Surgical Technique Affects the Incidence of Marginal Ulceration after Roux-en-Y in Gastric Bypass

doi:10.4236/ss.2013.412A001

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Surgical Science, 2013, 4, 1-7

Published Online December 2013 (http://www.scirp.org/journal/ss)

http://dx.doi.org/10.4236/ss.2013.412A001

Open Access SS

Surgical Technique Affects the Incidence of Marginal

Ulceration after Roux-en-Y in Gastric Bypass

Yong Kwon Lee, Corrigan McBride, Valerie Shostrom, Jon Thompson

Department of Surgery, College of Public Health, University of Nebraska Medical Center, Omaha, USA

Email: jthom[email protected]

Received September 18, 2013; revised October 15, 2013; accepted October 23, 2013

which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

ABSTRACT

Background: Marginal ulceration (MU) is a recognized complication of Roux-en-Y gastric bypass (RYGB) surgery.

While several possible risk factors have been reported, the mechanism of MU remains incompletely understood. The

aim of this study was to compare the effect of surgical technique on the incidence of MU. Methods and Material: This

was a retrospective study of 749 patients undergoing RYGB over a ten-year period with at least one year of follow-up.

The diagnosis of MU was made based on clinical symptoms and confirmed by postoperative endoscopy (POE). We

assessed four different gastric bypass (GBP) techniques: T1—Open, non-divided stomach, circular stapler, non-vago-

tomy (n = 332); T2—Open, divided stomach, circular stapler, vagotomy (n = 91); T3—Laparoscopic, divided, circular

stapler, vagotomy (n = 152); T4—Laparoscopic, divided, linear stapler, vagotomy (n = 174). Results: The four groups

were similar with respect to age and mean BMI. The frequency of POE was 16%, 25%, 28% and 27% in groups T1-T4

respectively (NS). The incidence of MU was significantly lower in T1 (2.1%) compared to T2 (5.5%), T3 (15.1%) and

T4 (12.6%), p < 0.05. MU occurred significantly more frequently with an antecolic Roux limb versus retrocolic (14.5%

vs 5.6%, p < 0.05). Conclusion: The incidence of MU after RYGB surgery is influenced by surgical technique. The

lowest incidence of MU was with a non-divided stomach, no vagotomy, transverse staple line, and circular stapled an-

astomosis. A retrocolic Roux limb was protective. There was no difference in the incidence of MU using laparoscopic

versus open bypass if a similar technique was employed or using linear versus circular stapler for the gastrojeju-

nostomy.

Keywords: Gastric Bypass; Marginal Ulceration

1. Introduction

Marginal ulceration (MU) is a well-known complication

after Roux-en-Y gastric bypass (RYGB). The symptoms

can range from minimal abdominal discomfort to life

threatening bleeding or perforation [1]. The reported in-

cidence of MU has varied widely in the literature from

1% to 16% [1-10]. These differences may be related to

differences in surgical technique and patient factors, but

also vary depending on definition, method of detection

and follow-up.

The mechanism of MU formation after RYGB is in-

completely understood. Several technical factors have

been implicated, including pouch size and orientation, an

association with foreign material, staple line disruption

and gastrogastric fistula, and anastomotic technique [5,9,

11,12]. A variety of patient-related factors such as non-

steroidal antiinflammatory medication (NSAID), helico-

bacter pylori infection and smoking may also be impor-

tant [13]. The aim of the present study was to evaluate

the influence of different surgical techniques of RYGB

on MU.

2. Methods

Patients

This was a retrospective study of 749 adult patients (>19

years of age), who underwent primary open or laparo-

scopic RYGB procedures. Inclusion criteria were preop-

erative BMI ≥ 35, patient with unsuccessful non-surgical

weight loss treatment and one of the four RYGB tech-

niques received (Table 1). We had excluded techniques

that had less than 50 procedures performed (n = 18) and

revisional procedures (n = 90). All operations were per-

formed by four surgeons at a single institution from Oc-

tober 1995 to November 2005. Overall, there were 653

Y. K. LEE ET AL.

Table 1. Comparison of surgical techniques.

Technique 1 Technique 2 Technique 3 Technique 4

Surgical

Access Open Open Laparoscopic Laparoscopic

Gastric Pouch

Orientation

Staple Line

Pouch Size

Transverse

Nondivided

<30 cc

Vertical

Divided

<30 cc

Vertical

Divided

<30 cc

Vertical

Divided

<30 cc

Vagotomy No Yes Yes Yes

Anastomosis Circular

Stapler

Circular

Stapler

Circular

Stapler

Linear

Stapler

Roux Limb Ante or

Retrocolic

Ante or

Retrocolic

Ante or

Retrocolic

Ante or

Retrocolic

(87%) females and 96 (13%) males. Patients had a mean

age of 46 years with a range from 22 to 74 years. The

mean BMI was 51.5 with a range from 32 - 88 kg/m2.

Mean follow up was 52 months with a range of 12 to 133

months. Local internal review board (IRB) approval was

obtained.

The following variables were collected and analyzed.

Patient factors at the time of RYGB included age, gender,

BMI, active smoking, history of smoking (off cigarettes

at least 6 months), alcohol use, NSAID use, history of

peptic ulcer disease and follow up. Technical factors in-

cluded surgical access (open and laparoscopic), antecolic

versus retrocolic Roux limb and gastro-jejunal anasto-

mosis techniques. Postoperative endoscopy included in-

dications and findings. MU included any ulceration

within 2 cm of the anastomosis. The incidence of MU

was compared using the Kaplan and Meier log rank test.

If the overall log rank test yielded a p-value < 0.05, pair-

wise log rank tests were conducted using a Bonferroni

adjustment for multiple comparisons. The Cox regression

model for censored data was used to examine combina-

tions of patient characteristics associated with a multi-

variate analysis.

3. Surgical Procedures

3.1. Technique 1

Through a midline incision the gastrocolic ligament was

divided to gain access to the lesser sac. Windows were

created in the gastrohepatic ligament along the lesser

curve 4 cm from the GE junction and on the greater

curve. A TA-90B stapler was passed transversely from

the lesser to greater curve side sparing the vagus nerve

and positioned it in order to get a 30 cc pouch. This

pouch size is confirmed by insufflation with 30 cc of

fluid. The anvil of a 21-EEA stapler was placed in the

gastric pouch and secured with a 3-0 Prolene purse string.

The jejunum was divided 40 cm distal to the ligament of

Treitz between bowel clamps and an end-to-side hand-

sewn anastomosis was created between the proximal je-

junum and the side of the Roux limb, 150 cm distal. The

mesenteric defect was closed. The end of the Roux limb

was brought through the transverse mesocolon in retro-

colic or antecolic fashion. The EEA stapler was intro-

duced through the end of the Roux limb for a few cm and

exited the sidewall. It was connected to the anvil and

fired. The end of the Roux limb was amputated with the

TA60 stapler and imbricated with 3-0 silk. The anterior

two thirds of anastomosis were reinforced with horizon-

tal mattresses of 3-0 silk.

3.2. Technique 2

Through a midline incision the gastrocolic ligament was

divided to gain access to the lesser sac. A window was

created in the gastrohepatic ligament along the lesser

curve 4 cm from the GE junction to just below the first

branch of the left gastric artery. At this point, a partial (4

cm) horizontal transection of the stomach was carried out

with a GIA stapler. This divided the vagus nerve. A

small gastrotomy was created in the lower gastric seg-

ment laterally. This was used to introduce the 21 EEA

anvil into the upper gastric pouch, bring it through the

gastric wall and secure it with a pursestring in the proxi-

mal pouch. The gastric transection was then completed

with the GIA-60 stapler firing in a vertical fashion to the

angle of His. The small bowel was divided with a GIA

stapler 40 cm distal to the ligament of Treitz. A 150 cm

Roux limb cm was measured and the side-to-side jejuno-

jejunostomy performed. The mesenteric defect was

closed. The end of the Roux limb was brought through

the transverse mesocolon in an antecolic or retrocolic

fashion. The 21-EEA stapler was introduced through the

end of the Roux limb for a few cm and exited the side

wall. It was connected to the anvil and fired. The end of

the jejunum was amputated with the TA-60 stapler and

imbricated with 3-0 silk. The anastomosis was reinforced

with horizontal mattresses of 3-0 silk.

3.3. Technique 3

Pneumoperitoneum was established and five laparo-

scopic ports were placed. We identified the angle of His

and dissected a window. An opening was created in the

gastrohepatic ligament along the lesser curve 4 cm from

the GE junction just below the first branch of the left

gastric artery. The GIA was then used to go across the

stomach transversely 4 cm. This divided the vagus nerve.

A small opening was made in the midpoint of that staple

line. We then placed two stay sutures in the distal stom-

ach and made a gastrotomy. The anvil of a 21 EA stapler

was passed through the left sided port site and brought

through the distal gastrotomy and up through the trans-

verse staple line. The distal gastrotomy was then closed

with a GIA stapler. The GIA-60 was fired in a vertical

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Y. K. LEE ET AL. 3

fashion up to the angle of His to complete the pouch. The

small bowel was divided with a GIA stapler 40 cm distal

to the ligament of Treitz. We then performed a side-to-

side stapled anastomosis between the proximal jejunum

and the side of the Roux limb 150 cm distal. The Roux

limb was brought in an antecolic or retrocolic fashion.

Next, we positioned with the anvil and fired. We ampu-

tated the end of the Roux limb with the GIA-60. Non-

absorbable antitension sutures were placed at each corner

of the anastomosis.

3.4. Technique 4

Pneumoperitoneum was established and five laparo-

scopic ports were placed. We identified the angle of this

and dissected a window. The small bowel was run 40 cm

from the Ligament of Treitz and transected using an

Endo GIA 60-2.5 stapler. The Roux limb was measured

150 cm distally. We then performed a side to side stapled

anastomosis between the proximal jejunum and the side

of the Roux Limb. The Roux limb was brought up an

antecolic or retrocolic fashion. The mesenteric defect

was closed. The gastrohepatic ligament was opened and

the lesser curve was identified 4 cm from the GE junc-

tion just below the first branch of the left gastric artery.

The gastric pouch was created using a series of Endo

GIA 60-3.5 staples going 4 cm transversely, including a

vagotomy. Complete gastric transection was assured in a

vertical fashion. An Endo GIA 45-3.5 stapler was in-

serted intraluminally to 2.5 cm and fired. The anastomo-

sis was completed in a handsewn fashion with an inner

layer of absorbable suture and outer layer of non-ab-

sorbable suture. The gastroscope was directed down the

esophagus and across the gastrojejunal anastomosis.

4. Results

The four patient groups were similar in age and BMI.

There was no difference in the incidence of a history of

ulcer disease, alcohol consumption and use of NSAID

(Table 2). Active smoking, history of smoking and gen-

der were the variables which were significantly different

among groups. There were a lesser proportion of females

in technique 2 versus technique 3. Both active smoking

and history of smoking were significantly less frequent in

patients undergoing technique 4.

Overall, POE was performed in 166 (22%) patients.

There was a statistically significant difference in the in-

cidence of POE among the groups (Table 3). The main

indications for POE were nausea and vomiting (40%),

followed by abdominal pain (23%) (Table 4). The find-

ings of POE were the following: normal n = 85 (50%),

MU n = 57 (34%), stricture n = 23 (14%), bleeding n = 2

(1%) and more than 2 pathologic sign n = 1 (1%). The

incidence of MU at POE ranged from 13% - 53% among

the different techniques.

Table 2. Comparison of clinical characteristi cs.

Technique 1Technique 2 Technique 3 Technique 4

Number 332 91 152 174

Mean BMI

(range) 51.4 (32 - 88)52.1 (36 - 76) 52.1 (32 - 78) 50.8 (36 - 79)

Mean age

years (range)47 (25 - 72)44 (25 - 71) 44 (22 - 74) 46 (26 - 71)

Gender (%

female) 88 78# 91 89

Alcohol use

Yes

330 (99%)

2 (1%)

88 (97%)

3 (3%)

150 (99%)

2 (1%)

173 (99%)

1 (1%)

Active

smoking

Yes

264 (80%)

68 (20%)

73 (80%)

18 (20%)

122 (80%)

30 (20%)

160 (92%)*

14 (8%)

History of

smoking

Yes

216 (65%)

116 (35%)

66 (73%)

25 (27%)

98 (64%)

54 (36%)

139 (80%)*

35 (20%)

NSAID

Yes

296 (89%)

36 (11%)

72 (79%)

19 (21%)

126 (83%)

26 (17%)

144 (83%)

30 (17%)

History of

Peptic ulcer

Yes

326 (98%)

6 (2%)

89 (98%)

2 (2%)

148 (97%)

4 (3%)

173 (99%)

1 (1%)

*p < 0.05 vs other; #p < 0.05 vs T3.

Overall, MU occurred in 57 (7.6%) of patients (Table

3). Fifteen (26%) occurred in the first two postoperative

years. The specific location of the ulcers at endoscopy

was gastro-jejunal anastomosis n = 27 (47%), jejunal n =

22 (39%), gastric n = 7 (12%) and multiple sites n = 1

(2%). All of the ulcers were localized within 2 cm from

the anastomotic site.

Univariate analysis using a log-rank test revealed a

significant difference in incidence of MU by technique

(Tables 3 and 5). Specifically, the incidence of MU was

smaller for the technique 1 compared with each of the

other techniques. There were no differences among T2,

T3, and T4. In univariate analysis there was evidence that

MU was associated with retrocolic Roux limb route (p <

0.0001) and a tendency with history of smoking (p =

0.1453).

In the multivariate Cox proportional hazards regres-

sion model, these three variables (technique, history of

smoking, and Roux limb fashion) were included in the

model (Table 6). After accounting for history of smoking

and Roux limb fashion, technique was significantly asso-

ciated with MU. The risk of MU is 43 times higher for

subjects treated with technique 2 (p < 0.0001), 19 times

higher for patients treated with technique 3 (p < 0.0001)

and 52 times higher for subjects treated with technique 4

p ≤ 0.0001) compared with technique 1. After ac- (

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Y. K. LEE ET AL.

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Table 3. Incidence of marginal ulceration and endoscopy.

Technique 1 Technique 2 Technique 3 Technique 4 Total

Number of Marginal Ulcer (%) 7 (2.1%)* 5 (5.5%) 23 (15.1%) 22 (12.6%) 57 (7.6 %)

Number of Postoperative Endoscopy (%) 53 (16%)# 23 (25%) 43 (28%) 47 (27%) 166 (22%)

Endoscopy with Marginal Ulcer (%) 13%# 22% 53% 46% 34%

*p < 0.05 vs T2, T3, T4; #p < 0.05 vs T3, T4.

Table 4. Indications for postoperative endoscopy.

Nausea and vomiting 66 (40%)

Abdominal pain 38 (23%)

Multiple symptoms 20 (12%)

Symptomatic reflux 18 (10%)

Anemia 10 (6%)

Gastrointestinal bleeding 9 (5%)

Other 7 (4%)

Table 5. Results of univariate analysis.

Comparison p-value (log-rank test)

Technique Overall <0.0001

T1 vs T2

T1 vs T3

T1 vs T4

T2 vs T3

T2 vs T4

T3 vs T4

<0.0006

0.4392

0.99

0.6414

Active smoking 0.3984

Age quartile 0.3317

Alcohol use 0.5156

BMI quartile 0.5599

Gender 0.8269

History of smoking 0.1453

NSAID 0.4081

Peptic ulcer disease 0.3432

Roux limb route <0.0001

counting for technique and Roux limb fashion, the risk of

MU is 2.2 times higher for those with a history of smok-

ing compared to those with no history of smoking (p =

0.0054). After accounting for technique and history of

smoking, the risk of MU for patients with a retrocolic

Roux limb is 0.15 times that of patients with antecolic

fashion (p < 0.0001).

Overall 171 (23%) Roux Limbs were antecolic and

578 (77%) were retrocolic (Table 7). The incidence of

Table 6. Results of multivariate analysis.

Variable Hazard Ratio p-value

T2 vs T1 42.577 <0.0001

T3 vs T1 19.151 <0.0001

T4 vs T1 52.342 <0.0001

History of smoking yes vs no 2.172 0.0054

Retrocolic vs antecolic route 0.152 <0.0001

MU was higher with antecolic versus with retrocolic

Roux Limb (14.0% vs 5.7%, p < 0.05). The majority of

procedures in T1 (99%), T2 (96%) and T3 (70%) were

with a retrocolic limb compared to T4 (33%).

5. Discussion

Marginal ulcer (MU) formation is a common complica-

tion after RYGB. Overall, our incidence of MU was

7.5% which is consistent with others studies published

[1-12]. The present study focused on the potential rela-

tionship between MU and the technique of RYGB em-

ployed. We demonstrated that the RYGB technique used

strongly influences MU formation.

Univariate analysis revealed a significant difference in

incidence of MU by technique. Specifically, incidence of

MU was smaller for technique 1 (Open, non-divided

stomach, circular stapler, non-vagotomy) compared with

each of the other techniques. There was no difference

among the other groups. Using multivariate analysis,

history of smoking and Roux limb route were signify-

cantly associated with MU. After accounting for history

of smoking and Roux limb route, technique was signify-

cantly associated with MU. The risk of MU is 19 times

higher for subjects treated with technique 2, 52 times

higher for patients treated with technique 3, and 43 times

higher for subjects treated with technique 4 compared

with technique 1.

The patient groups undergoing the different proce-

dures were similar with respect to age, BMI and several

relevant patient factors. However, there was a signify-

cantly lower incidence of active smoking and history of

smoking in technique 4. After accounting for technical

factors, the risk of MU is 2.2 times higher for those with

a history of smoking compared to those with no history

Y. K. LEE ET AL. 5

Table 7. Comparison of marginal ulcer and roux limb

route.

Antecolic

No ulcer Ulcer Total number

Technique 1 4 0 4

Technique 2 4 0 4

Technique 3 36 10 46

Technique 4 103 14 117

Total 147 24 (14.0%) 171

Retrocolic

No ulcer Ulcer Total number

Technique 1 321 7 328

Technique 2 82 5 87

Technique 3 93 13 106

Technique 4 49 8 57

Total 545 33 (5.7%)* 578

*p < 0.05 vs antecolic.

of smoking. This was the only patient-related factor that

we identified. The incidence of postoperative endoscopy

was also similar in the four groups.

Since there are several different technical aspects in

the techniques, the reasons for the lower MU rate in

Technique 1 are not clear. This was an open technique.

However, the similar outcomes in techniques 2 and 3

where surgical access is the only difference in technique

suggest that surgical access is not an important issue.

There are few studies comparing the effect of surgical

access. Patel et al. [1] reported similar incidence of MU

(5.4% and 5.1%) with an open technique identical to our

technique 1 and laparoscopic technique similar to our

technique 3.

Technique 1 included a non-divided stomach. This

might improve blood supply, which is presumed to con-

tribute significantly to preventing formation of MU.

There may also be less inflammation since wound heal-

ing occurs at a transection site. Pope et al. [4] found that

increasing the number of staple rows from 4 to 8 in the

non-divided stomach increased the incidence of MU.

However, the study by Patel et al. [1] mentioned above

would argue against this point.

The vagus nerve was not divided in technique 1.

Vagus nerve preservation, which will preserve stimula-

tion of parietal cells in the pouch and distal stomach to

increase acid production, may subsequently irritate the

gastric mucosa as well as anastomotic site [14]. However,

normal gastric peristalsis will remain intact, which may

act as clearance of acid from surgical site avoiding a

formation of MU [15]. Ikramuddin, S. et al. (poster pres-

entation at Society for Surgery of the Alimentary Tract in

San Francisco, May 2002) compared laparoscopic gastric

bypass with (n = 91) and without (n = 84) vagotomy

along the greater curve and found a similar incidence of

MU (4.3% vs. 1.1%), suggesting vagotomy at this loca-

tion is not an important factor. Interestingly, truncal

vagotomy has been employed therapeutically with suc-

cess for intractable MU [16].

The gastric pouch in technique 1 had a transverse

rather than vertical orientation, similar to the technique

of Patel et al. [1]. As noted, they found no difference in

MU rate. Since the gastric pouch is known to contain

parietal cells and have acid production, making a small

pouch has been emphasized in preventing MU [9,10,

12,14,17,18]. Printen [18] demonstrated that reducing

pouch size decreased MU. Others have found that the

length of a vertically oriented pouch correlates with MU

rate [9,19].

Technique 1 included a circular stapled anastomosis.

This is unlikely to be an important factor. Techniques 3

and 4 were similar techniques except for a circular or

linear stapled anastomosis. However, the incidence of

marginal ulcer was similar. Similarly, others have found

no difference in MU rate with type of anastomosis, in-

cluding hand sewn vs. circular stapled [20] and linear vs.

circular [21,22]. Suggs et al. [23] found fewer ulcers

with the 21-mm vs 25-mm circular stapler, however.

Thus, type of anastomosis does not appear to be an im-

portant factor.

After accounting for technique and history of smoking,

the risk of MU for patients with Roux Limb in a retro-

colic fashion was 0.15 times that of patients with ante-

colic fashion. We feel this may be related to more tension

and potential ischemia at the anastomosis. Taylor et al.

[24] compared Roux limb route and found no difference

in the incidence of stricture, but did not evaluate MU.

This study has several limitations. We employed se-

lective endoscopy for symptoms in the present study.

This will affect the detection of MU. Several studies

suggest MU is fairly frequent in the early postoperative

period [25,26]. Only 24% of MU in the present study

occurred early. Our endoscopy rate of 22% and findings

of MU in 34% of endoscopy is similar to other reports

with selective endoscopy [27,28]. Asymptomatic ulcers

would have been missed since routine endoscopic screen-

ing was not carried out. Not all surgeons performed all

four operations. Open procedures were performed pre-

dominantly early in the study period. H. pylori was not

routinely sought in patients with MU. Some non-ab-

sorbable sutures were used in the seromuscular layers at

the anastomosis in all four groups but not in a standard

fashion.

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Y. K. LEE ET AL.

6. Conclusion

In conclusion, the incidence of MU after RGBP surgery

is influenced by surgical technique. The overall 7.5%

incidence of MU is consistent with other studies. The

lowest incidence of MU was the technique with a non-

divided stomach, no vagotomy, and a circular anastomo-

sis. A retrocolic Roux limb was protective. There was no

difference of MU using linear or circular stapler for the

gastrojejunostomy and no difference in laparoscopic ver-

sus open bypass if a similar technique was employed.

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