S. Hosie1 S. Loff1 H. Wirth1 H.-J. Rapp2 C. von Buch3 K.-L.

Waag1

Experience of 49 Longitudinal Intestinal Lengthening Procedures for Short Bowel Syndrome

Original Article

Abstract
Patients, Methods and Results: Forty-nine patients with a mean age of 25 months underwent a longitudinal intestinal lengthening procedure for short bowel syndrome (SBS) in our institution. Indications for the operation were dependence on parenteral nutrition in spite of adequate conservative management. The small bowel was lengthened from a mean of 27 cm to a mean of 51 cm. There was no intraoperative mortality. The following early complications occurred in our early series: ischemia of a short bowel segment of 2 cm, requiring resection in two patients, insufficiency of the longitudinal anastomosis in two patients and an intra-abdominal abscess in one. Four of 9 non-survivors died of liver failure and 3 of sepsis. Follow-up showed that 19 patients were weaned from parenteral nutrition after a mean of 9.1 months. Long-term complications encountered were dismotility with malabsorption due to bacterial overgrowth caused by progressive dilatation of the bowel, d-lactic acidosis, cholelithiasis and urolithiasis. Conclusions: A longitudinal intestinal lengthening procedure is an effective and safe surgical approach for SBS, provided it is perfomed in time, the patients preoperative condition is optimized and technical surgical details are taken into account. Key words Short bowel syndrome bowel lengthening surgical treatment

Rsum
Patients, Mthodes et Rsultats: 49 patients avec un ge moyen de 25 mois ont subi un allongement longitudinal de lintestin pour un grle court dans notre Institution. Les indications de cette opration taient la dpendance la nutrition parentrale en dpit de la prise en charge. Lintestin tait allong de 25 cm 51 cm. Il ny a pas eu de mortalit intra-opratoire. Les complications survenant prcocement dans notre premire srie taient: une ischmie dun segment intestinal de 2 cm ncessitant une rsection chez deux patients, une insuffisance de lanastomose longitudinale chez deux patients, et un abcs intra-abdominal chez un patient. Quatre sur 9 des patients dcds prsentaient une dfaillance hpatique et trois un sepsis. Le suivi montrait que chez 19 patients on pouvait arrter la nutrition parentrale aprs une moyenne de 9,1 mois. Les complications long terme rencontres taient une dysmotilit avec une malabsorption due une pullulation microbienne cause par une dilatation progressive de lintestin, une acidose lactique, une lithiase choldocienne et une urolithiase. Conclusion: Lallongement longitudinal de lintestin est une mthode efficace et sre pour amliorer les grles courts, dans la mesure o cette intervention est ralise au moment o les conditions pr-opratoires du patient sont optimales et que les dtails de la technique chirurgicale sont bien pris en compte. Mots-cls Grle court allongement du grle traitement chirurgical

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Affiliation Department of Pediatric Surgery, Mannheim University Hospital, Heidelberg University, Germany 2 Department of Anesthesia, Mannheim University Hospital, Heidelberg University, Germany 3 Department of Pediatrics, Mannheim University Hospital, Heidelberg University, Germany Correspondence Prof. Dr. med. Stuart Hosie Klinik fr Kinderchirurgie Klinikum Mnchen Schwabing Klner Platz 1 80804 Mnchen Germany E-mail: stuart.hosie@kms.mhn.de Received: October 30, 2004 Accepted after Revision: December 11, 2004 Bibliography Eur J Pediatr Surg 2006; 16: 171 175 Georg Thieme Verlag KG Stuttgart New York DOI 10.1055/s-2006-924251 ISSN 0939-7248

Resumen
Pacientes, Mtodos y Resultados: 49 pacientes con una edad media de 25 meses fueron sometidos a alargamiento intestinal longitudinal por sndrome de intestino corto en nuestra institucin. La indicacin para la operacin fue la dependencia de alimentacin parenteral a pesar del tratamiento conservador adecuado. En intestino delgado fue alargado de una media de 27 cm a una media de 51 cm. No hubo mortalidad intraoperatoria. Las siguientes complicaciones precoces ocurrieron en nuestras series iniciales: Isquemia de un segmento de 2 cm que requiri reseccin en 2 pacientes, insuficiencia de la anastomosis longitudinal en 2 pacientes y absceso intraabdominal en 1. Cuatro de 9 no sobrevivientes murieron de fallo heptico y 3 de sepsis. El seguimiento ha mostrado que 19 pacientes pudieron ser liberados de la alimentacin parenteral tras una media de 9,1 meses. Las complicaciones encontradas a largo plazo fueron dismotilidad con malaabsorcin debida a sobrecrecimiento bacteriano causado por dilatacin progresiva del intestino, acidosis d-lctica, colelitiasis y urolitiasis. Conclusion: El alargamiento longitudinal intestinal es efectivo y seguro para el sndrome de intestino corto siempre que se lleve a cabo a tiempo, que la condicin preoperatoria del paciente sea buena y que los detalles quirrgicos tcnicos sean tenidos en cuenta. Palabras clave Sndrome del intestino corto alargamiento intestinal tratamiento quirrgico

Zusammenfassung
Patienten, Methoden und Ergebnisse: 49 Patienten mit einem mittleren Alter von 25 Monaten wurden einer longitudinalen Darmverlngerung aufgrund eines Kurzdarmsyndroms unterzogen. Operationsindikation war die Notwendigkeit der parenteralen Ernhrung trotz adquater konservativer Therapie. Der Dnndarm wurde im Mittel von 27 cm auf 51 cm verlngert. Es trat keine intraoperative Mortalitt auf. Folgende frhe Komplikationen wurden beobachtet: Ischmie eines 2 cm messenden Dnndarmsegmentes, welches reseziert werden musste, bei zwei Patienten, Insuffizienz der Lngsnaht bei zwei Patienten und ein intraabdomineller Abszess bei einem weiteren. 9 Patienten sind verstorben, davon vier an Leberinsuffizienz und 3 an Sepsis. Die Nachuntersuchung hat gezeigt, dass 19 Patienten nach im Schnitt 9,1 Monaten keiner parenteralen Ernhrung mehr bedurften. Beobachtete Sptkomplikationen waren Darmtransportstrung mit Malabsorption aufgrund bakterieller berwucherung durch eine erneute Darmdilatation, D-Laktat-Azidose, Cholelithiasis und Urolithiasis. Schlussfolgerungen: Die longitudinale Darmverlngerung ist eine effektive und sichere Operationstechnik bei Kurzdarmsyndrom, vorausgesetzt die Operationsindikation wird beizeiten gestellt, der properative Zustand des Patienten wird optimiert und operativ-technische Einzelheiten werden beachtet. Schlsselwrter Kurzdarmsyndrom Darmverlngerung chirurgische Therapie

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Original Article

Introduction
Short bowel syndrome (SBS) is defined as malabsorption after congenital or acquired loss of part of the small intestine [3]. The incidence of neonatal SBS in a Canadian population-based study was 24.5 per 100 000 live births, with a reported mortality estimate for children under the age of 4 years of 2/100 000 population/year [10]. Since the first description of a longitudinal intestinal lengthening procedure by Bianchi in 1980, this technique has gained wide acceptance as the surgical therapy for short bowel syndrome in children [2]. With this technique, the dilated small bowel is divided longitudinally, two narrower loops are created and anastomosed in an isoperistaltic manner. This improves intestinal transport, prevents stasis of bowel contents and therefore prevents bacterial overgrowth. Furthermore, transit time is prolonged, and the contact area between intestinal mucosa and bowel contents is optimized [2, 7,11]. Nevertheless the indication to perform this procedure is rare, so that larger series are scarce. The aim of this report is to describe our series of 49 patients, who underwent a longitudinal intestinal lengthening procedure for SBS, with particular focus on the preoperative evaluation, technical surgical aspects and postoperative management.

Patients and Methods

Since 1982 49 patients underwent an intestinal lengthening procedure in our institution. Table 1 shows the entities which led to the short bowel syndrome. Indications for operation were: dependence on parenteral nutrition and impossibility of achieving at least 50 % of the caloric requirement enterally, after 6 months of adequate conservative treatment. Further indications were the inclusion of all intestinal segments into bowel continuity by anastomoses of eventual enterostomies. Preoperative studies included a thorough clinical examination, complete blood cell count, serum electrolytes, C-reactive protein, transaminases, bilirubin, acetylcholinesterase, total protein and albumin, fat-soluble vitamins, trace elements and coagulation tests (prothombin time, thrombin time and activated partial

Table 1

Entities leading to short bowel syndrome

18 14 10 7 49

Gastroschisis Small bowel atresia Midgut volvulus Necrotizing enterocolitis Total

Hosie S et al. Experience of 49 Eur J Pediatr Surg 2006; 16: 171 175

Original Article

Fig. 1 Small intestinal loop divided longitudinally at the mesenteric and anti-mesenteric sides. Note the branches of the mesenteric vessels supplying each bowel strip.

Fig. 2 A thinner loop was created by longitudinal suture of one bowel strip. The proximal part of the loop corresponds to the right side of the picture.

thromboplastin time). A gastrointestinal contrast study was performed in every case to evaluate the patency, length and dilatation of the remaining small bowel, and also the presence and length of the colon and, if clinically suspected, gastroesophageal reflux. Doppler imaging of the central vessels was performed when indicated, to assess patency and possible thrombosis. Serial blood culture as well as nasopharyngeal cultures were obtained to search for potential pathogens, since most patients were referred from other institutions and had spent most of their lives in hospital. In the last 5 patients, we included percutaneous liver biopsy and determination of single coagulation factors in the preoperative evaluation. The operative technique has been previously described [8, 9]. Briefly, only small bowel dilated to a diameter of at least double the normal size (about 5 cm) was considered adequate for the lengthening procedure. The bowel loop was divided longitudinally along the antimesenteric border using bipolar scissors. Division on the mesenteric side was accomplished in the same manner, after careful dissection of the small vessels supplying each half-circumference of the bowel loop (Fig. 1). Fashioning of the new bowel loops was accomplished by inverting running sutures; anastomoses were performed in an isoperistaltic manner (Figs. 2 and 3). Oral feeding was started after return of bowel function, usually on the 5th postoperative day. Feedings were progressively advanced until achieving 10 bowel movements per day. Solid food was introduced when formula was tolerated by the patient.

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Fig. 3 Small bowel loops after longitudinal intestinal lengthening. Longitudinal suture lines were covered with fibrin glue. After positioning the loops in a circular manner, the most proximal part, in continuity with the duodenum, corresponds to the lower loop on the left side of the picture. The right side of the lower loop has to be anastomosed with the left part of the upper loop. The right end of the upper loop is anastomosed to the colon.

tively and required resection. Two patients developed a leakage along the longitudinal suture, and one patient developed an intra-abdominal abscess necessitating re-laparotomy and drainage. Nine patients have died so far, which amounts to a mortality rate of 18 %. Causes of death are shown in Table 2. Follow-up of our patients showed that 19 patients were weaned from parenteral nutrition after a mean of 9.1 months (range 1 72 months). 5 patients still need parenteral nutrition at home 4 to 21 months postoperatively. 16 patients were lost to follow-up. Frequently encountered problems in the long term were bowel dysmotility secondary to recurrent dilatation of the lengthened bowel loops and bacterial overgrowth leading to steatorrhea, dHosie S et al. Experience of 49 Eur J Pediatr Surg 2006; 16: 171 175

Results
Patients mean age at the time of operation was 25 months with a range of 4 months to 12 years. Preoperatively the small bowel had a mean length of 27 cm (range, 12 to 60 cm). After the lengthening procedure, the mean small bowel length was increased to 51 cm (range 18 to 120 cm). There was no intraoperative mortality. As early complications we observed ischemia of a short bowel segment of 2 cm in two patients. This was noticed intraopera-

Table 2

Causes of mortality after longitudinal intestinal lengthening

4 3 1 1 9

Liver failure Sepsis Massive aspiration with gastroesophageal reflux Cardiac failure, multiple thromboses Total

Liver failure caused by progressive cholestasis due to long-term total parenteral nutrition and recurrent septicemias is the main cause of death in patients with SBS. In our series 4 out of 9 patients died of end-stage liver failure. Bianchi reported on a series of 20 patients who underwent a longitudinal lengthening procedure. Overall mortality was 55 %, in all cases due to end-stage liver failure [1]. For this reason we strongly recommend early referral to surgical therapy as soon as indicated. The prolongation of an unsuccessful conservative treatment with the risk of deterioration of liver function or other major complications is counterproductive. Dilatation of the small bowel on preoperative X-ray studies is most probably secondary to the adaptive response after massive intestinal loss. It should not be misinterpreted as secondary dilatation due to mechanical obstruction, since this could lead to further resection of vitally important bowel surface. In contrast to other authors we do not routinely perform longitudinal lengthening using a conventional stapling device, since the branches are very big [6, 7,11]. Thompson et al. reported necrosis of one of the divided bowel limbs, requiring resection, after a lengthening procedure performed with a stapler [6]. In our opinion careful dissection and sparing of the small mesenteric vessels is best accomplished with fine scissors. Bleeding is markedly reduced with the help of bipolar scissors. Inverted hand suturing allows the exact apposition of the intestinal wall, sparing the small mesenteric vessels. Furthermore this technique minimizes the loss of intestinal area due to the surgical procedure. Nevertheless, on one occasion we used an endoscopic linear cutter (Ethicon, Nordestedt, Germany) with good results. The instruments branches are small enough to be inserted in the triangle between the mesenteric bowel wall and the vessels supplying each bowel hemicircumference. Sealing of the suture lines with fibrin glue seems to be effective in preventing fistula formation and avoids traction on the mesenteric vessels. We have not observed any insufficiency of the suture lines since we routinely use fibrin glue. Like Bianchi, we consider an intestinal diameter of about 5 cm suitable for the lengthening procedure [1]. Weber considered a diameter of 3 cm adequate and used a stapling device in all cases except one. Five of his 16 patients developed bowel obstruction in the early postoperative period, which required re-operation [11]. We have not experienced this complication so far. The most frequent complication in the long term is recurrent dilatation of the lengthened bowel segments. This phenomenon leads to dismotility, stasis, bacterial overgrowth and malabsorption. In the past, these symptoms had to be treated conservatively with dietary measures and recurrent bowel decontamination with antibiotics, eventually leading to further problems such as candidiasis. Kim and coworkers recently published a surgical technique they called serial transverse enteroplasty (STEP). The bowel is lengthened by serial transverse incisions with a GIA stapler from opposite directions, creating a zig-zag loop [4]. Ample and long-term experience with this technique is still not available, therefore we would be hesitant to use it as the primary procedure for the surgical therapy of SBS at present. Nevertheless it might prove to be effective and safe in future, particularly

lactic acidosis requiring dietary measures and bowel decontamination, cholelithiasis and urolithiasis.

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Original Article

Discussion
Previous to considering a lengthening procedure the following conditions must be fulfilled: all intestinal segments must be included into bowel continuity by closure of enterostomies in order to recruit the entire resorption area available; allowance must be made for adequate bowel adaptation by offering oral feedings over a sufficient time interval; there must be a sufficient adaptive bowel dilatation of about 5 cm diameter; it must previously have been proved to be impossible to increase the enteral caloric intake despite adequate conservative treatment. Since these patients are frequently multimorbid, a careful preoperative evaluation is essential. In the early series we operated on patients with end-stage liver disease as an ultima ratio. All of them died of liver failure in the early postoperative period, which led us to exclude such patients from surgical therapy. It is imperative to optimize the patients preoperative condition, for example to compensate nutritional deficits such as deficits of vitamins (vitamin B12, fat-soluble vitamins such as vitamin K which are important for synthesis of coagulation factors) and trace elements, and also to correct electrolyte and acid-base disorders, anemia, coagulation disorders, thrombocytopenia and hypoalbuminemia. It is also highly important to detect and treat thrombosis resulting from the central venous catheter. Thorough bacteriological screening allows early institution of specific antibacterial therapy, and adequate perioperative prophylaxis, including antifungal agents when required. Frequently liver function will partially recover by reducing or cycling parenteral lipids. Some patients have a compensated functional impairment of the liver in spite of normal or nearly normal laboratory findings. They may acutely decompensate after an insult such as an operative procedure or a perioperative infection. One patient died in the early postoperative period from liver failure after a postoperative sepsis, although she had had normal preoperative laboratory tests. After this experience, we started to routinely perform a percutaneous liver biopsy preoperatively in order to assess the real liver status, and thus to be able to estimate risk and prognosis.
Hosie S et al. Experience of 49 Eur J Pediatr Surg 2006; 16: 171 175

as an option to treat recurrent dilatation after longitudinal intestinal lengthening [5]. Our series, the largest published so far, shows that the longitudinal intestinal lengthening procedure is a safe and effective surgical therapy for children with SBS, provided that the surgical therapy is performed early enough, before liver function deteriorates. A careful and extensive preoperative evaluation and therapy leading to an optimal preoperative condition is of vital importance. A careful surgical technique, which takes account of various surgical details, should reduce the complication rate and thus improve outcomes.

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Galea MH, Holliday H, Carachi R. Short-bowel syndrome: a collective review. J Pediatr Surg 1992; 27: 592 596 Kim HB, Fauza D, Garza J, Oh JT, Nurko S, Jaksic T. Serial transverse enteroplasty (STEP): a novel bowel lengthening procedure. J Pediatr Surg 2003; 38: 425 429 Kim HB, Lee PW, Garza J, Duggan C, Fauza D, Jaksic T. Serial transverse enteroplasty for short bowel syndrome: a case report. J Pediatr Surg 2003; 38: 881 885 Thompson JS, Pinch LW, Murray N, Vanderhoof JA, Schultz LR. Experience with intestinal lengthening for the short bowel syndrome. J Pediatr Surg 1991; 26: 721 724 Vernon AH, Georgeson KE. Surgical options for short bowel syndrome. Semin Pediatr Surg 2001; 19: 91 98 Waag K-L, Heller K. Surgical techniques in short-bowel syndrome. Progr Pediatr Surg 1990; 25: 81 89 Waag K-L, Hosie S, Wessel L. What do children look like after longitudinal intestinal lengthening? Eur J Pediatr Surg 1999; 9: 260 262 Wales PW, de Silva N, Kim J, Lecce L, To T, Moore A. Neonatal short bowel syndrome: population-based estimates of incidence and mortality rates. J Pediatr Surg 2004; 39: 690 695 Weber TR. Isoperistaltic bowel lengthening for short-bowel syndrome in children. Am J Surg 1999; 178: 600 604

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Original Article

Hosie S et al. Experience of 49 Eur J Pediatr Surg 2006; 16: 171 175