A retrospective study of internal small bowel herniation following pelvic lymphadenectomy for gynecologic carcinomas

After pelvic lymphadenectomy (PLA), pelvic vessels, nerve, and ureter are skeletonized. Internal hernias beneath the skeletonized pelvic structure following pelvic lymphadenectomy (IBSPP) are a rare complication following PLA. To the best of our knowledge, only 12 IBSPP cases have been reported and clinical details on such hernias remain unknown. The aim of the study was to investigate the incident and etiology of IBSPP. 1313 patients who underwent open or laparoscopic pelvic lymphadenectomy were identified from our database. A retrospective review was performed. Mean follow-up period was 33.9 months. A total of 12 patients had IBSPP. Multivariate analysis of laparoscopic surgeries group as compared to open surgeries group, para-aortic lymphadenectomy rate, number of dissected lymph nodes by PLA, antiadhesive material use rate, and blood loss were lower in laparoscopic surgeries group: odd ratio (OR) = 0.13 [95% confidence interval (CI) 0.08–0.19], and OR = 0.70 [95% CI 0.50–0.99], OR = 0.17 [95% CI 0.10–0.28], OR = 0.93 [95% CI 0.92–0.94]. However, no significant difference was observed in the incidence of IBSPP between laparoscopic surgery (1.0%) and open surgery (0.8%). All IBSPP occurred in the right pelvic space. These findings may contribute to the development of prevention methods for this disease.


Methods
Patient population. We retrospectively searched our patient database for the records of 1313 women with primary gynecological cancer who underwent pelvic lymphadenectomy and hysterectomy or trachelectomy and/or para-aortic lymphadenectomy (PALA) and/or omentectomy at the Cancer Institute Hospital of JFCR, from January 1, 2015, to February 29, 2020, and retrospective review was performed. In these 1313 patients, none received sentinel node procedures. The study was approved by the the Cancer Institute Hospital of JFCR Review Board and was performed in accordance with relevant guidelines and regulations of the institutional review board. Participants provided signed informed consent.
Surgical technique of PLA. In all cases of pelvic lymphadenectomy, tissues along the internal iliac, external iliac, obturator, common iliac vessels, and obturator nerve were completely removed so that these vessels and nerve and ureter were completely skeletonized (Fig. 1). Retroperitoneal suction drainage was performed in all the patients. The choice of affixing or sparing antiadhesive material onto a skeletonized pelvic structure after PLA was based on each surgeon's preference. The retroperitoneum was left open at the end of surgery in all patients.

Follow-up.
As a follow-up of cancer, each case is visited to hospital every few months. If there are symptoms such as abdominal pain or vomiting, or suspicious of recurrence of malignant tumor, CT scan was done. Even if there are no such symptoms, CT scan was done every six months. The follow-up period is determined according to the risk of recurrence in each case.
Definition of IBSPP. IBSPP was defined as an internal hernia suspected preoperatively based on imaging and clinical symptoms and a surgeon-diagnosed internal hernia at the time of surgery that was caused by skeletonized pelvic vessels, nerve, or ureter following PLA.
Statistical analyses. Comparison between groups was performed using the chi-squared test. Means were compared using the T-test or Mann-Whitney U test. All continuous variables were expressed as mean ± standard deviation. Comparison between open surgery and laparoscopic surgery are studied using multiple logistic regression analysis. A p-value < 0.05 was considered to indicate statistical significance. Results were analyzed using the Prism version 6.0 software (GraphPad, USA).
Ethics approval and consent to participate and consent for publication. All subjects gave their informed consent for inclusion before they participated in the study. The study was conducted in accordance with the Declaration of Helsinki and the protocol was approved by the Ethics Committee of Cancer Institute Hospital of JFCR (Approval No. 2020-1033).

Results
Among the 1313 women in this study, 12 (0.91%) had IBSPP (Fig. 2). Clinical and surgical factors were compared between subjects with IBSPP and those without IBSPP (Table 1). No significant differences were observed in age, primary disease, PALA rate, number of lymph nodes dissected by PLA, blood loss, operation time, or laparoscopic surgery rate between these groups.   Table 1. Clinical and surgical factors related to IBSPP. a Ratio of the number of PALA cases divided by the total number of cases. b Ratio of the number of cases which antiadhesive material was affixed or sprayed beneath a skeletonized pelvic structure after PLA cases divided by the total number of cases. c Ratio of the number of laparoscopic surgery cases divided by the total number of cases. d The period from primary surgery to last visit of institution.  Table 2. Clinical and surgical factors and incidence of IBSPP in each surgical procedure. a Ratio of the number of PALA cases divided by the total number of cases. b Ratio of the number of cases which antiadhesive material was affixed or sprayed beneath a skeletonized pelvic structure after PLA cases divided by the total number of cases. c The period from primary surgery to last visit of institution.  Table 2). Patients' initial surgical characteristics are presented in Table 4. There were seven laparotomy cases and five laparoscopic surgery cases. PALA was performed in half of all cases. No significant difference was observed in the number of lymph nodes removed between the right and left PLAs (p > 0.05). In most cases (91.6%), antiadhesive material was used on skeletonized pelvic structures following PLA. In all cases, skeletonized pelvic structures were not closed after PLA. In eight cases (66.7%), adjuvant chemotherapy or radiotherapy was administered between initial operations and IBSPP operations.

Open surgery (n = 835) Laparoscopic surgery (n = 478) p-value
Surgical findings at the time of IBSPP operation are presented in Table 5. The median interval time between operation and onset of obstruction was 13.5 months. All IBSPP occurred in the right pelvic space and did not occur on the left side. Hernial orifices are presented in Fig. 3. Four cases (33.3%) were relative to the obturator artery. Excluding unclear cases, the small bowel herniation point was within 20 cm of the ileocecal valve in four cases (57.1%). There was no recurrence of internal hernia in any of the cases. Four cases (33.3%) received laparoscopic surgery; however, one case required conversion from laparoscopic surgery to laparotomy. Seven cases (58.3%) required bowel resection. Excluding unclear cases, resection of the obturator or umbilical artery was performed in three cases (30%), four cases (40%) were closed by mobilizing the caecum or sigmoid colon, and two cases (20%) were unrepaired.

Discussion
This is the first retrospective study on internal hernia beneath skeletonized pelvic structures following pelvic lymph node dissection. We discuss the incidence, risk factors, etiology, repair method, and prevention methods of IBSPP.  8,14 . This is because low adhesions are a risk factor for internal hernia. However, in this study, no significant difference was observed in the incidence of IBSPP between laparoscopic and open surgeries. In the laparoscopic surgeries group, there was lower operative stress to be expressed due to lower blood loss, PALA rate, number of dissected lymph nodes by PLA, (this mean lower internal hernia risk due to low adhesion), and lower rate of antiadhesion material use (lower internal hernia risk due to high adhesion). As a result, the risk of IBSPP might be offset.
We describe about the etiology of IBSPP. The most significant finding in this study is that all cases occurred on the right side. This finding has implication on the investigation of internal hernia prevention measures. We Table 5. The surgical findings at IBSPP repair operation. TL, total laparoscopic surgery. a Interval months between operation and onset of obstruction. b Position of the incarcerated small bowel. c Length of postoperative hospital stay. d The Clavien-Dindo scale was used to evaluate postoperative complications, and IIIa or higher was defined as major complications.

No
Interval months a Hernial orifice  www.nature.com/scientificreports/ have inferred that there are two causes for this asymmetry. First, peristalsis of the small intestine was from the ligament of Treitz (abdominal midline) to the ileocecum, which is on the right side of the abdomen near the right skeletonized pelvic structure. Therefore, IBSPP tends to occur on the right side. Second, the left skeletonized pelvic structure was covered by the sigmoid colon following PLA. Therefore, IBSPP tends not to occur on the left side. The strangulated small intestine was often close to the ileocecal region. This was probably because the dissection site of the right lymph node was close to this region. We describe about IBSPP repair surgery. Several techniques for closing orifices following PLA can be discussed. Closing the orifice with peritoneum flap and/or sigmoid colon and/or ileocecum 10,13 has been thought to be the most convenient method. However, other techniques are sometimes required due to limited peritoneum around the skeletonized structure. Closing the orifice using a free peritoneal graft 9 or by gluing a collagen patch 12 or mesh 11 with running absorbable surgical sutures may be secondary options. If the causal structure is unimportant, such as the obturator artery, resection of the causal structure 14 is an option.
We describe about preventive methods for internal hernia. Peritoneal closure of the pelvic lymph node dissection space might prevent IBPSS. Because bilateral peritoneal closure may increase the frequency of lymphoma cysts [18][19][20] and IBSPP tends to occur on the right side, right-side closure only may be sufficient. Right-side space closure by mobilizing the caecum might be effective and low invasive method. More sentinel node procedures might be most direct prevention method of IBSPP.
This study has some limitations. Larger sample sizes may be needed to delineate the risk factors for IBSPP. Larger sample sizes may reveal the statistical risk factors for IBSPP; however, event size is limited by low incidence. It was not possible to investigate what preventive measures would reduce the incidence of IBSPP; however, our findings of IBSPP tending to occur on the right side may help develop beneficial precautions. A prospective study of whether various preventive measures can prevent internal hernia is desired.
In conclusion, IBSPP tends to occur on the right side. The incidence of IBSPP is not different in both open and laparoscopic surgery significantly. These findings may contribute to the development of prevention methods for this disease.

Data availability
The datasets analyzed during the current study are available from the corresponding author on reasonable request.

Code availability
The software application/code used during the current study is available from the corresponding author on reasonable request. All the experiment protocol for involving human data was in accordance to guidelines of institutional Declaration of Helsinki.