Laparoscopic Petersen’s Hernia Reduction Was Associated With A Better Clinical Course Than Open Reduction After Gastrectomy: A Multicenter Observational Cohort Study


 Background The aim of this multicenter cohort study was to compare the clinical courses between open and laparoscopic Petersen’s hernia (PH) reduction.Materials and method We retrospectively collected the clinical data of patients who underwent PH repair surgery after gastrectomy for gastric cancer from 2015-2018. Forty patients underwent PH reduction operations that were performed by six expert surgeons at four hospitals. Among the 40 patients, 15 underwent laparoscopic PH reduction (LPH), and 25 underwent open PH reduction (OPH), including 4 patients who underwent LPH but required conversion to OPH.Results We compared the clinical factors between the LPH and OPH groups. In the clinical course, we found no differences in operation times or intraoperative bowel injury, morbidity, or mortality rates between the two groups (p>0.05). However, the number of days on a soft fluid diet (OPH vs. LPH; 5.8 vs. 3.7 days, p=0.03) and length of hospital stay (12.6 vs. 8.2 days, p=0.04) were significantly less in the LPH group than the OPH group. Regarding postoperative complications, the OPH group had a case of pneumonia and sepsis with multi-organ failure, which resulted in mortality. In the LPH group, one patient experienced recurrence and required reoperation for PH.Conclusion Laparoscopic PH reduction was associated with a faster postoperative recovery period than open PH reduction, with a similar incidence of complications. The laparoscopic approach should be considered an appropriate strategy for PH reduction.

3.7 days, p=0.03) and length of hospital stay (12.6 vs. 8.2 days, p=0.04) were signi cantly less in the LPH group than the OPH group. Regarding postoperative complications, the OPH group had a case of pneumonia and sepsis with multi-organ failure, which resulted in mortality. In the LPH group, one patient experienced recurrence and required reoperation for PH.
Conclusion Laparoscopic PH reduction was associated with a faster postoperative recovery period than open PH reduction, with a similar incidence of complications. The laparoscopic approach should be considered an appropriate strategy for PH reduction.

Background
Internal hernia can occur as a result of the arti cial mesenteric opening left by entero-entero anastomosis or Petersen's space after a Roux-en-Y anastomosis. Petersen's hernia (PH) is rare but potentially fatal complication that can develop as the result of strangulation or perforation of a herniated small bowel [1]. Therefore, PH should be treated as soon as possible following its detection. Recently, it was reported that the incidence of internal hernia was higher after laparoscopic gastrectomy than after open gastrectomy, possibly because of poor adhesion after laparoscopic surgery [2].
Laparoscopic surgery is a recommended treatment modality for cancer (stomach, colon, liver, biliary) because it is associated with faster postoperative recovery, a lower incidence of complications, and better quality of life outcomes of patients than open surgery [3][4][5][6][7][8]. Laparoscopic internal hernia reduction in the small segment of the small bowel has been reported, but the surgical outcomes associated with laparoscopic PH reduction have not been reported [9,10]. The aim of this multicenter cohort study was to compare the clinical courses between open and laparoscopic PH reductions. This is the rst report involving a large multicenter cohort of gastric cancer patients after gastrectomy.

Methods
A retrospective observational study was designed and carried out according to the principles of the Declaration of Helsinki, 1989. This study was approved by the institutional review board (approval  number of rst author's institution, IRB-D-1909-009-002, and corresponding author's institution, GNUH-IRB-2020-3-32 and 21 underwent open PH reduction (OPH). Therefore, a total of 25 patients underwent OPH (Fig. 1).
Six expert surgeons in laparoscopic gastrectomy have been meeting and sharing their experiences with LPH since 2015. All the surgeons were specialists in gastric cancer surgery with experience in performing more than 200 laparoscopic gastrectomies.
The data of patients who underwent surgery from 2015 to 2018 for intestinal obstruction caused by PH were collected. The inclusion criteria for this study were as follows: 1) previous radical surgery for histologically proven primary gastric adenocarcinoma; and 2) no evidence of other distant metastases.
We collected data regarding the operation, postoperative complications, and course by retrospective chart review after surgery. We compared the past gastric cancer surgery method, TNM stage, surgical information, and postoperative course.

Operations
Decision of open vs. laparoscopic reduction The decision to perform laparoscopic reduction or open reduction was made by the surgeon after determining whether the patient had undergone laparoscopic surgery in the past, whether the patient presented with poor vital signs in the emergency room, and the statuses of bowel edema and dilation in the abdominal cavity on abdominal CT.
Open reduction The operation began with an incision at the site of the previous incision, and an additional incision was made if necessary. During the incision, adhesiolysis was carefully performed to prevent injury to organs with adhesions. After the abdominal wall was opened, the viability of the herniated small bowel was determined. If the herniation direction was easy to detect, surgery was performed immediately. However, it was sometimes di cult to determine the correct direction of herniation. In these cases, we performed the following. First, we identi ed the ileocolic valve and fully reduced the herniated bowel. After complete reduction, we checked the status of bowel perforation and necrosis. If the bowel was not viable even after reduction, we resected the damaged small bowel segment. We closed Petersen's space with non-absorbable sutures.
Laparoscopic reduction The rst trocar was inserted inferior to the umbilicus or in the lower abdomen area by an open method with a new incision. Mostly, we performed the reduction using three or four trocars. The intra-abdominal reduction process was the same as that performed in the open method. However, it was di cult to determine the correct direction of herniation with a laparoscope. Therefore, we rst identi ed the ileocolic valve and fully reduced the herniated bowel by pulling it out. After complete reduction, we checked the status of bowel perforation and necrosis. If the bowel was not viable even after reduction, we resected the damaged small bowel segment. We closed Petersen's space with nonabsorbable sutures (supplement Video).
The possibility of damage or bleeding in the small intestine is higher during laparoscopic hernia reduction than during open reduction due to forceful pulling of laparoscopic graspers. We recommend open conversion for patients with a poor pneumoperitoneum condition or severely damaged bowel, as reduction is di cult due to severe bowel edema.

Statistical analysis
We used SPSS Statistics version 24 (IBM SPSS, Inc., Chicago, IL, USA) for the statistical analyses. Continuous data were compared using unpaired Student's t-test and are presented as means ± standard deviations; non-continuous variables were assessed with the chi square test. In all analyses, p values less than 0.05 were considered statistically signi cant.

Patient demographics
Between 2015 and 2018, a total of 40 PH operations were performed at the four hospitals. The patient demographics are described in Table 1. The average age of patients was 63.9 years old, and the ratio of men to women was 4:1 (32:8). The TNM stage at past gastrectomy was as follows: the highest was stage I, which accounted for 60%; stage II accounted for 22.5%; stage III was the lowest and accounted for 5%; and unknown TNM stage accounted for 12.5%. Regarding past surgeries, there were 11 total gastrectomies (TGs), 24 distal gastrectomies (DGs) and 2 proximal gastrectomies (PGs). The past surgical methods comprised open methods in 28 cases, laparoscopic methods in 7 cases, and unknown methods in ve cases. The mean period between operations was 28.2 months. The mean duration between the presentation of pain and hernia operation was 51.3 hours.  (Fig. 1). The causes of open conversion were di culty in creating a pneumoperitoneum (n = 2) and di culty in laparoscopic reduction due to small bowel and mesentery thickness (n = 2). The mean operation time was 79.5 minutes; 4 patients experienced small bowel injury during reduction. The mean hospital stay was 10.9 days. The morbidity rate was 10% (4 cases), and there was one mortality.

Comparison of clinical factors between the LPH group and the OPH group
We compared the clinical factors between the LPH and OPH groups. We found that the OPH group was older (68.8 years) than the LPH group (55.7 years) (p < 0.001) and had a higher C-reactive protein (CRP) level (OPH vs. LPH; 5.5 vs. 0.72, p = 0.03). However, there were no differences in sex, initial symptoms, duration between operations, TNM stage, previous operation, previous approach method, preoperative white blood cell (WBC) count, or erythrocyte sedimentation rate (ESR) (p > 0.05, Table 2).

Discussion
The aim of this multicenter cohort study was to compare the clinical courses between open and laparoscopic PH reductions. The postoperative recovery course is generally better, and operative wounds are generally smaller with the laparoscopic approach than with open surgery. However, to the best of our knowledge, no one has reported the bene ts of laparoscopic PH reduction. The present multicenter observational cohort study is the rst to report the advantage of laparoscopic PH reduction in terms of postoperative recovery.
PH is a very rare disease that occurred in only 0.54% of patients who underwent gastrectomy for gastric cancer (2,417; the number of patients requiring PH reduction surgery was 13) between 2015 and 2018. In a previous study, the incidence of PH after gastrectomy was 0.42%, which was similarly low compared to our data [2,3]. For PH reduction surgery, the open method is the standard procedure due to the following: rst, it is di cult to develop pneumoperitoneum due to bowel edema and bowel dilation in the abdominal cavity; second, bowel reduction is di cult due to bowel wall and mesentery edema, and usually the whole small bowel is herniated; third, experience in laparoscopic PH reduction is limited [2,9,11]. In our group, the rst laparoscopic reduction was performed in 2014 in Kosin University Hospital; since then, gastric experts from the four centers share their experiences with laparoscopic PH reduction during regular meetings. Sharing their experiences facilitates the application of laparoscopic PH reduction because all surgeons are gastric cancer surgery specialists with experience in performing more than 200 laparoscopic gastrectomies.
Laparoscopic surgery has advantages. We found that the number of days on a soft uid diet and postoperative hospital length of stay were signi cantly less in the laparoscopic reduction group than in the open group. The reason for the faster recovery is likely that laparoscopic surgery resulted in fewer operative wounds and less pain than open surgery. Additionally, if the bowels were not manipulated excessively by the surgeon during laparoscopy, a postoperative diet could be permitted quickly, causing a potential decrease in the length of hospital stay.
Recently, the application of the laparoscopic approach for primary gastrectomy has increased; however, one study reported the possibility of an increased incidence of internal hernia [2]. They reported that laparoscopic TG was associated with a higher incidence of internal hernia than open TG (4.5%, 29/638 vs. 0.8%, 4/475), with the same results for laparoscopic DG compared with open DG (2.7% vs. 0.9%). In the multivariate analysis, they found that non-closure of mesenteric defects, the laparoscopic approach, and a total laparoscopic approach were independent risk factors for internal hernia. We expected the incidence of PH to be higher in primary laparoscopic gastrectomy patients; however, the incidence of PH was higher in primary open gastrectomy patients. This may be because more patients underwent open gastrectomy than laparoscopic gastrectomy in the past. Even though there was only a small number of PH cases included in this study, interestingly, the laparoscopic or open primary approach for gastrectomy did not affect the incidence of PH. In contrast, a recent study reported that closure of the mesenteric space (5.5%) signi cantly decreased the cumulative incidence of reoperation for small bowel obstruction by internal hernia after surgery compared to no mesenteric closure (10.2%) [12]. Therefore, to reduce postoperative complications, especially the incidence of internal hernia after gastrectomy surgery, the closure of mesenteric defects should be performed [2]. The centers included in this study routinely repair mesenteric defects after gastrectomy and have recently started performing closure of Petersen's space to prevent PH.
In terms of postoperative complications, pneumonia generally occurs more frequently in patients who undergo open surgery; open surgery patients also experience more wound pain than patients who undergo minimally invasive surgery [7]. In this study, the one pneumonia patient was an 80-year-old individual who was at increased risk for postoperative complications due to age. In the laparoscopic group, a complication of internal hernia recurrence after reduction surgery was observed. This suggests that we need to close defects more carefully because reduction and closure after laparoscopic surgery is more di cult than after manual open surgery.
Despite the very low incidence of PH, there were some limitations to our study, such as the small number of PH reduction surgeries especially laparoscopic reduction surgeries. The surgeons did not have extensive experience with the laparoscopic approach for PH reduction because it is not a common technique, and PH is a rare disease. Nevertheless, to the best of our knowledge, this is the rst report comparing the surgical outcomes associated with open and laparoscopic approaches for PH reduction.

Conclusions
Laparoscopic PH reduction was associated with faster postoperative recovery and a similar incidence of complications compared with open surgery. The laparoscopic approach could be considered an appropriate strategy for PH reduction.