INTRODUCTION ORIGINAL ARTICLE. Doo Yeon Go, Yoon Jung Boo, Ji Sung Lee 1, Cheol Woong Jung 2

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ORIGINAL ARTICLE pissn 2288-6575 eissn 2288-6796 http://dx.doi.org/10.4174/astr.2016.91.2.80 Annals of Surgical Treatment and Research Transumbilical laparoscopic-assisted appendectomy is a useful surgical option for pediatric uncomplicated appendicitis: a comparison with conventional 3-port laparoscopic appendectomy Doo Yeon Go, Yoon Jung Boo, Ji Sung Lee 1, Cheol Woong Jung 2 Division of Pediatric Surgery, Department of Surgery, Korea University College of Medicine, Seoul, 1 Department of Medical Statistics, Seoul Asan Medical Center, Seoul, 2 Department of Surgery, Korea University College of Medicine, Seoul, Korea Purpose: Transumbilical laparoscopic-assisted appendectomy (TULA) is a single incision technique that uses a combined intra- and extracorporeal method. The aim of this study was to compare surgical outcomes of TULA with conventional 3- port laparoscopic appendectomy (LA). Methods: A retrospective review of medical records between 2010 and 2014 identified 303 pediatric patients who underwent LA with uncomplicated acute appendicitis. Of these, 85 patients underwent TULA and 218 patients underwent conventional LA. Demographic data, clinical characteristics, perioperative outcomes and postoperative complications were compared between the 2 groups. Results: The mean operation time in the TULA group was 30.39 minutes, which was significantly shorter than that of the LA group (47.83 minutes) (P < 0.001). The first day of oral intake after surgery was earlier (1.05 days vs. 1.32 days; P < 0.001) and the length of hospital stay was also shorter (2.54 days vs. 3.22 days; P < 0.001) for the TULA group than the LA group. Furthermore, the postoperative complication rate was lower in the TULA group (1 of 85, 1.25%) compared to the LA group (19 of 218, 8.7%) (P = 0.018). Conclusion: In conclusion, TULA procedure is recommended for uncomplicated appendicitis in children due to its simplicity and better postoperative outcomes. [Ann Surg Treat Res 2016;91(2):80-84] Key Words: Appendectomy, Child, Laparoscopy, Umbilicus INTRODUCTION Laparoscopic appendectomy (LA) has been widely accepted as a treatment of choice for acute appendicitis for pediatric surgeons because of its advantages of lower complication rate, shorter length of hospital stay, reduced pain, and improved cosmetic outcomes compared to open appendectomy [1,2]. In the 1990s, laparoscopic-assisted appendectomy employing an umbilical incision as a single-port access was implemented by Pelosi and Pelosi [3]. This technique, termed single incision lapar oscopic surgery (SILS), has attracted attention from surgeons in anticipation of less invasiveness and better cosmetic results than conventional multiport procedures. However, recent randomized controlled studies did not find that SILS was more effective in terms of operative time and postoperative pain [4,5]. Our group has performed transumbilical laparoscopic-assisted appendectomy (TULA), approaching through a single Received April 4, 2016, Revised June 11, 2016, Accepted June 21, 2016 Corresponding Author: Yoon Jung Boo Division of Pediatric Surgery, Department of Surgery, Korea University College of Medicine, 73, Inchon-ro, Seongbuk-gu, Seoul 02841, Korea Tel: +82-2-920-6844, Fax: +82-2-928-1631 E-mail: drboo@korea.ac.kr Copyright c 2016, the Korean Surgical Society cc Annals of Surgical Treatment and Research is an Open Access Journal. All articles are distributed under the terms of the Creative Commons Attribution Non- Commercial License (http://creativecommons.org/licenses/by-nc/4.0/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. 80

Doo Yeon Go, et al: Transumbilical laparoscopic-assisted appendectomy umbilical incision using a multichannel separable glove port to exteriorize the appendix and perform the appendectomy extra-abdominal side. This simple, quick technique has the advantages of both laparoscopic and open methods. Recently, several studies have reported favorable outcomes with single incision techniques similar to ours compared with conventional laparoscopy in terms of length of hospital stay, postoperative pain and complications [6,7]. However, these studies are different from ours in technique, since they describe use of a rigid single channel trocar for exploration of the appendix, and also include cases of complicated appendicitis or a small sample size, potentially leading to bias in the results. The aim of this study was to compare the efficacy of TULA and LA focusing on perioperative outcomes for pediatric patients with acute uncomplicated appendicitis. METHODS Patients We retrospectively reviewed the records of all pediatric pa tients under the age of 15 who were diagnosed with acute appendicitis and underwent LA at Korea University-affiliated Hospitals between January 2010 and January 2014. A total of 499 patients underwent laparoscopic surgery with acute appendicitis during this period. Among them, 196 children who were diagnosed with complicated appendicitis were excluded. Of the remaining 303 patients, 85 underwent TULA and 218 underwent conventional 3-port LA. All operations were performed by attending surgeons who had practiced laparoscopic surgery for more than 5 years. Diagnosis of acute appendicitis Suspicion of appendicitis was based on either patient his tory and physical examination such as abdominal pain in the right lower quadrant (RLQ) or migration of pain from the periumbilical area to the RLQ, or laboratory findings indicating elevation of inflammatory markers. Abdominal ultrasonography was used as the first diagnostic tool for these cases. Children underwent surgery based on diagnosis using ultrasonography or CT scan, and a confirmatory diagnosis was made based on pathologic reports. Surgical procedures Laparoscopic appendectomy Each patient was placed in the supine position under general anesthesia and mechanical ventilation. Laparoscopic access into the abdominal cavity was carried out using a vertical um bilical incision. After inserting a 10-mm laparoscopic trocar into the umbilicus, capnoperitoneum was achieved by carbon dioxide (CO2) gas. Two additional 5-mm trocars were introduced in the right lower abdomen. A 30o 10-mm laparoscope was inserted for abdominal examination. A grasper was used to identify the mesoappendix and to dissect adhesions. After ligating vessels using clips, the appendix was ligated using a laparoscopic endoloop and then resected. The appendix was exteriorized through the umbilicus using a laparoscopic endo-bag. The fascial defect on the 10-mm port site was closed with absorbable sutures. Transumbilical laparoscopic-assisted appendectomy Patient preparations were the same as for conventional LA. An approximately 10-mm-sized single vertical umbilical incision was performed. A multichannel separable glove port was used for single-port access. This port can be used as a wound protector after separation during surgical procedures for an exteriorized appendix through the umbilicus. After the establishment of capnoperitoneum, a 30o 5-mm laparoscope was introduced for explorative laparoscopy. The tip of the appendix was grasped with a Babcock clamp and exteriorized through the umbilical incision, which was easily done in most cases. For the few cases with difficulty in exterio rization of the appendix, further dissection was per formed to free the lateral peritoneal attachment of the cecum to facilitate exteriorization. The appendix was dissected and resected outside the abdominal cavity as in an open procedure (Fig. 1). Data Information related to age, sex, initial body temperature, WBC count, levels of CRP, operative time, length of hospital stay, day of first oral intake after surgery, and postoperative complications was collected. Exclusion criteria Children who had a complicated overall status with an abscess in the abdominal cavity or diffuse peritonitis confirmed by imaging reports were not included. Cases identified as complicated appendicitis on the surgical record or pathologic report were also excluded. Fig. 1. View of an exteriorized appendix through the umbili cal incision site. Annals of Surgical Treatment and Research 81

Annals of Surgical Treatment and Research 2016;91(2):80-84 Statistical analysis Differences between the 2 groups were tested by SAS ver. 9.3 (SAS Institute Inc., Cary, NC, USA). Continuous variables were compared using the Student t-test. Discrete variables were analyzed with the chi-square test or Fisher exact test. All hypothesis tests were 2-sided. Multiple logistic regression analysis was performed to measure the adjusted odds ratios (ORs) of characteristics for complications. A P-value of less than 0.05 was considered statistically significant. RESULTS Table 1 shows the demographic and clinical characteristics of study patients. The age and sex ratios of these 2 groups were not statistically different. The clinical characteristics, including initial temperature, preoperative WBC count, or CRP levels, showed no significant differences between the LA and TULA groups. In terms of perioperative outcomes, the mean operative time of the TULA group was 30.39 ± 13.12 minutes, which was significantly shorter than that of the LA group (47.83 ± 16.59 minutes) (P < 0.001). The time to first oral intake was shorter for the TULA group compared to the LA group (1.05 ± 0.43 days vs. 1.32 ± 0.52 days) (P < 0.001), and the TULA group also had a shorter average length of hospital stay (2.54 ± 0.72 days vs. 3.22 ± 1.01 days) (P < 0.001) (Table 2). Postoperative complications were experienced in 19 of 218 patients (8.7%) in the LA group versus 1 of 85 (1.25%) in the TULA group (P = 0.018) (Table 2). Complications were frequently associated with superficial surgical site infection (SSI), accounting for 17 patients in the LA group and 1 patient in the TULA group. The LA group included 1 case of deep SSI and 1 case of intra-abdominal abscess. There were no intra-abdominal abscess cases in the TULA group. In order to identify variables independently associated with postoperative complications, a multiple logistic regression was performed. LA was significantly associated with a higher risk of postoperative complications compared to TULA (adjusted OR [95% confidence interval], 9.82 (1.27-76.04), P = 0.029), while age, weight, CRP levels, and initial body temperature were not shown to be contributable factors to post operative complications (Table 3). DISCUSSION In recent years, several innovative procedures have been intro duced to improve cosmetic outcomes and optimize surgical out comes of minimally invasive surgery such as natural orifice transluminal endoscopic surgery (NOTES) [8,9] and SILS [10]. However, NOTES has yet to be clinically applied in humans and requires specialized instruments and training [11]. Moreover, a prospective randomized study comparing SILS and LA in children argued that SILS resulted in significantly longer mean operative times without the advantages related to reductions in complications [5]. Since SILS approaches the abdominal cavity via a single incision site through the umbilicus, the intricate nature of the intracorporeal dissection and resection of the appendix may have led to prolonged operative times [12]. TULA is similar to SILS in that it uses a single port during Table 2. Comparison of perioperative outcomes and postoperative complications Variable LA (n = 218) TULA (n = 85) P-value Operative time (min) 47.83 ± 16.59 30.39 ± 13.12 <0.001 First oral intake (day) 1.32 ± 0.52 1.05 ± 0.43 <0.001 Length of hospital stay 3.22 ± 1.01 2.54 ± 0.72 <0.001 (day) Postoperative complications 19 (8.7) 1 (1.2) 0.018 Values are presented as mean ± standard deviation or number (%). LA, conventional laparoscopic appendectomy; TULA, transumbilical laparoscopic-assisted appendectomy. Table 1. Demographic data and clinical characteristics of study patients Variable LA (n = 218) TULA (n = 85) P-value Age (yr) 9.64 ± 2.14 9.02 ± 2.28 0.087 Sex Female:male 81:137 35:50 0.518 Initial body temperature 37.3 37.1 0.188 ( o C) WBC ( 10 3 /μl) 11.46 ± 5.43 10.15 ± 4.89 0.543 CRP (mg/l) 35.40 ± 18.40 29.50 ± 19.30 0.322 Values are presented as n or mean ± standard deviation. LA, conventional laparoscopic appendectomy; TULA, trans umbilical laparoscopic-assisted appendectomy. Table 3. Multiple logistic regression analysis for postoperative complications Variable Adjusted OR 95% CI P-value Age 0.93 0.75 1.16 0.514 Weight 1.50 0.59 1.05 0.398 CRP 1.02 0.99 58.53 0.107 Body temperature 0.88 0.34 2.24 0.782 LA vs. TULA TULA Reference - - LA 9.82 1.27 76.04 0.029 OR, odds ratio; CI, confidence interval; LA, laparoscopic appendectomy; TULA, transumbilical laparoscopic-assisted appendectomy. 82

Doo Yeon Go, et al: Transumbilical laparoscopic-assisted appendectomy the surgery. However, TULA uses a combined laparoscopic and open technique, including intra-abdominal laparoscopic mobilization and extracorporeal removal of the appendix [6]. TULA is more cost-effective since it requires smaller numbers of trocars and surgical supplies compared to conventional LA [13,14]. In children, where the distance between the appendix and umbilicus is shorter and the abdominal wall is more flexible than in adults, it is easier to exteriorize the appendix through the umbilicus than in adults [6]. We found that the TULA group had significantly shorter operation times than the LA group (P < 0.001). However, Bergholz et al. [7] reported from a prospective study that TULA showed a propensity to take longer than LA, although the difference was not statistically significant. The discrepancy between studies is likely due to differences in study patients and surgical instruments. Bergholz et al. [7] included cases of complicated appendicitis and the instruments used for intraabdominal dissection were rigid 12-mm ports and all-in-one laparoscopic instruments that involved a rigid side-arm viewing laparoscope and a long single grasper. These instruments might result in interference and collision between surgical instruments. In contrast, our study only included children with simple acute appendicitis. In addition, the separable multichannel glove port used in our study was more flexible, making it easier to mobilize the appendix. The TULA group started oral intake earlier (P < 0.001), and stayed in the hospital for less time than the LA group (P < 0.001). These results stem from the straightforward process and minimal invasiveness of the TULA procedure, which revisits the concept of fast-track surgery. TULA is broadly in accordance with the concept of fast-tracking, a comprehensive program for optimization of perioperative care in elective surgery by alleviating stress and discomfort, and where maxi mization of advantages includes better postoperative outcomes [15]. The rate of postoperative complications was significantly lower in the TULA group than the LA group (1.2% vs. 8.7%; P = 0.018). In support of this finding, multiple logistic regression analysis revealed that undergoing LA compared to TULA (adjusted OR [95% confidence interval], 9.82 (1.27 76.04), P = 0.029) was significantly associated with postoperative complications. Superficial SSI was the most common complication in the LA group in our study. The shorter operation time of TULA and reduced surgical trauma to the incisional site with extracorporeal management of the appendix could be attributed to the lower SSI rate. TULA offers additional advantages of a more favorable cosmetic result compared to 3-port LA. Furthermore, TULA is simple and easy, rescuing surgeons from ergonomically difficult and prolonged single incision techniques. Accordingly, if a patient is diagnosed with an uncomplicated appendicitis, TULA appears to be the preferred option to LA in pediatric patients. This study has several limitations. First, the retrospective design may have included selection biases, although multiple logistic regression analysis was performed to control for confounders. Second, the procedures were not performed in the same time period. TULA was more frequently performed in more recent surgeries, which may also have led to a bias in patient selection. In conclusion, TULA was a more effective surgical option compared to conventional LA in patients with acute uncomplicated appendicitis, offering reduced operative time, early initiation of oral nutrition, shorter length of hospital stay, and less postoperative complications. CONFLICTS OF INTEREST No potential conflict of interest with this article was reported. REFERENCES 1. Masoomi H, Nguyen NT, Dolich MO, Mills S, Carmichael JC, Stamos MJ. Laparoscopic appendectomy trends and outcomes in the United States: data from the Nationwide Inpatient Sample (NIS), 2004-2011. Am Surg 2014;80:1074-7. 2. Eypasch E, Sauerland S, Lefering R, Neugebauer EA. Laparoscopic versus open appendectomy: between evidence and common sense. Dig Surg 2002;19:518-22. 3. Pelosi MA, Pelosi MA 3rd. Laparoscopic appendectomy using a single umbilical puncture (minilaparoscopy). J Reprod Med 1992;37:588-94. 4. Carter JT, Kaplan JA, Nguyen JN, Lin MY, Rogers SJ, Harris HW. A prospective, randomized controlled trial of single-incision lapar oscopic vs conventional 3-port laparoscopic appendectomy for treatment of acute appendicitis. J Am Coll Surg 2014; 218:950-9. 5. Perez EA, Piper H, Burkhalter LS, Fischer AC. Single-incision laparoscopic surgery in children: a randomized control trial of acute appendicitis. Surg Endosc 2013;27: 1367-71. 6. Ohno Y, Morimura T, Hayashi S. Transum bilical laparoscopically assisted appen dectomy in children: the results of a single-port, single-channel procedure. Annals of Surgical Treatment and Research 83

Annals of Surgical Treatment and Research 2016;91(2):80-84 Surg Endosc 2012;26:523-7. 7. Bergholz R, Krebs TF, Klein I, Wenke K, Reinshagen K. Transumbilical lapar oscopic-assisted versus 3-port laparoscopic and open appendectomy: a case-control study in children. Surg Laparosc Endosc Percutan Tech 2014;24:244-7. 8. Palanivelu C, Rajan PS, Rangarajan M, Parthasarathi R, Senthilnathan P, Prasad M. Transvaginal endoscopic appen dectomy in humans: a unique approach to NOTES--world's first report. Surg Endosc 2008;22:1343-7. 9. Bernhardt J, Steffen H, Schneider-Koriath S, Ludwig K. Clinical NOTES appen dectomy study: comparison of trans vagi nal NOTES appendectomy in hybrid technique with laparoscopic appen dectomy. Int J Colorectal Dis 2015;30:259-67. 10. Merchant AM, Cook MW, White BC, Davis SS, Sweeney JF, Lin E. Transumbilical Gel port access technique for performing single incision laparoscopic surgery (SILS). J Gastrointest Surg 2009;13:159-62. 11. Atallah S, Martin-Perez B, Keller D, Burke J, Hunter L. Natural-orifice transluminal endoscopic surgery. Br J Surg 2015;102:e73-92. 12. Oltmann SC, Garcia NM, Ventura B, Mitchell I, Fischer AC. Single-incision lapar oscopic surgery: feasibility for pediatric appendectomies. J Pediatr Surg 2010; 45:1208-12. 13. Visnjic S. Transumbilical laparoscopically assisted appendectomy in children: hightech low-budget surgery. Surg Endosc 2008;22:1667-71. 14. Deie K, Uchida H, Kawashima H, Tanaka Y, Masuko T, Takazawa S. Single-incision laparoscopic-assisted appendectomy in children: exteriorization of the appendix is a key component of a simple and costeffective surgical technique. Pediatr Surg Int 2013;29:1187-91. 15. Kehlet H, Wilmore DW. Evidence-based surgical care and the evolution of fasttrack surgery. Ann Surg 2008;248:189-98. 84