Prospective Study Open Access
Copyright ©The Author(s) 2015. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Surg. Oct 27, 2015; 7(10): 261-266
Published online Oct 27, 2015. doi: 10.4240/wjgs.v7.i10.261
Obese patients have similar short-term outcomes to non-obese in laparoscopic colorectal surgery
Manish Chand, Henry D De’Ath, Muhammed Siddiqui, Chetanya Mehta, Shahnawaz Rasheed, James Bromilow, Tahseen Qureshi, Department of Surgery, Poole General Hospital, Poole BH15 2JB, United Kingdom
Author contributions: All authors contributed to this manuscript.
Institutional review board statement: This study has been reviewed and approved by the Colorectal Department of Poole General Hospital.
Clinical trial registration statement: N/A.
Informed consent statement: N/A.
Conflict-of-interest statement: None of the authors have any conflict of interest.
Data sharing statement: N/A.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Correspondence to: Manish Chand, Laparoscopic Fellow in GI Surgery, Department of Surgery, Poole General Hospital, Longfleet Road, Poole BH15 2JB, United Kingdom. mans001@aol.com
Telephone: +44-1202-442323
Received: April 5, 2015
Peer-review started: April 7, 2015
First decision: July 17, 2015
Revised: July 19, 2015
Accepted: August 20, 2015
Article in press: August 21, 2015
Published online: October 27, 2015

Abstract

AIM: To determine whether obese patients undergoing laparoscopic surgery within an enhanced recovery program had worse short-term outcomes.

METHODS: A prospective study of consecutive patients undergoing laparoscopic colorectal resection was carried out between 2008 and 2011 in a single institution. Patients were divided in groups based on body mass index (BMI). Short-term outcomes including operative data, length of stay, complications and readmission rates were recorded and compared between the groups. Continuous data were analysed using t-test or one-way Analysis of Variance. χ2 test was used to compare categorical data.

RESULTS: Two hundred and fifty four patients were included over the study period. The majority of individuals (41.7%) recruited were of a healthy weight (BMI < 25), whilst 50 patients were classified as obese (19.6%). Patients were matched in terms of the presence of co-morbidities and previous abdominal surgery. Obese patients were found to have a statistically significant difference in The American Society of Anesthesiologists grade. Length of surgery and intra-operative blood loss were no different according to BMI.

CONCLUSION: Obesity (BMI > 25) does not lead to worse short-term outcomes in laparoscopic colorectal surgery and therefore such patients should not be precluded from laparoscopic surgery.

Key Words: Laparoscopic surgery, Colorectal cancer, Obese: body mass index, Outcomes

Core tip: Laparoscopic colorectal surgery for cancer can be safely performed in obese patients without an increase in adverse events or outcomes. Patients should not be precluded from laparoscopy in such cases based on their body mass index. However it is important for the team to assess patients pre-operatively to decide on whether additional or more intensive peri-operative care is needed to ensure optimal outcomes.



INTRODUCTION

Obesity is a considerable and growing healthcare concern, and more patients treated for colorectal cancer are obese with a body mass index (BMI) of greater than 30. Historically, individuals with an increased BMI have been thought of as having a higher risk of poorer outcomes following surgery with an increased rate of peri-operative complications and longer hospital stays, however more recent studies have challenged this view[1-3].

The surgical management of colorectal cancer has shifted towards a minimally-invasive approach and the current expectation is that the majority of patients should undergo laparoscopic surgery. It is now recognised as a safe and more advantageous alternative to laparotomy for most patients as benefits include reduced morbidity and shorter hospital stays with comparable oncological outcomes to open surgery[4-7].

However, obesity has long been considered a relative contraindication to laparoscopic surgery due to the perceived associated technical difficulty and increased morbidity[8-10]. Despite more recent reports of good short-term outcomes in colorectal cancer resections[11-13], there remains a reluctance to offer laparoscopic surgery to obese patients. Consequently, an increasing number of patients with a high BMI are being denied the benefits of laparoscopic surgery.

The aim of this study was to determine whether obesity was an acceptable contraindication to laparoscopic colorectal surgery by comparing the short-term outcomes of patients with an increased BMI to those of a healthy weight-to-height ratio.

MATERIALS AND METHODS
Study design and setting

A prospective cohort study conducted between 2008 and 2011 at a single colorectal surgery institution in the United Kingdom.

Study population

All consecutive patients undergoing laparoscopic colorectal surgery were included. There were no exclusion criteria. Consistent with the surgical protocol of the unit, all individuals were enrolled into its enhanced recovery after surgery (ERAS) program. A standardised approach to both the anaesthetic and the surgery was performed in all patients.

Data collection

Data were collected prospectively on each individual patient and recorded anonymously on a database. These included patient demographics and BMI, The American Society of Anesthesiologists (ASA) grade, nature of surgery, operative and anaesthetic time, stoma formation, intra-operative blood loss, complications including anastomotic leak, unplanned high dependency unit (HDU) admission, length of hospital stay and readmission rates. Complications were recorded according to the Clavien-Dindo classification system.

The ERAS protocol

All patients were counselled by a nurse specialist prior to surgery and given a detailed explanation of what to expect throughout the course of their hospital stay. Each patient was given contact details for a member of the ERAS team.

Patients were admitted on the day of surgery. The evening before admission each patient received a 100 g of Pre-Load (96 g of carbohydrate; osmolarity of 285 mOsm) mixed in 400 mL of water. On the morning of admission, a further 50 g of Pre-Load in 400 mL of water was given 2 h before surgery. Following discharge, a dedicated nurse practitioner telephoned the patients at 48 h to enquire about any concerns. Patients were followed up in the out-patient department at 6 wk regardless of any concurrent oncological referral.

Peri-operative anaesthetic regime

A standardised anaesthetic protocol was used for all patients. This consisted of a spinal anaesthetic before induction using 2 mL 0.5% plain bupivacaine with 700 mcg of diamorphine. Routine doses of propofol and remifentanil were used for induction and atracurium for neuromuscular blockade. Intraoperative medication included 6.6 mg of dexamethasone, 4 mg of ondansetron, 1.5 g cefuroxime and 500 mg metronidazole. In addition to the intrathecal diamorphine, perioperative analegesia included 1 g IV paracetamol and 75 mg IV diclofenac. An orogastric tube and urinary catheter were sited with the former removed at the end of the procedure. Routine maintenance fluids during the procedure consisted of 1.5 L Hartmann’s solution. Temperature was maintained using a Bair Hugger® blanket. Post-operative fluid regime included 1 L Hartmann’s solution given over 10 h in addition to oral fluids and high calorie drinks. All patients were given oral paracetamol 1 g QD and Ibuprofen 400 mg TD. Patients were managed on an elective surgical ward and allowed oral fluids on the night of surgery. The urinary catheter was removed on the first operative day and patients were encouraged to take a solid oral diet and to mobilise.

Surgical technique

All surgical procedures were carried out using a standardised modular technique. Patients were placed in the modified Lloyd-Davies position for all resections with the legs in stirrups but with the femurs horizontal to the floor, the arms positioned by the sides and high-friction gel pads were used. Arm boards and shoulder supports were avoided. Routine port positions were used for left and right-sided procedures with the use of a 10 mm 30 degree camera. Dissection was predominantly performed using the “hook” with diathermy attached and occasional use of an energy device. Specimens were extracted through a wound protector device using either lower right- or left-sided transverse muscle splitting incisions for right and left-sided resections, respectively. Extraction sites were closed in layers making sure to avoid muscle in the suture line and infiltrated with maximal safe dosage of bupivacaine 0.375%. For left-sided resections a leak test was performed with a flexible sigmoidoscope which was also used to inspect the anastomosis, but was not passed through it.

Statistical analysis

Individuals were classified according to their BMI as healthy weight (< 25), overweight (26-30) and obese (> 30). Outcomes were compared between the three groups.

Continuous data are expressed as mean with standard deviation and categorical data as an absolute number and percentage. Continuous data were analysed using Analysis of Variance (ANOVA). Fisher’s exact test or χ2 test was used to compare categorical data. A two-sided P value of less than 0.05 was considered significant. All data analyses were performed using SPSS version 21 (SPSS Inc., Chicago IL).

RESULTS

Two hundred and fifty four patients were included over the study period. The majority of individuals (41.7%) recruited were of a healthy weight (BMI < 25), whilst 50 patients were classified as obese (19.6%). In all groups, there were more female patients than males. Overall, patients were well matched in terms of the presence of co-morbidities and previous abdominal surgery. Obese patients were found to have a statistically significant difference in ASA grade. Patient characteristics are shown in Table 1.

Table 1 Patient characteristics n (%).
AllBMI < 25BMI 26-30BMI > 30P value
Number254106 (41.7)98 (38.6)50 (19.7)< 0.001
Males122 (48)41 (38.7)58 (59.2)23 (46)0.01
BMI26 (23-30)22.5 (2.1)27.8 (1.5)35.3 (5.9)< 0.001
ASA grade2 (0.6)1.9 (0.6)2.0 (0.6)2.2 (0.6)0.04
Previous abdominal surgery80 (31.5)34 (32)30 (30.6)16 (32)0.972
Co-morbidities187 (73.6)76 (71.7)75 (76.5)36 (72)0.789

Anterior resection and right hemicolectomy were the two most frequently performed operations, accounting together for three quarters of the procedures undertaken (Table 2). There were no significant differences in the incidence and nature of operations across the BMI cohorts.

Table 2 Nature and number of operations.
OperationTotalBMI < 25BMI 26-30BMI > 30P value
Anterior resection107 (42.1)46 (43.4)37 (37.8)24 (48)0.462
Right hemicolectomy82 (32.3)32 (30.2)34 (34.7)16 (32)0.789
Left hemicolectomy7 (2.8)3 (2.8)2 (2.1)2 (2)0.787
Ileocaecal resection10 (3.9)5 (4.7)5 (5.1)0 (0)0.277
Panproctocolectomy7 (2.8)5 (4.7)2 (2.1)0 (0)0.209
Abdominoperineal resection2 (0.8)0 (0)2 (2.1)0 (0)0.201
Sigmoid colectomy5 (2)1 (0.9)3 (3.1)1 (2)0.553
Subtotal/total colectomy11 (4.4)6 (5.7)3 (3.1)2 (4)0.426
Hartmann’s3 (1.2)1 (0.9)2 (2.1)0 (0)0.530
Miscellaneous20 (7.9)7 (6.6)8 (8.2)5 (10)0.756

There were few significant differences in outcomes between obese patients and healthier weight individuals (Table 3). Only readmission rates with rectal bleeding were higher in the obese (2 patients in the obese group compared with none in the other groups), whilst there was a non-significant trend towards increasing anaesthetic time and length of stay associated with higher BMI. Unplanned HDU admission rates favoured patients with a higher BMI, whilst the rate of stoma formation was lower although not significant. Length of surgery and intra-operative blood loss were no different according to BMI.

Table 3 Outcomes split by body mass index.
BMI < 25BMI 26-30BMI > 30P value
Anaesthetic time, min mean (SD)41.10 (50.9)52.62 (62.6)67.55 (70.9)0.080
Length of surgery, min mean (SD)181.1 (65.4)177.8 (56.6)192.63 (61.5)0.421
Intra-op blood loss, mL mean (SD)33.18 (31.9)44.00 (67.1)38.33 (33.6)0.309
Stoma22 (20.8)22 (22.5)8 (16)0.600
LOS, d, mean (SD)4.1 (4.1)3.9 (3.9)5.8 (7.7)0.076
All complications23 (21.7)15 (15.3)14 (28)0.686
Anastomotic leak2 (1.9)0 (0)1 (2)0.771
Re-admission8 (7.5)12 (12.2)3 (6)0.984
Wound infection1 (0.9)1 (1)1 (2)0.609
Abdominal collection1 (0.9)5 (5.1)0 (0)0.859
PR bleeding0 (0)0 (0)2 (4)0.021
DVT/PE0 (0)1 (1)0 (0)0.769
Obstruction/ileus3 (2.8)2 (2)0 (0)0.254
Vomiting/diarrhoea3 (2.8)1 (1)0 (0)0.156
Non-specfic abdo pain0 (0)2 (2)0 (0)0.677
DISCUSSION

This study revealed that obese patients with an increased BMI have comparable short-term outcomes to healthy weight individuals. Furthermore, outcomes of overweight patients with a BMI of between 26 and 30 were also similar. In particular, there was no significant increase in post-operative complications or length of stay, both of which are historically associated with obese patients. Additionally, the length of operating time and intra-operative blood loss were similar in all groups, suggesting a comparable degree of operative difficulty. Finally of note, all patients in the study underwent an ERAS protocol with no adverse outcomes as a result of this approach, in spite of the traditional caution in patients with an increased BMI.

The relationship between obesity and various conditions has been clearly established including with type 2 diabetes, cardiovascular disease, cerebrovascular disease, pulmonary disease, and more recently, cancer[14-17]. Therefore, it would be expected that more perioperative complications would be likely in the obese population consistent with associated co-morbidities. It has been well documented that wound complications are significantly more common in obese patients following, in particular, those receiving long midline incisions[18-20]. Given that this may be the case, it is even more important in this group of patients to limit the surgical stress, so it is felt that they may actually be better off undergoing laparoscopic rather than open surgery. The relationship between obesity and laparoscopic colorectal surgery has evolved over the years. Initial reports investigating the feasibility of laparoscopy in patients with an increased BMI resulted in worse outcomes compared to the non-obese. This included more post-operative complications, conversions to open procedures and an increased length of stay. In cases of cancer resections, however, this was shown to be oncologically safe. Nonetheless, as techniques have improved and there is greater familiarity and capability with laparoscopic surgery, short-term outcomes have become more comparable to open surgery[21-23]. Yet there remains a reluctance to offer laparoscopy to obese patients. It is important to recognise that open surgery in obese patients also takes longer and is more difficult.

Technically, the surgery can be demanding and has been shown repeatedly to lead to a higher learning curve[9]. A thicker, heavier mesentery creates difficulty in recognising the planes of dissection and causes limited space to operate within the abdomen. In those series which show comparable operating times and peri-operative outcomes such as blood loss, improved technology in the form of instruments and high-definition laparoscopes have been cited as factors. Classically, the obese male patient with a narrow pelvis has been considered the most challenging of surgery for colorectal surgeons.

The present study has shown that despite increased BMI, the intra-operative outcomes of blood loss and operating time are no different to non-obese patients. Previous reports have shown an increased operating time in obese patients which is most likely a reflection of the difficulty in operating in these patients[10]. Interestingly, studies which showed an increase in the number of complications in obese patients also reported an increased length of stay. However, these two outcomes are intrinsically linked. For example, ileus is the most common cause of prolonged hospital admission after colorectal surgery[24]. This can be attributed to longer operating time and post-operative complications which need resolution prior to discharge. Therefore, it is not surprising that if the number of complications is reduced, so is the length of stay.

The rate of stoma formation was similar across groups. Stomas may often be formed to protect an anastomosis which is at risk of leaking, a concern associated with technically challenging surgery. It must be noted that stoma formation is also technically more challenging in obese patients due to the increased distance from the abdominal cavity to the skin.

The peri-operative approaches to laparoscopic cases in our institution are identical regardless of whether the resection is right or left-sided. This includes anaesthesia, patient preparation and positioning, and post-operative care. Clearly, there will be modifications in the port positioning although for the vast majority of cases no more than 4 ports and a transverse incision extraction site are used. Using a standardised approach allows clarity for all staff involved in the peri-operative care of the patient.

This study has shown that using a standardised peri-operative protocol including anaesthesia and surgical technique, obese patients can safely be offered laparoscopic surgery for colorectal cancer resections. The short-term outcomes including post-operative complications and length of stay are comparable to non-obese patients. Consequently, obesity should not preclude laparoscopic surgery being offered to patients for colorectal cancer.

COMMENTS
Background

An increased body mass index (BMI) has been traditionally associated with a higher rate of complications. Initial reports on laparoscopy stated the increased BMI should be a preclusion for laparoscopic approaches in colorectal cancer surgery. However as techniques have improved and become more standardised it is possible to safely operate on patients with a high BMI.

Research frontiers

There is still some contention as to whether laparoscopic surgery can be safely performed for colorectal cancer without compromising oncological outcomes.

Innovations and breakthroughs

This study demonstrates that patients can undertake laparoscopy without additional complications and similar short-term outcomes as non-obese patients.

Applications

This study should allow clinicians to assess patients with a high BMI confidently and not preclude them from laparoscopy based solely on BMI.

Peer-review

The study is clear, well-written and easy to read.

Footnotes

P- Reviewer: Castro FJ, Mehmood RK S- Editor: Ji FF L- Editor: A E- Editor: Lu YJ

References
1.  Choban PS, Flancbaum L. The impact of obesity on surgical outcomes: a review. J Am Coll Surg. 1997;185:593-603.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 193]  [Cited by in F6Publishing: 199]  [Article Influence: 7.4]  [Reference Citation Analysis (0)]
2.  Mullen JT, Moorman DW, Davenport DL. The obesity paradox: body mass index and outcomes in patients undergoing nonbariatric general surgery. Ann Surg. 2009;250:166-172.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 354]  [Cited by in F6Publishing: 364]  [Article Influence: 24.3]  [Reference Citation Analysis (0)]
3.  Dindo D, Muller MK, Weber M, Clavien PA. Obesity in general elective surgery. Lancet. 2003;361:2032-2035.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 472]  [Cited by in F6Publishing: 512]  [Article Influence: 24.4]  [Reference Citation Analysis (0)]
4.  Lacy AM, García-Valdecasas JC, Delgado S, Castells A, Taurá P, Piqué JM, Visa J. Laparoscopy-assisted colectomy versus open colectomy for treatment of non-metastatic colon cancer: a randomised trial. Lancet. 2002;359:2224-2229.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1901]  [Cited by in F6Publishing: 1768]  [Article Influence: 80.4]  [Reference Citation Analysis (0)]
5.  Guillou PJ, Quirke P, Thorpe H, Walker J, Jayne DG, Smith AM, Heath RM, Brown JM. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomised controlled trial. Lancet. 2005;365:1718-1726.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2360]  [Cited by in F6Publishing: 2210]  [Article Influence: 116.3]  [Reference Citation Analysis (0)]
6.  Kuhry E, Schwenk WF, Gaupset R, Romild U, Bonjer HJ. Long-term results of laparoscopic colorectal cancer resection. Cochrane Database Syst Rev. 2008;CD003432.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 188]  [Cited by in F6Publishing: 237]  [Article Influence: 14.8]  [Reference Citation Analysis (0)]
7.  Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, Haglind E, Påhlman L, Cuesta MA, Msika S. Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;6:477-484.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 1691]  [Cited by in F6Publishing: 1611]  [Article Influence: 84.8]  [Reference Citation Analysis (0)]
8.  Pikarsky AJ, Saida Y, Yamaguchi T, Martinez S, Chen W, Weiss EG, Nogueras JJ, Wexner SD. Is obesity a high-risk factor for laparoscopic colorectal surgery? Surg Endosc. 2002;16:855-858.  [PubMed]  [DOI]  [Cited in This Article: ]
9.  Tekkis PP, Senagore AJ, Delaney CP, Fazio VW. Evaluation of the learning curve in laparoscopic colorectal surgery: comparison of right-sided and left-sided resections. Ann Surg. 2005;242:83-91.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 571]  [Cited by in F6Publishing: 580]  [Article Influence: 30.5]  [Reference Citation Analysis (0)]
10.  Zhou Y, Wu L, Li X, Wu X, Li B. Outcome of laparoscopic colorectal surgery in obese and nonobese patients: a meta-analysis. Surg Endosc. 2012;26:783-789.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 60]  [Cited by in F6Publishing: 54]  [Article Influence: 4.2]  [Reference Citation Analysis (0)]
11.  Hemandas AK, Abdelrahman T, Flashman KG, Skull AJ, Senapati A, O’Leary DP, Parvaiz A. Laparoscopic colorectal surgery produces better outcomes for high risk cancer patients compared to open surgery. Ann Surg. 2010;252:84-89.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 74]  [Cited by in F6Publishing: 79]  [Article Influence: 5.6]  [Reference Citation Analysis (0)]
12.  Benoist S, Panis Y, Alves A, Valleur P. Impact of obesity on surgical outcomes after colorectal resection. Am J Surg. 2000;179:275-281.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 186]  [Cited by in F6Publishing: 182]  [Article Influence: 7.6]  [Reference Citation Analysis (0)]
13.  Makino T, Shukla PJ, Rubino F, Milsom JW. The impact of obesity on perioperative outcomes after laparoscopic colorectal resection. Ann Surg. 2012;255:228-236.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 120]  [Cited by in F6Publishing: 122]  [Article Influence: 10.2]  [Reference Citation Analysis (0)]
14.  Flegal KM, Kit BK, Orpana H, Graubard BI. Association of all-cause mortality with overweight and obesity using standard body mass index categories: a systematic review and meta-analysis. JAMA. 2013;309:71-82.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 2536]  [Cited by in F6Publishing: 2515]  [Article Influence: 228.6]  [Reference Citation Analysis (0)]
15.  Wolin KY, Carson K, Colditz GA. Obesity and cancer. Oncologist. 2010;15:556-565.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 462]  [Cited by in F6Publishing: 463]  [Article Influence: 33.1]  [Reference Citation Analysis (0)]
16.  Calle EE, Rodriguez C, Walker-Thurmond K, Thun MJ. Overweight, obesity, and mortality from cancer in a prospectively studied cohort of U.S. adults. N Engl J Med. 2003;348:1625-1638.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 5430]  [Cited by in F6Publishing: 5075]  [Article Influence: 241.7]  [Reference Citation Analysis (0)]
17.  Basen-Engquist K, Chang M. Obesity and cancer risk: recent review and evidence. Curr Oncol Rep. 2011;13:71-76.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 326]  [Cited by in F6Publishing: 282]  [Article Influence: 21.7]  [Reference Citation Analysis (0)]
18.  Balentine CJ, Wilks J, Robinson C, Marshall C, Anaya D, Albo D, Berger DH. Obesity increases wound complications in rectal cancer surgery. J Surg Res. 2010;163:35-39.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 46]  [Cited by in F6Publishing: 57]  [Article Influence: 4.1]  [Reference Citation Analysis (0)]
19.  Power K, Davies MM, Hargest R, Phillips S, Torkington J, Morris C. A case-control study of risk factors for wound infection in a colorectal unit. Ann R Coll Surg Engl. 2014;96:37-40.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 9]  [Cited by in F6Publishing: 9]  [Article Influence: 0.9]  [Reference Citation Analysis (0)]
20.  Dobson MW, Geisler D, Fazio V, Remzi F, Hull T, Vogel J. Minimally invasive surgical wound infections: laparoscopic surgery decreases morbidity of surgical site infections and decreases the cost of wound care. Colorectal Dis. 2011;13:811-815.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 28]  [Cited by in F6Publishing: 27]  [Article Influence: 2.1]  [Reference Citation Analysis (0)]
21.  Senagore AJ, Delaney CP, Madboulay K, Brady KM, Fazio VW. Laparoscopic colectomy in obese and nonobese patients. J Gastrointest Surg. 2003;7:558-561.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 124]  [Cited by in F6Publishing: 134]  [Article Influence: 6.4]  [Reference Citation Analysis (0)]
22.  Leroy J, Ananian P, Rubino F, Claudon B, Mutter D, Marescaux J. The impact of obesity on technical feasibility and postoperative outcomes of laparoscopic left colectomy. Ann Surg. 2005;241:69-76.  [PubMed]  [DOI]  [Cited in This Article: ]
23.  Poulsen M, Ovesen H. Is laparoscopic colorectal cancer surgery in obese patients associated with an increased risk? Short-term results from a single center study of 425 patients. J Gastrointest Surg. 2012;16:1554-1558.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 37]  [Cited by in F6Publishing: 38]  [Article Influence: 3.2]  [Reference Citation Analysis (0)]
24.  Schwenk W, Böhm B, Haase O, Junghans T, Müller JM. Laparoscopic versus conventional colorectal resection: a prospective randomised study of postoperative ileus and early postoperative feeding. Langenbecks Arch Surg. 1998;383:49-55.  [PubMed]  [DOI]  [Cited in This Article: ]  [Cited by in Crossref: 144]  [Cited by in F6Publishing: 149]  [Article Influence: 5.7]  [Reference Citation Analysis (0)]