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Journal of Pediatric Gastroenterology & Nutrition:
doi: 10.1097/MPG.0b013e318230c27e
Original Articles: Gastroenterology

Intestinal Rehabilitation and Bowel Reconstructive Surgery: Improved Outcomes in Children With Short Bowel Syndrome

Khalil, Basem A.*; Ba’ath, Muhammad E.*; Aziz, Anuar*; Forsythe, Lynette*; Gozzini, Sara*; Murphy, Fiona*; Carlson, Gordon; Bianchi, Adrian*; Morabito, Antonino*

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Author Information

*Department of Paediatric Surgery, Royal Manchester Children's Hospital

Adult Intestinal Failure Unit, Hope Hospital, Manchester, UK.

Address correspondence and reprint requests to Mr Antonino Morabito, Honorary Senior Lecturer, University of Manchester School of Medicine, Consultant Paediatric and Neonatal Surgeon, Royal Manchester Children's Hospital, Oxford Road, Manchester M13 9WL, UK (e-mail: antonino.morabito@cmft.nhs.uk).

Received 8 December, 2010

Accepted 5 July, 2011

The authors report no conflicts of interest.

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Abstract

Background and Aim: Short bowel syndrome poses a great challenge to pediatric teams. Several innovative techniques in the management of total parenteral nutrition (TPN) and bowel reconstructive surgery have improved the outcomes of these children. The authors present their experience during the last decade as a specialist unit using improved techniques and multidisciplinary approaches in the management of this condition.

Methods: All of the children presenting with short bowel syndrome between 2000 and 2009 were identified. Diagnosis, length of residual gut, age at definitive surgery, length of gut prelengthening, length of gut postlengthening, TPN status, and survival were recorded. Median values were calculated.

Results: Twenty-seven children were identified (14 boys, 13 girls). Overall survival was 92%. Two children died. Nineteen children required bowel lengthening and 8 children had simple bowel reconstruction while on our protocol. Overall median age at definitive surgery was 12 months. Overall median residual gut length for these was 35.5 cm, whereas the median residual gut length for patients undergoing bowel lengthening was 25 cm. Postbowel lengthening, the median gut length was 90 cm. TPN data were unavailable for 2 patients. Overall, excluding the 2 patients who died and the 2 we have no TPN data on, of 23 patients, 21 (91%) are now off TPN.

Conclusions: Our series shows improved results not only with survival but also in the number of patients that are off TPN. Multidisciplinary approach consisting of both medical and surgical expertise is necessary in the management of these patients. The authors advocate centralisation of short gut services to experienced centers with multidisciplinary expertise.

See the Letters to the Editor in this issue for further information/commentary on this important topic.

Short bowel syndrome is a rare and serious condition. Most cases are due to gastroschisis, necrotising enterocolitis, midgut volvulus, and intestinal atresia (1). The definition of short bowel is still not clear; however, bowel length <100 cm in the first year of life is regarded to be abnormal. Less than 40 cm traditionally requires therapy according to the practice of most centers (2). It should also be noted that the gestational age of the child and the timing of the actual incident that caused short bowel will need to be taken into consideration when defining short bowel syndrome. In our unit, we define short bowel syndrome as a multisystemic disorder caused by inadequate length of small bowel usually less than half the expected for gestational age. Again, management will vary from patient to patient. The consequences of short bowel syndrome are huge. With most children dependent on total parenteral nutrition (TPN) for long periods of time, damage to the liver is common. Several medical therapies have been used to enhance bowel adaptation. TPN is used to enhance growth and nutrition of the child until adaptation occurs. In the event of failed adaptation and in the face of liver failure and reduced venous access, transplantation becomes the only hope for these children (3). Transplantation in this unfortunate group of patients usually involves combined liver and small bowel transplant. In a few cases in which the liver has not experienced irreversible damage, isolated intestinal transplant could be performed. In the former group, portal hypertension is a potential risk factor; however, there are encouraging results in the field of transplantation with combined liver/small bowel transplant and isolated intestinal transplant. The long-term results of bowel transplantation are under review. The management of these patients postoperatively is complex and morbidity is high. Surgical reconstruction of the bowel in short gut infants has been used since the 1960s (4,5); however, actual autologous bowel lengthening procedures started after Bianchi (6) published his procedure in 1980. Since then, several centers have performed the Bianchi procedure with varying degrees of success (7). Recent reports have shown clear benefit of bowel lengthening in patients with short bowel syndrome. These benefits include more rapid weaning off TPN and enhanced growth and enteral autonomy (8). In 1999, Bianchi published a series of 20 cases that had been performed since 1982. In that series, the survival rate was 45% (9). After 1999, our center embarked on a multisystemic approach to the management of short bowel syndrome. This included novel techniques using hepatosparing TPN, bowel expansion, enhanced adaptation, and bowel lengthening. The present study describes our techniques and looks at their effect on the outcome of another 27 patients in the last 10 years.

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INTESTINAL REHABILITATION PROGRAMME

This programme is a focused patient management system, not based on surgical procedures only but on “what to do for the patients rather than to the patients.” The programme has several key points, which are summarised in Table 1. The points are described in the following sections.

Table 1
Table 1
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Central-line Insertion

We use an open technique for inserting our central lines. We usually use the smallest possible catheter that can be reasonably used. Care of the central line involves regular use of urokinase and/or 70% alcohol lock to avoid blockage of the catheter (10,11). Central-line infections are treated promptly with empirical antibiotics (based on previous infection if recorded) until microbiological cultures and sensitivities are available; however, if the child clinically deteriorates, the catheter is removed and another is placed using the same vein (if possible) but a different tract.

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TPN

We had good results with the “hepatosparing” TPN regimen, which consists of fat-free/fat-reduced (nil to 0.5 g · kg−1 · day−1) 3.75 g · kg−1 · day−1 of protein and 14 g · kg−1 · day−1 of glucose during the first 4 weeks of life and during episodes of sepsis and a low-fat regimen (1–1.5 g · kg−1 · day−1) with the same amount of protein and glucose in the typical situation. All of our patients are fed orally and feeding adds more energy to their daily intake. This supplemental TPN regime provides approximately 81.8 kcal · kg−1 · day−1. We emphasise that children who receive no fat in their TPN do receive some fat via enteral feeds. Thus, fat-free TPN does not mean fat-free nutrition. As bowel adaptation increases and better absorption of feeds occurs, the TPN is weaned as tolerated. Essential fatty acids are given separately in addition to the TPN as a bolus. We have used the low-fat regimen to rescue liver function in patients referred to us with TPN-associated liver disease.

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Enteral Feeds

Oral feeding is generally started as soon as possible with normal breast milk or formula and patients are weaned at the appropriate time. There is a chance that these patients need a special diet to enhance absorption and adaptation. Specialist dieticians review the child regularly and advise parents and staff on the necessary feeds. We avoid gastrostomy insertions as much as possible. We are aggressive with enteral feeds and aim to provide the child the full expected volume of feeds. Stoma losses are replaced with intravenous normal saline infusions with or without potassium. Stoma output replacement varies from patient to patient. Some are milliliter per milliliter and some are half replacement, whereas others have their average daily losses replaced as part of their TPN volume. Serum electrolytes and fluid balance dictate the method used.

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Surgery

Bowel preservation is essential and minimal surgery at birth is indicated.

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Initial Bowel Expansion

We have used initial bowel expansion in children with short bowel whose bowel has not been dilated. This technique has been described in detail by Bianchi (12) and a summary is given here. A catheter is placed in the distal end of the proximal small bowel and secured using a purse-string suture. The end is then sutured to the inside of the anterior abdominal wall, as in a tube jejunostomy. The catheter is then brought out of the abdominal wall as a proximal tube stoma. The colon or its remnant is treated the same way. The level of stomas depends on the remnant bowel. The child is fed postoperatively and the proximal tube stoma is clamped for progressively longer periods after feeds. The aim is to achieve circumferential expansion of the bowel to about twice its original size. The progressive bowel expansion also increases the absorptive surface area of the gut, allowing for more absorption of nutrients. Once the child can tolerate full feeds with the tube clamped for 4 hours after a feed, we regard the bowel to be fully expanded. This usually takes about 6 to 12 weeks of expansion, but it can take up to 24 weeks in cases of ultrashort gut. If expansion started right from birth, we would wait until the child is at least 6 months of age before embarking on further reconstructive surgery to enhance full gut adaptation.

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Bowel Lengthening

Once the child has achieved maximal expansion as above and is older than 6 months of age, bowel lengthening is performed. Our team uses the Bianchi technique because we have almost 30 years experience with this procedure (Fig. 1). Longitudinal intestinal lengthening and tailoring (LILT) is performed on the expanded gut, as originally described by Bianchi. In patients who have been referred to us from other units, lengthening is performed once the child is in good clinical condition, has stable liver function tests, and if the bowel is already dilated, albeit in an uncontrolled fashion; however, if the bowel was not dilated, we would embark on an expansion programme first before lengthening. The pre- and postbowel lengthening gut lengths are measured and documented. Pre- and postlength are important to assess the efficacy of the lengthening operation. In children with <30 cm of small bowel, length is important because they have less absorptive capacity and faster transit time. In children who have dilated bowel >30 cm, rather than performing tapering procedures, which lose bowel surface area, the authors use bowel lengthening as a tailoring procedure and mucosal sparing procedure as well as achieving more length.

Figure 1
Figure 1
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Post-Bianchi Procedure

The child is progressively weaned off TPN as tolerated and enteral feeding is continued until the child gains full enteral autonomy with a healthy liver. TPN cycling is an integral component of weaning in our center.

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Social Integration

The programme should be formulated in the hospital but delivered as much as possible at the patient's home, with short and selected trips to the hospital. School-age children should be slowly reintegrated in school.

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METHODS

All of the patients with short bowel syndrome managed by this team between 2000 and 2009 were identified and the notes retrieved. Primary diagnosis, length and state of the gut, length of time on TPN before reconstructive surgery, type of reconstructive surgery, length of time on TPN postoperatively, need for transplantation, and mortality were recorded. Median values were used.

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RESULTS

Twenty-seven patients were identified (14 boys, 13 girls) in the 10-year period 2000 to 2009. The gestational age for 19 patients was available. Median gestational age was 35 weeks (range 24–38). The birth weight for 19 patients was also available. Median birth weight was 1.95 kg (range 0.64–3.1 kg). Two patients in the series had their ileocecal valve and the whole colon. The rest had lost their ileocecal valve and ascending colon. Sixteen patients had gastroschisis, 5 had intestinal atresia, 4 had necrotising enterocolitis, whereas 1 patient each had intestinal ganglioneuroma and Hirschsprung disease. Of the 16 patients with gastroschisis, 5 had an associated atresia, 2 had an associated midgut volvulus, and 2 developed necrotising enterocolitis. One patient with small bowel atresia also had meconium ileus. The patient that had ganglioneuroma developed short gut following resection of the lesion. He was left with 20 cm of gut. The child with Hirschprung disease developed short bowel syndrome as a result of multiple gut resections before being transferred to our unit. Overall, median age at definitive reconstructive surgery was 12 months (range 1 day–129 months). Data on residual gut length at initial laparotomy were available for 18 patients. Median residual gut length for these was 35.5 cm (range 10–100 cm). Eight patients were managed on our protocol and on definitive surgery did not need bowel lengthening. Nineteen patients underwent LILT. These patients had a median initial residual bowel length of 25 cm. Median length of bowel found pre-LILT was 60 cm (range 18–140 cm). Post-LILT, median bowel length was 90 cm (range 37–260 cm). Twenty-five patients survived giving an overall survival of 92%. Two patients died. One died after liver and small bowel transplantation following failure of gut adaptation. He died at age 7 years. The second died of liver and multiorgan failure 63 days postsurgery. She was 3 years old.

Of the 25 survivors, 7 were managed postoperatively in other centers (5 were outside the UK). The exact length of time of postoperative TPN is unavailable for these 7 patients, but we know from contacts with these centers that at least 5 of these patients are off TPN. Postoperative TPN data regarding the other 2 patients are unavailable. Of the 18 patients who were managed postoperatively in our unit, only 2 patients remain on TPN. One of these actually came off TPN postoperatively but developed intestinal obstruction several months after lengthening and was managed in another center. We have been told that the child went back on TPN and is being weaned off. The other 16 patients are all off TPN at a median time of 6 months postreconstructive surgery (range 2 weeks–12 months). Overall, excluding the 2 patients who died and the 2 we have no TPN data on, of 23 patients, 21 (91%) are now off TPN. The median weight centile presurgery was the 0.4th percentile. This improved to a median of the 9th percentile after surgery. Further breakdown of the data into 2 groups is as follows: group 1 that had LILT and group 2 that did not have LILT are shown in Tables 2 and 3, respectively. Generally, infants presurgery showed delayed milestones, which were later achieved postsurgery. All of our children who are of school age attend mainstream schools.

Table 2
Table 2
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Table 3
Table 3
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DISCUSSION

The management of short bowel syndrome has evolved in the last decade because of better understanding of the physiology of patients with short bowel and their family needs. A healthy patient undergoing an elective bowel lengthening following controlled dilation stands a higher chance of success than one who undergoes such procedures in an emergency situation.

Surgery is not “another operation” but part of a structured programme, which starts with the prevention of central line sepsis and preservation of the available bowel and continues with a lengthening procedure or procedures. For this reason, we do not acknowledge treatment as a single process. Surgery is therefore an approach to bowel reconstruction termed “autologous gastrointestinal bowel reconstruction.” As a consequence, our improved outcomes are primarily the result of better timing of the optimal surgical techniques, appropriate use of TPN in the right concentrations, early introduction of enteral feeds, and central line preservation. A healthy liver is necessary for optimum gut function and good overall outcome. Survival alone is not a reliable measurement of good outcome because survivors and their families demand a good quality of life. An essential part of the intestinal rehabilitation programme is controlled tissue expansion that chronically enhances bowel absorptive capacity by contact with nutrients, thus increasing enteral feed tolerance and reducing the need for TPN. Bowel expansion is indicated in patients whose bowel is not dilated. By doubling the surface area of the bowel, subsequent lengthening achieves double the length with normal circumference, thus increasing absorptive area rather than lengthening with normal circumference, which ends up with double length but half circumference of the loops. Tissue expansion as described in the present study is not achieved by anastomosing pathologically dysmotile, nonperistalsing, or dilated proximal bowel to collapsed and nonused distal bowel. It is achieved by graded and controlled clamping of the proximal stoma. This avoids stasis, translocation, sepsis, feed intolerance, feed aversion, and loss of venous access. The catheter enterostomy allows bowel emptying and bowel washout or “housekeeping” on a regular basis, aiming to keep the bowel mucosa healthy. We have had cases of children with a reasonable length of bowel being referred to us with a diagnosis of intestinal failure. On laparotomy, we have found that the bowel was dilated and dysmotile because of functional obstruction as a result of anastomosing large dilated bowel to collapsed distal bowel. In these cases, if the bowel is healthy, tailoring alone is an option, but because some of these children did have large portions of gut resected, we opted to do a LILT rather than “throw away” bowel with an essential amount of mucosa. As the absorptive capacity of the bowel increases, use of TPN with its attendant liver problems decreases (13). It must be emphasised that it is oral feeding and not gastrostomy or continuous nasogastric feeding that plays an essential role in controlled tissue expansion. Bowel mucosa is not designed to receive feeds continuously for 24 hours. That is not to say that it cannot, but the authors believe that the nearer management is to normal physiology, the better it is for the patient. Patients who have deranged liver function tests are extensively investigated in our unit. If no portal hypertension is present, then a liver rescue regimen is applied. This involves no-fat/low-glucose TPN and aggressive enteral feeding. The bilirubin and the liver function tests are monitored. In our experience of several cases (including children who do not have short gut), this regimen is successful in normalising the liver function. Indeed, children with bilirubin levels >200 μmol/L have been managed successfully on this regimen. We would accept a transient loss of weight or static weight gain if the liver functions showed a trend to normalisation before cautious restarting of the fat.

The use of new lipid formulation (soybean, coconut, olive, and fish oils) to help prevent TPN-related cholestasis has been introduced in the UK and could provide a new, successful way of treating these patients (14). We presently have 2 patients on the intestinal rehabilitation programme using SMOF, but it is too early to draw conclusions with regard to outcomes. A recent randomised controlled trial showed that SMOF was safe and well tolerated in children and reduced plasma bilirubin level (15,16). It is important to note that in this series, the cautious use of intralipid in a hepatosparing TPN protocol kept these patients alive with good liver function. It is extremely imperative to protect the liver in these children. The 2 children who died in our series had significant liver disease.

In children who have had previous surgery and have developed a physiological obstruction and bowel dilatation, a contrast study is used to further assess this and an appropriate surgical plan is formulated thereafter. A laparotomy is usually necessary to formally assess the bowel. If on laparotomy the bowel is found to be dilated and healthy (healthy mucosal involutions), then lengthening is performed. If, however, the bowel is dilated but evidence of chronic mucosal inflammation is seen, then we recommend that lengthening be postponed and tube stomas be formed to allow the gut to recover. In cases in which the gut is not dilated, the length of the gut is measured taking into account the presence of the ileocecal valve and the residual colon. If it is deemed that more length is needed, then tube stomas are fashioned and expansion is commenced with a view to lengthening in the future. We have also noticed that children who initially presented with short gut during the neonatal period would have naturally increased their gut length at the time of lengthening. In such children, if the gut is dilated, then a LILT is performed. Thus, the 2-step autologous gastrointestinal bowel reconstruction consists of initial bowel expansion for undilated gut followed by bowel lengthening. Further lengthening procedures may be done if the patient fails to achieve enteral autonomy; however, if there is no gut dilation and both proximal and distal bowel are healthy and it is deemed that there is possibly enough bowel, we would give the child a chance of end-to-end anastomosis. It is extremely important to consider that the length of the residual gut at initial surgery would not be the same months after the initial procedure, as is shown by our data. This has significant implications when sending children for transplantation on the basis of an initially ultrashort gut, which may have increased in length and may be simply dysmotile because of a functional obstruction that could be resolved by elective bowel reconstruction rather than by transplantation. Recently, our unit has used the serial transverse enteroplasty procedure (STEP) procedure published by Kim et al (17) in managing a patient who had dilated bowel but was deemed to have sufficient length. The STEP procedure is a complementary procedure to our existing armamentarium and should be considered in the protocols of specialist centers addressing the short bowel state. The STEP procedure is used as a mucosal sparing and tapering procedure to improve function. Its role in providing length is only 68%. It can be used following a Bianchi procedure to achieve more length if desired. If adequate residual length is present (>40 cm), the STEP procedure may be of use if the bowel is dilated. We do not use the STEP procedure as the primary procedure in children with <40 cm of bowel but reserve it in case a second lengthening is needed. There are 111 patients on the international STEP registry as of September 2010 (personal communication). According to the registry, the STEP procedure has a 34% success rate of weaning off TPN at a median follow-up of 12.6 months (18).

Our study also demonstrates the necessity, and indeed, difficulty, in maintaining efficient lines of communication with referring centers, especially with international referrals. We have partial data on 5 children referred from outside centers and another 2 children have been lost to follow-up. Centralisation of short gut services may provide better and more efficient guidelines on maintaining communication with national and international referrals.

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CONCLUSIONS

Overall, our experience shows that using a multidisciplinary approach, combining both medical and surgical expertise, patients with short bowel syndrome can achieve enteral autonomy.

The use of the intestinal rehabilitation programme has helped us to improve results in the management of short gut syndrome. The target is to achieve enteral autonomy with preservation of liver function. We propose that patients with short bowel syndrome be treated in specialist units with appropriate multidisciplinary expertise.

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REFERENCES

1. Wales PW, Christison-Lagay ER. Short bowel syndrome: epidemiology and etiology. Semin Pediatr Surg 2010; 19:3–9.

2. Soden JS. Clinical assessment of the child with intestinal failure. Semin Pediatr Surg 2010;19:10–9.

3. Nayyar N, Mazariegos G, Ranganathan S, et al. Pediatric small bowel transplantation. Semin Paediatr Surg 2010;19:68–77.

4. Hammer JM, Seay PH, Johnston RL, et al. The effect of antiperistaltic bowel segments on intestinal emptying time. Arch Surg 1959; 79:537–541.

5. Baldwin-Price HK, Copp D, Singleton AO Jr. Reversed intestinal segments in the management of anenteric malabsorbtion syndrome. Ann Surg 1965:161;225–30.

6. Bianchi A. Intestinal loop lengthening—a technique for increasing small intestinal length. J Pediatr Surg 1980; 15:145–151.

7. Reinshagen K, Kabs C, Wirth H, et al. Long-term outcome in patients with short bowel syndrome after longitudinal intestinal lengthening and tailoring. J Pediatr Gastroenterol Nutr 2008; 47:573–578.

8. Reinshagen K, Zahn K, Buch C, et al. The impact of longitudinal intestinal lengthening and tailoring on liver function in short bowel syndrome. Eur J Pediatr Surg 2008; 18:249–253.

9. Bianchi A. Experience with longitudinal intestinal lengthening and tailoring. Eur J Pediatr Surg 1999; 9:256–259.

10. Onland W, Shin CE, Fustar S, et al. Ethanol-lock technique for persistent bacteremia of long-term intravascular devices in pediatric patients. Arch Pediatr Adolesc Med 2006; 160:1049–1053.

11. Kethireddy S, Safdar N. Urokinase lock or flush solution for prevention of bloodstream infections associated with central venous catheters for chemotherapy: a meta-analysis of prospective randomized trials. J Vasc Access 2008; 9:51–57.

12. Bianchi A. From the cradle to enteral autonomy: the role of autologous gastrointestinal reconstruction. Gastroenterology 2006; 130:S138–S146.

13. Walker SR, Nucci A, Yaworski JA, et al. The Bianchi procedure: a 20-year single institution experience. J Pediatr Surg 2006; 41:113–119.

14. Le HD, Fallon EM, de Meijer VE, et al. Innovative parenteral and enteral nutrition therapy for intestinal failure. Semin Pediatr Surg 2010; 19:27–34.

15. Goulet O, Antébi H, Wolf C, et al. A new intravenous fat emulsion containing soybean oil, medium-chain triglycerides, olive oil, and fish oil: a single-center, double-blind randomized study on efficacy and safety in pediatric patients receiving home parenteral nutrition. JPEN J Parenter Enteral Nutr 2010; 34:485–495.

16. Goulet O, Joly F, Corriol O, et al. Some new insights in intestinal failure-associated liver disease. Curr Opin Organ Transplant 2009; 14:256–261.

17. Kim HB, Fauza D, Garza J, et al. Serial transverse enteroplasty (STEP): a novel bowel lengthening procedure. J Pediatr Surg 2003; 38:425–429.

18. Jones BA, Hull MA, Kim HB. Autologous intestinal reconstruction surgery for intestinal failure management. Curr Opin Organ Transplant 2010; 15:341–345.

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Keywords:

intestinal rehabilitation; short bowel

Copyright 2012 by ESPGHAN and NASPGHAN

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