreatic fistula rate, and length of stay were compared.

Results:

A total for 85 RADP were included, with 57 (67%) in the nonobese group and 28 (33%) in the obese group. No differences were found between nonobese and obese patients regarding demographic, preoperative risk, and perioperative parameters and mortality. There was a trend in the obese group associated with a higher rate of postoperative complications, but it was statistically insignificant. Clinically significant pancreatic fistula (grade B) occurred in 28.5% of obese patients and in 7% of nonobese patients, but without statistical significance (P = .064).

Conclusions:

Obesity does not have a significant impact on the perioperative outcomes and surgical risks for patients undergoing RADP, but high BMI may be a predictor for pancreatic fistula after RADP.

Introduction

Obesity, with a body mass index (BMI) of >30 kg/m², has progressively become a public health problem in the western countries since the early 20th century. The World Health Organization (WHO) formally recognized obesity as a global epidemic in 1997.¹ Thereafter, the prevalence of obesity in the United States has been steadily increasing. Currently, it is estimated that about 72.5 million adults in the United States are obese.² It is also reported that treatment for obesity-related illnesses consumes 10% of all US healthcare expenditures.^3,4

The potential influence of obesity on surgical procedures has always been a topic of debate over the years. Many surgeons have the perception that obese patients may have increased technical challenges, which may be associated with higher postoperative complications.⁵ However, controversy still exists in current literature. Some authors reported obesity as a potential risk factor in patients undergoing complex intra-abdominal cancer surgery with increased incidence of postoperative complications, such as intra-abdominal infection and wound infection.^6,7 Others demonstrated that obesity alone was not a risk factor for perioperative morbidity or mortality.^8–10 Obesity and pancreatic surgeries have also been discussed in literature, with controversial findings in concern of the impact of BMI on many perioperative complications.^4,7,11–15 Obesity has been claimed to cause increased blood loss,^4,14 operative time,¹⁴ wound infection rate,^7,13 and pancreatic fistula rate^7,16–19; whereas others did not observe any negative effect on surgical outcomes.^11,14

Minimally invasive surgeries, including both laparoscopic and robotic approaches, have made significant advances in the surgical field in the past decade and have become the new era in the field of surgery with advantages of less blood loss, reduced postoperative pain, enhanced postoperative recovery, fewer complications, and early discharge in a variety of surgeries, compared with traditional open surgery.^20,21 Because the pancreas is deeply located in the retroperitoneal space with a complex connection with surrounding intra-abdominal organs, robot-assisted distal pancreatectomy (RADP) has also been increasingly used in recent years and shown to have superiority when compared to the laparoscopic approach.²²

Both the numbers of obese patients and robotic surgeries have been increasing worldwide, and to our knowledge, there is no literature report discussing the relationship between BMI and outcomes after RADP. The purpose of this study is to evaluate the impact of BMI on surgical outcomes by comparing the perioperative parameters and risks in both nonobese and obese patients undergoing RADP.

Methods

This is a retrospective study of data retrieved from a prospectively collected database for robotic surgery, as part of standard care. An institutional review board approved the study protocol and the retrospective review of medical records. All patients signed a consent form that allows review of their medical records for research purposes. All of the procedures were performed by the same surgeon (P.C.G.) at two different institutions. From January 2004 to March 2007, surgeries were performed at the Misericordia Hospital in Grosseto, Italy. From April 2007 to November 2013, surgeries were performed at the University of Illinois Hospital and Health Sciences System in the United States.

The cohort was divided by BMI according to the WHO definition of obese (BMI ≥30 kg/m²) and nonobese (BMI <30 kg/m²). Patients who failed to complete robotic surgery and required conversion or patients without BMI data available were excluded from this study. Demographics, perioperative data, American Society of Anesthesiologists (ASA) score, diagnosis, conversion rate, morbidity, surgical mortality, pancreatic fistula rate, and length of stay (LOS) were analyzed.

Conversion was referred to as the need to terminate the robotic surgery and convert to the open method. LOS was calculated from the date of surgery until the time of discharge. Surgical mortality was defined as death occurring within the first 30 postoperative days or before discharge from the hospital. All postoperative complications were classified using the Clavien–Dindo classification.²³ Pancreatic fistulas were identified and graded according to the International Study Group of Pancreatic Fistula (ISGPF).²⁴

The operative time was calculated as the time between skin incision and the last port skin closure. The times for exploratory laparoscopy, robotic setup, and docking, and any associated procedure needed were incorporated in the operative time as well. Diagnoses were categorized into benign, malignant, metastatic, and neuroendocrine tumor (NET) according to the pathological findings. Benign disease includes serous cystadenoma, mucinous cystadenoma, intraductal papillary mucinous neoplasm, chronic pancreatitis, lymphoepithelial cyst, and pseudocyst. Malignant tumors include pancreatic adenocarcinoma, intraductal papillary mucinous carcinoma, and mucinous cystadenocarcinoma. Metastatic lesions include tumors most commonly derived from renal cell carcinoma. Pancreatic NET is a special entity of neoplasm with malignant potential and could present a protracted clinical course, which is different to pancreatic adenocarcinoma, and therefore, a separated category was assigned for this neoplasm.

Statistical analysis

Statistical analysis was carried out by using PASW Statistics 18 (Statistic Package for Social Sciences; SPSS, Inc., Chicago, IL). Descriptive statistics were calculated by using mean ± standard error of mean, median, and frequencies as appropriate to the type of data. The Student's t test was used for comparison of the means of the two groups. Categorical variables were compared by the chi-square or Fisher's exact test. P values <.05 were considered significant.

Results

Demographics

Eighty-five patients underwent RADP with and without splenectomy. Among these patients, 57 (67%) were nonobese and 28 (33%) obese. The average BMI was 25.2 kg/m² with a range of 16.8–29.15 kg/m² for the nonobese patients and 33.3 kg/m² with a range of 30–46.7 kg/m² for the obese patients. There were no significant differences between the two groups with regard to age, sex, and the preoperative risk assessment according to the ASA classification system. The mean tumor size was 48.3 and 35.7 mm in the nonobese and obese patients, respectively (P = .07). There was no significant difference in the preoperative diagnosis and indication for surgery between the two groups (Table 1).

Table 1.

Demographics in Nonobese and Obese Patients Undergoing Robot-Assisted Distal Pancreatectomy

Variable	Total	Nonobese	Obese	P
N (%)	85	57 (67)	28 (33)
Age (mean)	56.66	56.33	57.32	.7746
BMI (mean)	27.9	25.2	33.3
Gender, n (%)
Male	24 (28.24)	16 (28.07)	8 (28.57)	.962
Female	61 (71.76)	41 (71.93)	20 (71.43)	.962
ASA risk, n (%)
I/II	53 (62.3)	40 (70.1)	13 (46.4)	.056
III/IV	32 (37.7)	17 (29.9)	15 (53.5)	.056
Tumor location
Body	25 (29.4)	15 (26.3)	10 (35.7)	.452
Tail	42 (49.4)	32 (56.1)	10 (35.7)	.104
Body-tail	18 (21.2)	9 (15.7)	9 (32.1)	.249
Tumor size, mean (SE)	43.09 (3.78)	48.36 (5.82)	35.75 (3.73)	.0727
Diagnosis
Benign	51 (60.00)	31 (54.39)	20 (71.43)	.132
Malignant	15 (17.65)	12 (21.05)	3 (10.71)	.240
Metastatic	3 (3.53)	1 (1.75)	2 (7.14)	.206
Neuroendocrine tumor	16 (18.82)	13 (22.81)	3 (10.71)	.180

ASA, American Society of Anesthesiologists; BMI, body mass index; N, number; SE, standard error.

Perioperative parameters

The perioperative parameters following distal pancreatectomy are described in Table 2. There was no difference observed in the rates of spleen preservation between the two different BMI groups. Four patients required conversion, with an overall conversion rate of 4%. The conversion rate was 5.3% in the nonobese group and 3.5% in the obese group (P = .71). The mean overall operation time of RADP was 252 minutes. There was no significant difference in the mean operative time between the two groups (252.1 versus 253.4 in the nonobese and obese patients; P = .9). The mean overall estimated blood loss was 216.3 mL, with 193 mL in the nonobese patients and 252 mL in the obese patients (P = .47). There was no significant difference seen in the mean hospital stay (9.8 versus 7.8 days, P = .14). The readmission rate was equal in the two groups (7%, P = 1.00).

Table 2.

Perioperative Parameters in Nonobese and Obese Patients Undergoing Robot-Assisted Distal Pancreatectomy

Variable	Total	Nonobese	Obese	P
N (%)	85	57	28
Procedure type
Spleen-preserving distal pancreatectomy, N (%)	41 (48.24)	26 (45.61)	15 (53.57)	.490
Distal pancreatectomy with splenectomy, N (%)	44 (51.76)	31 (54.39)	13 (46.43)	.490
Conversion, N (%)	4 (4.76)	3 (5.36)	1 (3.57)	.717
Operating time (minutes)	252.58	252.11	253.46	.9416
Blood loss (mL)	216.39	193.64	252.14	.4704
Hospital stay (days)	9.15	9.85	7.82	.1444
Readmission, N (%)	6 (7)	4 (7)	2 (7)	1.000

Postoperative outcomes

Postoperative outcomes are described in Table 3. Thirty-five percent of the nonobese patients and 60.7% of the obese patients experienced a postoperative complication (P = .02). Both minor and major complications were more frequent in the obese patients (26.3% and 8.7% versus 39.2% and 21.4%, respectively). However, this difference was not statistically significant (P = .4). When specific complications, such as pulmonary complications, intra-abdominal fluid collection, and deep vein thrombosis, were compared, there was no statistical difference between the two groups. A grade A postoperative pancreatic fistula developed in 17 patients (20%): 12 nonobese patients (21%) and 5 obese patients (17.8%), (P = .150). The clinically significant fistula rate (grade B) of the entire series was 14.1%. Four nonobese (7%) and eight obese patients (28.5%) developed a grade B fistula. This difference was not statistically significant (P = .06). There was no grade C fistula in either group and mortality rates were nil.

Table 3.

Complications in Nonobese and Obese Patients Undergoing Robot-Assisted Distal Pancreatectomy

Variable	Total	Nonobese	Obese	P
N	85	57	28
Clavien–Dindo classification, N (%)
Total	37 (43.5)	20 (35)	17 (60.7)	.023
Minor (I–II)	26 (30.5)	15 (26.3)	11 (39.2)	.495
Major (III–IV)	11 (12.9)	5 (8.7)	6 (21.4)	.495
Complications, N (%)
Pulmonary embolism	4 (4.7)	1 (1.7)	3 (10.7)	.223
Pneumonia	4 (4.7)	2 (3.5)	2 (7.1)	.916
ARDS	1 (1.1)	0	1 (3.5)	.916
Abdominal wall hematoma	3 (3.5)	3 (5.2)	0
Renal failure	1 (1.1)	0	1 (3.5)
Splenic vein thrombosis	4 (4.7)	1 (1.7)	3 (10.7)	.178
Intra-abdominal fluid collection	4 (4.7)	1 (1.7)	3 (10.7)	.257
UTI	4 (4.7)	1 (1.7)	3 (10.7)	.264
Seroma	4 (4.7)	1 (1.7)	3 (10.7)	.178
Chylous fistula	1 (1.1)	1 (1.7)	0
DVT	1 (1.1)	1 (1.7)	0
Pancreatic fistula grade, N (%)
No fistula	56 (65.8)	41 (71.9)	15 (53.5)	.817
A	17 (20)	12 (21)	5 (17.8)	.158
B	12 (14.1)	4 (7)	8 (28.5)	.064
C	0	0	0	—

ARDS, acute respiratory distress syndrome; DVT, deep vein thrombosis; UTI, urinary tract infection.

Discussion

Obesity is becoming one of the most important health issues in western countries with an estimate of more than $140 million in expenditures each year on obesity-related diseases in the United States.³ Consequently, due to the increased prevalence of obesity, it is important to have an understanding of how obesity could affect the care of patients. Minimally invasive surgery has brought about a new evolution in surgery with many advantages related to patient recovery.^20,21 The pancreas has always been one of the most challenging fields of abdominal surgery. Although mortality has been improved over the years, it is still associated with high morbidity.²⁵ The complexity of this procedure has lead to reluctance in using the laparoscopic approach in pancreatic surgery. Robotic technology emerged and brought several advantages to the minimally invasive techniques, which were not provided by laparoscopic surgery and thus has driven surgeons to take on the challenges associated with these procedures once again.^26,27 Although there have been published results concerning obesity in pancreatic surgery, most of them involve traditional open cases.^4,11–14 So far, only one article from Weber et al. has addressed the impact of BMI on laparoscopic distal pancreatectomy and stated that higher BMI was associated with major complications.¹⁵ There is currently no information about the impact of obesity in pancreatic surgery.

Our study evaluated patients undergoing RADP, comparing obese (BMI ≥30 kg/m²) and nonobese (BMI <30 kg/m²) groups. The demographic distributions were not different among the two cohorts. Recent meta-analyses on laparoscopic distal pancreatectomy demonstrated that the rate of conversion from laparoscopy to open procedure ranged from 9.2% to 11%.²⁰ Some even reported up to a 30% conversion rate.²² Our overall conversion rate is 4.7% with no difference observed between obese or nonobese patients. This result was consistent with our previously published data.²⁷ A comparative study between RADP and laparoscopic distal pancreatectomy (LDP) by Daouadi et al. also found that RADP had a significantly reduced rate of conversion (0% versus 16%, P < .05).²² However, there was criticism on the lower conversion rate of robotic surgery when compared to laparoscopic surgery, which might be due to selection bias toward easier cases for the newer robotic technique.²² Our study clearly demonstrated no selection bias on BMI, since all of the patients with indications for distal pancreatectomy were performed robotically. There are two potential reasons for this low conversion rate in our series. First, it may be attributed to the improvement of the constraints of laparoscopic surgery, such as increases in the range of motion and the three-dimensional (3D) visualization, which can improve a surgeon's dexterity and allow more meticulous dissection over the splenic vessels. Second, this study was based on a single experienced robotic surgeon's work, which may eliminate the learning curve that could incur on less experienced surgeons.

The overall mean operation time of RADP was 252 minutes and the mean blood loss was 216 mL, without significant differences among the obese and nonobese groups. These findings were consistent with those of other RADP series published by Cirocchi et al.^4,21 Although no available information could be found in the literature comparing the difference of surgical outcomes after RADP between obese and nonobese patients, there were comparative studies with conflicting results on obese and nonobese patients for other types of surgery. Mullen et al. found no difference in operative time and blood loss in a multi-institutional review of obesity and major oncological resections.^10,13

Two studies, one by William et al. and the other by Kodera et al. focusing on pancreaticoduodenectomy and obesity, found an increase in both operative time and blood loss among obese patients.^6,11,14,17 Yamada et al. found a significantly higher operative time in the obese group in both laparoscopic and open distal gastrectomy, with only a significant increase of blood loss in the obese patients who underwent open surgery.^24,28 This emphasizes the potential advantage of a minimally invasive approach in obese patients, which is demonstrated in our study with no difference in operative time and blood loss in robotic surgeries performed among the obese and nonobese groups.

In open surgery on an obese patient, the operative field may be a challenge to surgeons, with a potentially poor operative field due to the thick abdominal wall and excessive amount of fatty tissue. This disadvantage may be overcome by a minimally invasive approach, robotic or laparoscopic, due to the setting up of pneumoperitoneum, which can provide better exposure. In robotic surgery, the current advanced technology provides an enhanced vision with 3D images and articulated robotic arms with 360° movements. This allows the surgeon to carry out meticulous dissection. This will be very helpful in the obese patients especially, with well-developed omentum and accumulation of fat tissue around the visceral organs, which will not only impair the exposure of the operative field but also obscure anatomy structures to be identified during the operation.

In our study, the LOS and readmission rate in both groups were similar without statistical difference. These results were also comparable to other findings on the robotic approach in the literature.²² When looking at the obese and nonobese groups, most of the studies, including different types of pancreatic surgery and other intra-abdominal surgeries, had the same results with no differences in LOS in different BMI categories.^4,5,11,13 Only one study from Williams et al. showed a significantly longer postoperative stay after pancreaticoduodenectomy in obese patients, which was claimed to be contributed to increased postoperative complications.¹⁴

With regard to the Clavien–Dindo classification, there was no statistical difference between our two groups of patients, although obese patients seemed to have a trend toward developing more postoperative complications. There were variable results in the literature evaluating the effect of BMI on patients undergoing a variety of surgeries. Mullen et al. published a large study that collected data from 14 academic medical centers and evaluated the correlation of BMI on perioperative outcomes after a major intra-abdominal oncologic surgery. That study only included open procedures and showed no correlation of BMI with complications.¹³ Dindo et al. found that increasing BMI correlated with a higher risk of wound infection, but not with development of postoperative complications.¹⁰ However, there were also studies that showed that obesity was related to an increased risk of postoperative complications.^6,29

Few studies evaluated the effect of obesity on complications after pancreatic surgery, and even fewer with the laparoscopic or robotic approach. There is only one laparoscopic distal pancreatectomy study from Weber et al. that also used the Clavien–Dindo classification to evaluate complications. This study found that higher BMI was associated with major complications.¹⁵ Kelly et al. also reported an association of high BMI with morbidity.¹² Others studies focused mainly on the open approach and included both pancreaticoduodenectomy and distal pancreatectomy. Some revealed a positive association of obesity with increased complications, but one study from House et al. found this association to be related to visceral retrorenal fat instead of BMI.^4,7 In contrast, several studies in the literature concluded that the development of complications was not substantially different across all BMI groups.^3,11,14

We found an increased rate of pancreatic fistula in the obese group, which was consistent with other reports.^15,16,30 In our series, the obese patients had a higher rate of grade B pancreatic fistula (28.5% versus 7%), even though this result did not reach statistical significance (P = .064). This may be related to an increased percentage of fatty tissue infiltrated in the obese patient. Studies reported an association of increased BMI with increased fat infiltration, and House et al. specifically focused on retrorenal visceral fat thickness that correlated with a higher rate of pancreatic fistula.^7,16–19 All patients who had intra-abdominal fluid collection were obese patients with grade B pancreatic fistula, except one nonobese patient with BMI of 29 kg/m², which would be classified as overweight by the WHO classification. Therefore, high BMI might be a predictor for pancreatic fistula and intra-abdominal fluid collection.

Conclusions

In conclusion, our study demonstrated that RADP could be safely performed in obese patients with a low conversion rate. Higher BMI was associated with higher rates of pancreatic fistula and intra-abdominal abscess, which may be a reflection of fatty infiltration in the pancreas. However, RADP could provide comparable results for both obese and nonobese patients in terms of perioperative outcomes, including operative time, blood loss, hospital stay, and other surgical risks. Therefore, obesity is not necessarily related to poor outcomes in pancreatic surgery and the minimally invasive approach, such as RADP, should be encouraged for obese patients in the future.

Footnotes

Acknowledgments

S.W. and D.D. had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. The Department of Surgery has a Proctoring Agreement and Grant Support with Intuitive Surgical.

Disclosure Statement

S.W., D.D., M.A.M., K.P., and F.M.B. have no conflicts of interest to disclose. P.C.G. is a consultant for Covidien.

References

Caballero

. The global epidemic of obesity: An overview. Epidemiol Rev, 2007; 29:1–5.

Centers for Disease Control and Prevention (CDC). Vital signs: State-specific obesity prevalence among adults—United States, 2009. MMWR Morb Mortal Wkly Rep, 2010; 59:951–955.

Del Chiaro

, Rangelova

, Ansorge

, et al. Impact of body mass index for patients undergoing pancreaticoduodenectomy. World J Gastrointest Pathophysiol, 2013; 4:37–42.

Benns

, Woodall

, Scoggins

, et al. The impact of obesity on outcomes following pancreatectomy for malignancy. Ann Surg Oncol, 2009; 16:2565–2569.

Melis

, Weber

, Shridhar

, et al. Body mass index and perioperative complications after oesophagectomy for adenocarcinoma: A systematic database review. BMJ Open, 2013; 3:pii: e001336.

Kodera

, Ito

, Yamamura

, et al. Obesity and outcome of distal gastrectomy with D2 lymphadenectomy for carcinoma. Hepatogastroenterology, 2004; 51:1225–1228.

House

, Fong

, Arnaoutakis

, et al. Preoperative predictors for complications after pancreaticoduodenectomy: Impact of BMI and body fat distribution. J Gastrointest Surg, 2008; 12:270–278.

Thomas

, Goldman

, Mangione

, et al. Body mass index as a correlate of postoperative complications and resource utilization. Am. J. Med, 1997; 102:277–283.

Klasen

, Junger

, Hartmann

, et al. Increased body mass index and peri-operative risk in patients undergoing non-cardiac surgery. Obes Surg, 2004; 14:275–281.

10.

Dindo

, Muller

, Weber

, et al. Obesity in general elective surgery. Lancet, 2003; 361:2032–2035.

11.

Balentine

, Enriquez

, Cruz

, et al. Obesity does not increase complications following pancreatic surgery. J Surg Res, 2011; 170:220–225.

12.

Kelly

, Greenblatt

, Wan

, et al. Risk stratification for distal pancreatectomy utilizing ACS-NSQIP: Preoperative factors predict morbidity and mortality. J Gastrointest Surg, 2011; 15:250–259; discussion 259–261.

13.

Mullen

, Davenport

, Hutter

, et al. Impact of body mass index on perioperative outcomes in patients undergoing major intra-abdominal cancer surgery. Ann Surg Oncol, 2008; 15:2164–2172.

14.

Williams

, Rosato

, Kennedy

, et al. Impact of obesity on perioperative morbidity and mortality after pancreaticoduodenectomy. J Am Coll Surg, 2009; 208:210–217.

15.

Weber

, Cho

, Merchant

, et al. Laparoscopic left pancreatectomy: Complication risk score correlates with morbidity and risk for pancreatic fistula. Ann Surg Oncol, 2009; 16:2825–2833.

16.

Ramsey

, Martin

. Body mass index and outcomes from pancreatic resection: A review and meta-analysis. J Gastrointest Surg, 2011; 15:1633–1642.

17.

Noun

, Riachy

, Ghorra

, et al. The impact of obesity on surgical outcome after pancreaticoduodenectomy. JOP, 2008; 9:468–476.

18.

Rosso

, Casnedi

, Pessaux

, et al. The role of “fatty pancreas” and of BMI in the occurrence of pancreatic fistula after pancreaticoduodenectomy. J Gastrointest Surg, 2009; 13:1845–1851.

19.

Gaujoux

, Cortes

, Couvelard

, et al. Fatty pancreas and increased body mass index are risk factors of pancreatic fistula after pancreaticoduodenectomy. Surgery, 2010; 148:15–23.

20.

Nigri

, Rosman

, Petrucciani

, et al. Metaanalysis of trials comparing minimally invasive and open distal pancreatectomies. Surg Endosc, 2011; 25:1642–1651.

21.

Cirocchi

, Partelli

, Coratti

, et al. Current status of robotic distal pancreatectomy: A systematic review. Surg Oncol, 2013; 22:201–207.

22.

Daouadi

, Zureikat

, Zenati

, et al. Robot-assisted minimally invasive distal pancreatectomy is superior to the laparoscopic technique. Ann Surg, 2013; 257:128–132.

23.

Dindo

, Demartines

, Clavien

P-A

. Classification of surgical complications. Ann Surg, 2004; 240:205–213.

24.

Bassi

, Dervenis

, Butturini

, et al. Postoperative pancreatic fistula: An international study group (ISGPF) definition. Surgery, 2005; 138:8–13.

25.

Cameron

, Riall

, Coleman

, et al. One thousand consecutive pancreaticoduodenectomies. Ann Surg, 2006; 244:10–15.

26.

Hanly

, Talamini

. Robotic abdominal surgery. Am J Surg, 2004; 188,(4A Suppl):19s–26s.

27.

Giulianotti

, Sbrana

, Bianco

, et al. Robot-assisted laparoscopic pancreatic surgery: Single-surgeon experience. Surg Endosc, 2010; 24:1646–1657.

28.

Yamada

, Kojima

, Inokuchi

, et al. Effect of obesity on technical feasibility and postoperative outcomes of laparoscopy-assisted distal gastrectomy—Comparison with open distal gastrectomy. J Gastrointest Surg, 2008; 12:997–1004.

29.

Lee

, Dunn

, Chen

, et al. Impact of body mass index on radical cystectomy. J Urol, 2004; 172:1281–1285.

30.

Ferrone

, Warshaw

, Rattner

, et al. Pancreatic fistula rates after 462 distal pancreatectomies: Staplers do not decrease fistula rates. J Gastrointest Surg, 2008; 12:1691–1697; discussion 1697–1698.