A variety of neonatal intestinal disorders, such as meconium ileus (MI), congenital intestinal atresia (CIA) or necrotizing enterocolitis (NEC), requires urgent surgical intervention. The different operative strategies include creation of a primary anastomosis (PA) following bowel resection, formation of a temporary diverting stoma (DS), or an ostomy in continuity (OIC) such as Bishop-Koop (BK) or Santulli enterostomy (SE). The intra-operative decision-making process is based on individual patient conditions, severity of underlying disease, training backgrounds and personally expertise of the surgeon.
The PA following bowel resection promotes a single-stage procedure that maintains intestinal autonomy. However, without creation of a proximal protective enterostomy, the incidence of anastomotic leaks ranges between 1.6% and 31%.[1–7] Conversely, a 2-stage restoration of intestinal continuity using formation of the diverting enterostomy has been advocated for neonates who are at increased risk of anastomotic complications due to peritonitis (NEC) or size discrepancy between the dilated proximal and the unused distal bowel (CIA, MI). Even so, stoma related complications and the need for a second operation to close the stoma are issues of concern. The frequency of ostomy related complications ranges from 18% to 42% following ostomy formation[8–10] and is as high as 70% following ostomy closure.[11–13] Although the decision between PA or DS in the treatment of MI, CIA, and NEC remains an area of controversy, both treatment strategies are accepted as standard surgical modalities.
An alternative approach to PA and divided stoma (DS) is OIC, including Bishop-Koop procedure (BK) and Santuli enterostomy, which both allow sufficient bowel decompression while also preserving intestinal transit. Following resection of the intestinal segment, the end of the proximal limb is anastomosed to the side of the distal (BK) limb and the end of the distal limb is brought out as the enterostomy (also known as the “chimney”). The mirror image, in which the end of the proximal limb is used for the enterostomy, represents the SE.
Though the BK was initially designed for the treatment of infants with MI, it has been gradually applied in neonates with NEC[15,16] and CIA.[17–19] Recently, BK has also been utilized in the management of children with short bowel syndrome and severe jejunoileal atresia.
In our practice, BK has been used as a standard treatment for MI, CIA, and NEC, in addition to PA and DS. We have utilized this technique since 2000 with the intention of diverting the fecal stream and protecting the anastomosis. The preservation of intestinal continuity minimizes intestinal fluid loss seen in DSs. In cases of intestinal transport difficulty, the “chimney” acts as a safety vent, partially decompressing the anastomosis and reducing the risk of anastomotic breakdown. Furthermore, the “chimney” can also be used as an access point for diagnostic endoscopic procedures or contrast enema.
Despite its historical significance, the BK has largely fallen out of use in pediatric surgical practice as many pediatric surgeons prefer PA when clinically appropriate. We have found a paucity of comparative information in the recent literature exploring the suitability and safety of BK in neonatal surgery. Therefore, we decided to analyze and report our data to determine the clinical impact and suitability of BK procedure compared to DS in neonates with MI, CIA, and NEC.
2.1 Study design and patient selection
All patients who underwent BK and DS formation and closure from January 2000 to January 2019 at the Medical Center – University of Freiburg, Center for Surgery, Department of Pediatric Surgery were included in this retrospective case-control study. Data collection included gestational age, birth weight, age and weight at time of operation, indications for surgical therapy, level of intestinal diversion, time to stoma function, time to stoma closure and complications directly related to the ostomy. The institutional review board of the University of Freiburg granted approval for this retrospective study (#96/15).
2.2 Exclusion criteria
Children older than 6 months of age and neonates with associated congenital anomalies, such as anorectal malformation or Hirschsprung disease, were excluded from the study. Additionally, neonates with congenital syndromes affecting multiple organ systems were excluded. Children with CIA, MI, or NEC were also excluded from the study if the medical record was incomplete.
2.3 Surgical technique
2.3.1 Bishop-Koop procedure
The formation of Bishop-Koop anastomosis took place in the operation theater under general anesthesia. The procedures were performed by 1 of 4 experienced pediatric surgeons. After abdominal exploration, segmental bowel resection or other appropriate surgical intervention to solve the causative problem was performed. For reconstruction, the distal bowel was fashioned into a stoma and anastomosed side-to-end into the proximal bowel (Fig. 1). We used continuous single layer suture technique. The extension of the distal bowel was exteriorized as an end enterostomy or “chimney.” A postoperative drainage was not routinely used.
2.3.2 DS procedure
A DS was defined as bowel discontinuity, regardless of the distance between the proximal and the distal ends of the stoma. All divided ostomies were fixed to fascia.
2.4 Definitions of underlying medical conditions
MI was defined as intestinal obstruction characterized by the impaction of thick, inspissated, protein-rich, adhesive and dessicated meconium in children with or without cystic fibrosis (meconium plug syndrome). NEC was defined as ischemic necrosis of the intestinal mucosa with pneumoperitoneum secondary to intestinal perforation leading to resection of necrotic bowel segment. Infants with spontaneous intestinal perforation were included in the NEC group. CIA was defined as neonatal intestinal small bowel obstruction caused by jejunal or ileal atresia with large diameter ratio of the proximal and distal lumens.
2.5 Complications following ostomy formation and closure
We analyzed all ostomy related complications following formation and closure, including the following: parastomal hernias, mucocutaneous separation, necrosis, prolapse, retraction, stenosis, peristomal skin irritation, peristomal infection abscess, and fistula, as well as acute bowel obstruction for both BK and DS procedures.
Results are presented as absolute numbers, a percentage (%) frequency, a mean with corresponding standard deviation or a median with range when appropriate. Statistical analysis was performed using SPSS Version 23. The Student t test was used to determine statistical significance for data with normal distribution, and the Mann–Whitney U test was used to compare data that were not normally distributed. The chi-square and Fisher exact tests were used to compare complication rates between the groups. A significance level of < .05 was adopted. All P values were 2-sided.
Over the 19 year study period, 57 (55.8%) BK and 45 (44.2%) DS procedures were created and all of them subsequently closed at our institution. There were no intraoperative complications or hospital mortality in both groups. Demographic data and clinical characteristics are summarized in Table 1. There were no statistically significant differences regarding clinical characteristics between patients who had a BK and those who had DS. The proximal segment of BK and DS was localized in the jejunum (n = 12, 21.0% vs 17, 37.7%), ileum (n = 42, 73.6% vs n = 26, 57.7%) or large intestine (n = 3, 5.4% vs n = 2, 4.6%). The distal vent of BK and DS was localized in the jejunum (n = 12, 21.0% vs n = 15, 33.3%), the ileum (n = 41, 72.0% vs n = 23, 51.2%) or the large intestine (n = 4, 7.0% vs n = 7, 15.5%). The mean duration of stoma use was 246.1 ± 82 days in BK group and 221.5 ± 93 days in DS group (P = .15). In 2 patients (3.5%), the BK stoma closed spontaneously. Nevertheless, these patients also underwent formal ostomy closure to restore the integrity of the abdominal wall.
Complications leading to revisional surgery following ostomy formation occurred in 19 (18.6%) patients. Patients with DS developed significantly more stoma related complications compared to patients in BK group (14 (31.1%) vs 5 (8.7%), P = .005). Complications in children with DS included prolapse of stoma (n = 7, 50%), stoma stenosis (n = 5, 35.7%) and parastomal hernia (n = 2, 14.3%). Among the patients with BK procedure, small bowel obstruction without necrosis due to the rotation of bowel around the ostomy vent was seen in 4 patients and stoma prolapse in 1 patient. The clinical characteristics of patients with complications following BK formation are shown in Table 2. There was no evidence of anastomotic leakage or stricture.
To examine the influence of underlying diagnosis, gestational age, birth weight, age and weight at time of ostomy creation, and duration of ostomy use on surgical complications, additional sub-analysis was performed. The data is summarized in Table 3. The differences among patients with and without ostomy related complications within BKP and DS groups were not statistically significant.
Rates of complications following ostomy closure were generally low in both groups (n = 2, 3.5% vs n = 3, 6.7%, P = .65). Wound infections were seen in 2 (3.5%) patients within the BK group. Complications among DS group included anastomotic leakage (n = 1, 33.3%), anastomotic stricture (n = 1, 33.3%), and wound infection (n = 1, 33.3%). Wound infection was managed conservatively. Other complications required revisional surgery.
The operating time for BK closure was significantly shorter compared to DS (82.2 ± 51.4 vs 183 ± 84.5 min, P < .001) (Fig. 2). Patients with BK exhibited rapid recovery and the length of hospital stay was significantly shorter compared to the DS group (5.5 ± 2.7 vs 11.3 ± 3.9 days, P < .001) (Fig. 3).
To circumvent the surgical problems associated with PA if created without protective ostomy as well as stoma-related morbidity, we utilized the BK technique as a standard procedure to treat neonates with MI, CIA, and NEC.
The present study demonstrated a lower complications rate after BK creation compared with DS. BK closure was also associated with reduced operating time and shorter length of hospital stay. However, in spite of its potential benefits, data on BK utilization in neonates are very scarce. Table 4 summarizes the available literature on use of BK in neonates.
In our study, the frequency of complications following BK formation was 8.7% and 3.5% following its closure. The range of BK related complications reported in the literature varies from 0.0% to 19.9% for BK ostomy creation and from 0.0% to 7.4% for its closure.[17,22,23] The most frequent complication was the rotation of bowel around the ostomy vent, occurring in four patients in our series (7.0%). This unique type of complication can be regarded as specific to BK enterostomy and has also been reported with low incidence in other studies. We also observed 1 case of Bishop-Koop stoma prolapse. This type of stoma related complication is reported to be a very rare event. No cases of stoma necrosis, retraction, parastomal hernia, peristomal skin breakdown or wound cellulitis were observed. Furthermore, anastomotic leakage or stenosis did not occur in our BK patient cohort. According to the literature, anastomotic leakage following BK formation occurs in up to 5% of patients.[17,20,21] In contrast, prior studies demonstrate a variable rate of anastomotic complications following PA if created without protective ostomy ranging from 15% to 30% for MI,[1,2,24,25] from 6% to 10% for CIA,[26–28] and from 5% to 12% for NEC.[5,7,10,29] We hypothesize that the lower rate of anastomotic complications in BK compared to PA is due to presence of a diverting ostomy, which serves as a vent and thereby protects the anastomosis.
Some may argue that the BK procedure is time-consuming because it requires an anastomosis. However, in the current study, the operating time for ostomy formation did not significantly differ between BK and DS groups. Furthermore, the premature neonates with NEC and SIP represent a particular patient group in our study cohort. Due to immature motility of the bowel and peritonitis, the creation of DS seems to be safer than BKP. Nevertheless, all patients with NEC in the BK group survived and underwent successive ostomy closure. Moreover, we additionally compared operating times in the subgroup of patients with NEC and did not observed any statistical significant differences between BK and DS groups (150 ± 56.4 vs 130.2 ± 56.2, P = .35).
In the present study, only 2 patients in the BK group suffered from wound infections after ostomy reversal (n = 2, 3.5%); both were treated conservatively. This finding is in line with other studies in which the occurrence of wound infections after stoma closure reportedly range from 0.0% to 7.4%.[17,38] Conversely, in the DO group, more severe complications occurred following ostomy reversal, including anastomotic leakage and stenosis (n = 2, 4.4%) requiring revisional surgery. The differences are explained by the fact that there is no need for the creation of an anastomosis during BK takedown, with the reversal procedure consisting simply of chimney closure.
In our study, time to ostomy closure (246.1 ± 82 days in BK group and 221.5 ± 93 days in DS group) was found to be much longer than previously observed in other studies, in which mean time to reversal ranged from 84 to 177 days.[9,42–45] This discrepancy can be explained in part by surgeon's preference and our local protocol, but is not evidence-based. Surgical aspects that favor later ostomy closure include fewer postoperative abdominal adhesions,[46–48] anesthesiological aspects include potential adverse neurodevelopmental outcomes as a result of general anesthesia at a very young age.[49,50] Moreover, the unique anatomical advantage of BK anastomosis, which preserves intestinal continuity and maintains the fluid and electrolyte balance, relativizes the potential advantages of early ostomy closure. Nevertheless, there is currently no consensus for the optimal timing of ostomy reversal. In fact, although a number of studies have sought to determine the optimal time to close an enterostomy, there is no significant difference in the complication rate of infants whose enterostomy was reversed within 8 weeks (27–31%) or after 8 weeks (19–23%) following its creation.[11,51,52]
We are aware of several limitations of this study. These include a small patient population and the retrospective study design. Nevertheless, our study represents one of the largest series of BK procedures performed in neonates with gastrointestinal tract disorders.
In conclusion, Bishop-Koop procedure has a low rate of complications following its formation and a satisfactory operating time. Moreover, BK closure is associated with shorter operating time and shorter length of hospital stay compared to DS. Although it remains the responsibility of the surgeon to determine the utilization of treatment techniques, surgeons should keep this technique as an alternative approach in their repertoire. Nevertheless, without a sufficiently powered randomized controlled trial, no argument can be made regarding the superiority of one operative strategy over another.
Conceptualization: Illya Martynov, Jochen Raedecke, Joachim Schoenberger.
Data curation: Illya Martynov, Jessica Klima-Frysch, Jochen Raedecke, Joachim Schoenberger.
Formal analysis: Jessica Klima-Frysch, Wolfram Kluwe, Joachim Schoenberger.
Investigation: Illya Martynov, Joachim Schoenberger.
Methodology: Illya Martynov, Jochen Raedecke, Joachim Schoenberger.
Project administration: Illya Martynov, Jochen Raedecke.
Resources: Jessica Klima-Frysch.
Supervision: Jessica Klima-Frysch, Jochen Raedecke, Joachim Schoenberger.
Validation: Jessica Klima-Frysch, Joachim Schoenberger.
Visualization: Wolfram Kluwe, Jochen Raedecke.
Writing – original draft: Illya Martynov, Joachim Schoenberger.
Writing – review & editing: Illya Martynov, Jessica Klima-Frysch, Wolfram Kluwe, Jochen Raedecke, Joachim Schoenberger.
. Karimi A, Gorter RR, Sleeboom C, et al. Issues in the management of simple and complex meconium ileus. Pediatr Surg Int 2011;27:963–8.
. Jawaheer J, Khalil B, Plummer T, et al. Primary resection and anastomosis for complicated meconium ileus: a safe procedure? Pediatr Surg Int 2007;23:1091–3.
. Hillyer MM, Baxter KJ, Clifton MS, et al. Primary versus secondary anastomosis in intestinal atresia. J Pediatr Surg 2018;54:417–22.
. Stollman TH, de Blaauw I, Wijnen MH, et al. Decreased mortality but increased morbidity in neonates with jejunoileal atresia; a study of 114 cases over a 34-year period. J Pediatr Surg 2009;44:217–21.
. Singh M, Owen A, Gull S, et al. Surgery for intestinal perforation in preterm neonates: anastomosis vs stoma. J Pediatr Surg 2006;41:725–9.
. Karila K, Anttila A, Iber T, et al. Outcomes of surgery for necrotizing enterocolitis and spontaneous intestinal perforation in Finland during 1986–2014. J Pediatr Surg 2018;53:1928–32.
. Guelfand M, Santos M, Olivos M, et al. Primary anastomosis in necrotizing enterocolitis: the first option to consider. Pediatr Surg Int 2012;28:673–6.
. Lockhat A, Kernaleguen G, Dicken BJ, et al. Factors associated with neonatal ostomy complications
. J Pediatr Surg 2016;51:1135–7.
. van Zoonen AG, Schurink M, Bos AF, et al. Ostomy creation in neonates with acute abdominal disease: friend or foe? Eur J Pediatr Surg 2012;22:295–9.
. Mutanen A, Pierro A, Zani A. Perioperative complications
following surgery for necrotizing enterocolitis. Eur J Pediatr Surg 2018;28:148–51.
. Zani A, Lauriti G, Li Q, et al. The timing of stoma closure in infants with necrotizing enterocolitis: a systematic review and meta-analysis. Eur J Pediatr Surg 2016;27:7–11.
. Banerjee DB, Vithana H, Sharma S, et al. Outcome of stoma closure in babies with necrotising enterocolitis: early vs late closure. Pediatr Surg Int 2017;33:783–6.
. Aguayo P, Fraser JD, Sharp S, et al. Stomal complications
in the newborn with necrotizing enterocolitis. J Surg Res 2009;157:275–8.
. Bishop HC, Koop CE. Management of meconium ileus; resection, Roux-en-Y anastomosis and ileostomy irrigation with pancreatic enzymes. Ann Surg 1957;145:410–4.
. Vanamo K, Rintala R, Lindahl H. The Santulli enterostomy in necrotising enterocolitis. Pediatr Surg Int 2004;20:692–4.
. Mirza B. An interesting case of bishop-koop stoma prolapse. APSP J Case Rep 2010;1:24.
. Wit J, Sellin S, Degenhardt P, et al. Is the Bishop-Koop anastomosis in treatment of neonatal ileus still current? Chirurg 2000;71:307–10.
. Fleet MS, de la Hunt MN. Intestinal atresia with gastroschisis: a selective approach to management. J Pediatr Surg 2000;35:1323–5.
. Haxhija EQ, Schalamon J, Hollwarth ME. Management of isolated and associated colonic atresia. Pediatr Surg Int 2011;27:411–6.
. Sehgal S, Sandler AD, Alfred Chahine A, et al. Ostomy in continuity: A novel approach for the management of children with complex short bowel syndrome. J Pediatr Surg 2018;53:1989–95.
. Peng Y, Zheng H, He Q, et al. Is the Bishop-Koop procedure
useful in severe jejunoileal atresia? J Pediatr Surg 2018;53:1914–7.
. Hasan MS, Mitul AR, Karim S, et al. Comparison of t tube ileostomy and bishop koop ileostomy for the management of uncomplicated meconium ileus. J Neonatal Surg 2017;6:56.
. Zhang H, Zhong W, Sun J, et al. Application of Bishop-Koop stoma in refractory congenital intestinal atresia
. Zhonghua Wei Chang Wai Ke Za Zhi 2016;19:1154–9.
. Mentessidou A, Loukou I, Kampouroglou G, et al. Long-term intestinal obstruction sequelae and growth in children with cystic fibrosis operated for meconium ileus: expectancies and surprises. J Pediatr Surg 2018;53:1504–8.
. Miyake H, Urushihara N, Fukumoto K, et al. Primary anastomosis for meconium peritonitis: first choice of treatment. J Pediatr Surg 2011;46:2327–31.
. Hillyer MM, Baxter KJ, Clifton MS, et al. Primary versus secondary anastomosis in intestinal atresia. J Pediatr Surg 2019;54:417–22.
. Yeung F, Tam YH, Wong YS, et al. Early reoperations after primary repair of jejunoileal atresia in newborns. J Neonat surgery 2016;5:42.
. Kumaran N, Shankar KR, Lloyd DA, et al. Trends in the management and outcome of jejuno-ileal atresia. Eur J Pediatr Surg 2002;12:163–7.
. Hofman FN, Bax NMA, van der Zee DC, et al. Surgery for necrotising enterocolitis: primary anastomosis or enterostomy? Pediatr Surg Int 2004;20:481–3.
. Dickson JA. Apple peel small bowel: an uncommon variant of duodenal and jejunal atresia. J Pediatr Surg 1970;5:595–600.
. McPartlin JF, Dickson JA, Swain VA. Meconium ileus. Immediate and long-term survival. Arch Dis Child 1972;47:207–10.
. Valerio D, Jones PF. Immediate resection in the treatment of large bowel emergencies. Br J Surg 1978;65:712–6.
. Caniano DA, Beaver BL. Meconium ileus: a fifteen-year experience with forty-two neonates. Surgery 1987;102:699–703.
. Palmieri T, Kimura K, Soper RT, et al. A staged surgical approach to save ischemic bowel. J Pediatr Surg 1993;28:861–2.
. Herzog D, Atkison P, Grant D, et al. Combined bowel-liver transplantation in an infant with microvillous inclusion disease. J Pediatr Gastroenterol Nutr 1996;22:405–8.
. Murshed R, Spitz L, Kiely E, et al. Meconium ileus: a ten-year review of thirty-six patients. Eur J Pediatr Surg 1997;7:275–7.
. Arsalani-Zadeh R, Kallam R, Khan S, et al. Early restoration of intestinal continuity in acute mesenteric ischaemia using Bishop-Koop stoma. Ann R Coll Surg Engl 2010;92:W23–4.
. Burjonrappa S, Crete E, Bouchard S. Comparative outcomes in intestinal atresia: a clinical outcome and pathophysiology analysis. Pediatr Surg Int 2011;27:437–42.
. Kayastha K, Mirza B, Sheikh A. Volvulus of small bowel in a case of simple meconium ileus. APSP J Case Rep 2011;2:7.
. Watanabe Y, Takasu H, Sumida W. A preliminary report on the significance of excessively long segment congenital hypoganglionosis management during early infancy. J Pediatr Surg 2011;46:1572–7.
. Boczar M, Sawicka E, Zybert K. Meconium ileus in newborns with cystic fibrosis - results of treatment in the group of patients operated on in the years 2000-2014. Dev Period Med 2015;19:32–40.
. Bethell G, Kenny S, Corbett H. Enterostomy-related complications
and growth following reversal in infants. Arch Dis Child Fetal Neonatal Ed 2017;102:F230–f234.
. Wolf L, Gfroerer S, Fiegel H, et al. Complications
of newborn enterostomies. World J Clin Cases 2018;6:1101–10.
. Steinau G, Ruhl KM, Hornchen H, et al. Enterostomy complications
in infancy and childhood. Langenbecks Arch Surg 2001;386:346–9.
. Bælum JK, Rasmussen L, Qvist N, et al. Enterostomy complications
in necrotizing enterocolitis (NEC) surgery, a retrospective chart review at Odense University Hospital. BMC Pediatr 2019;19:110.
. Choudhry MS, Grant HW. Small bowel obstruction due to adhesions following neonatal laparotomy. Pediatr Surg Int 2006;22:729–32.
. Fredriksson F, Christofferson RH, Lilja HE. Adhesive small bowel obstruction after laparotomy during infancy. Br J Surg 2016;103:284–9.
. Lakshminarayanan B, Hughes-Thomas AO, Grant HW. Epidemiology of adhesions in infants and children following open surgery. Semin Pediatr Surg 2014;23:344–8.
. Andropoulos DB. Effect of anesthesia on the developing brain: infant and fetus. Fetal Diagn Ther 2018;43:1.
. Walkden GJ, Pickering AE, Gill H. Assessing long-term neurodevelopmental outcome following general anesthesia in early childhood: challenges and opportunities. Anesth Analg 2019;128:681–94.
. Veenstra M, Nagappala K, Danielson L, et al. Timing of ostomy reversal in neonates with necrotizing enterocolitis. Eur J Pediatr Surg 2015;25:231–5.
. Struijs MC, Sloots CE, Hop WC, et al. The timing of ostomy closure in infants with necrotizing enterocolitis: a systematic review. Pediatr Surg Int 2012;28:667–72.
Keywords:Copyright © 2019 The Authors. Published by Wolters Kluwer Health, Inc. All rights reserved.
Bishop-Koop procedure; complications; congenital intestinal atresia; divided stoma