Long-term Survival and Parenteral Nutrition Dependence in Adult Patients With the Short Bowel Syndrome

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1 GASTROENTEROLOGY 1999;117: ALIMENTARY TRACT Long-term Survival and Parenteral Nutrition Dependence in Adult Patients With the Short Bowel Syndrome BERNARD MESSING,* PASCAL CRENN,* PHILIPPE BEAU, MARIE CHRISTINE BOUTRON RUAULT,* JEAN CLAUDE RAMBAUD,* and CLAUDE MATUCHANSKY* *Department of Hepatogastroenterology and Nutrition Support and INSERM Unité 290, Hôpital Lariboisière-Saint-Lazare, Paris; and Department of Hepatogastroenterology and Nutrition Support, Hôpital La Milétrie, Poitiers, France Background & Aims: The short bowel syndrome (SBS) may be associated with either transient or permanent intestinal failure, presently treated by parenteral nutrition (PN). Survival and PN-dependence probabilities, taking into account both small bowel remnant length and the type of the digestive circuit of anastomosis, are not known in adult SBS patients. The aim of this study was to assess such prognostic factors. Methods: A total of 124 consecutive adults with nonmalignant SBS were enrolled from 1980 to 1992 at 2 home PN centers. They were analyzed for survival and PNdependence probabilities using the Cox model and for PN dependence using linear discriminant analysis. Data were updated in April Results: Survival and PN-dependence probabilities were 86% and 49% and 75% and 45% at 2 and 5 years, respectively. In multivariate analysis, survival was related negatively to end-enterostomy, to small bowel length of F50 cm, and to arterial infarction as a cause of SBS, but not to PN dependence. The latter was related negatively to postduodenal small bowel lengths of F50 and cm and to absence of terminal ileum and/or colon in continuity. Cutoff values of small bowel lengths separating transient and permanent intestinal failure were 100, 65, and 30 cm in end-enterostomy, jejunocolic, and jejunoileocolic type of anastomosis, respectively. Conclusions: In adult SBS patients, small bowel length of F100 cm is highly predictive of permanent intestinal failure. Presence of terminal ileum and/or colon in continuity enhances both weaning off PN and survival probabilities. After 2 years of PN, probability of permanent intestinal failure is 94%. These rates may lead to selection of other treatments, especially intestinal transplantation, instead of PN, for permanent intestinal failure caused by SBS. The crucial role of home parenteral nutrition (HPN) in the treatment of adult patients with intestinal failure, % 68% of whom have short bowel syndrome, 1,5 7 has been documented extensively. Three studies examined 3 5-year survival of patients receiving HPN, 1,2,7 but there seem to be no data specifying survival and parenteral nutrition (PN)-dependence probabilities for patients with the short bowel syndrome. Such data could contribute to a better understanding of intestinal failure caused by short bowel syndrome, which is the main reason for small bowel transplantation, as recently shown in the small bowel transplantation international registry. 8 The normal length of adult small bowel ranges from 3 to 8 m depending on methods of measurement; short bowel is generally defined as a remnant length of cm. 9,10 In patients with short bowel syndrome, PN dependence is thought to be influenced by the length of remnant small bowel and the type of the digestive circuit (end-enterostomy, jejunocolic, or jejunoileocolic) of anastomosis, because preservation of the ileocecal valve and colon improves oral water-mineral and energy balances. 11,12 We now report long-term survival and PN-dependence probabilities in 124 consecutive adult patients with nonmalignant short bowel syndrome. Materials and Methods Patients From January 1980 to December 1992, all consecutive adult patients with short bowel syndrome defined as remnant postduodenal small bowel length of 150 cm, half the shortest normal small bowel length in adults, 10 were included in the study. Data collection ended in April Bowel rehabilitation strategies, i.e., growth hormone treatment, 13 surgically reversed small bowel loop, 14 and intestinal transplantation, were then implemented at 1 of the 2 centers involved (Saint-Lazare Hospital). We excluded (1) patients with severe visceral failure at the time of short bowel occurrence (n 2); (2) patients with evolving primary malignancy either present at Abbreviations used in this paper: CI, confidence interval; HPN, home parenteral nutrition; PN, parenteral nutrition; RR, relative risk by the American Gastroenterological Association /99/$10.00

2 1044 MESSING ET AL. GASTROENTEROLOGY Vol. 117, No. 5 the time of short bowel occurrence (n 3) or recurring during follow-up (n 11); or (3) patients who had received other treatments than HPN for intestinal failure, e.g., growth hormone (n 0) 15,16 or reconstructive surgery of the remnant bowel such as surgically reversed small bowel loop (n 3) 17 or small bowel transplantation (n 0). 8 Patients with nondigestive organ failure and/or primary malignancy that started after short bowel constitution were included. Small bowel length was measured from the x-ray films of the latest barium meal follow-through by using an opisometer, a hand-held device used for measuring distances on maps. Opisometry results have been shown to correlate significantly with results of peroperative measurements of small bowel length. 18 Recorded length was measured along the antimesenteric side of the small intestine, 18 and is the mean of measurements obtained independently by 3 of the authors (B.M., P.C., and P.B.). The mean coefficient of variation was 4.9% (range, 0% 11.9%). Study Design Patients were enrolled and monitored at Saint-Lazare Hospital, Paris (n 80), and La Milétrie Hospital, Poitiers (n 44), 2 authorized French HPN centers for adults, one for the Ile-de-France and the other for Poitou-Charentes region, respectively. According to national administrative rules in France, all patients requiring HPN have to be treated and monitored under the responsibility of an authorized regional HPN center. 7 Forty patients in this series were included in a previous study reporting the 5-year survival rate of 217 patients receiving HPN. 7 The 2 HPN centers filled out a questionnaire for all patients matching the inclusion criteria. Data records included patients demographics (HPN center, sex, and age) and characteristics of intestinal tract, reasons for short bowel constitution, PN dependence, and cause of death. Intestinal tract characteristics were (1) time of surgery leading to short bowel and, if any, subsequent reestablishment of digestive continuity; (2) site (jejunum, ileum) and postduodenal length of remnant bowel; (3) digestive circuit type 1 (end-enterostomy), 2 (jejunocolic anastomosis), or 3 (jejunoileocolic anastomosis), i.e., without or with ileocecal valve and entire colon or part of it in continuity, respectively; and (4) presence or absence of radiographic abnormalities of remnant small bowel, recorded on barium meal follow-through. Weaning off PN was performed as described previously. 19 Briefly, immediately after the postoperative period, when oral intake was resumed, the number of PN infusions per week was gradually reduced by eliminating 1 or 2 infusions every second week during a 1 2-month period. In case of weight loss of 3 kg/mo, PN was reestablished at the previous level. Further attempts of PN weaning were made with the same protocol if a weight gain of 3 kg occurred later, in case of hyperphagiaassociated oral intake. 20 The dietary program was based on free solid food ingestion 20 instead of tap water restriction and, especially for patients with end-enterostomy, the use of either oral rehydration solution 10 or mineral Vichy-St-Yorre water (Société Commerciale des Faux Minérales du Bassin de Vichy, St-Yorre, France) containing 70 mmol/l Na. None of the patients was given oral supplements, oral medium-chain triglycerides, or oral or intravenous glutamine. Successful weaning off PN, i.e., recovery of full oral nutrition autonomy, was considered to be achieved when satisfactory nutritional status, as classified by Detsky et al. 21,22 into grades A (well-nourished) or B (moderately malnourished), was maintained for at least 1 year after end of PN. These weaned patients were classified as having transient intestinal failure. Patients either not weaned off PN or with severe persistent malnutrition (grade C in the classification by Detsky et al. 21,22 ) or with a relapse within 1 year of PN cessation were classified as being PN dependent or having permanent intestinal failure. Statistical Analysis All patients were followed up until death or April 1996, i.e., 40 months after the end of the inclusion period. Median follow-up was 64 months (range, months). Duration of PN was calculated from the date of the last surgical modification of digestive circuit, up to death, PN cessation, or end of follow-up for nonweaned living patients. Survival time was calculated from the date of surgery having led to short bowel to death or until April PN-dependence and survival probabilities were calculated using the Kaplan Meier method. 23 PN-dependence and survival variables were compared using univariate and multivariate analyses. PNdependence and survival distributions were compared using the log rank test, with P values of 0.05 considered statistically significant, in accordance with HPN center, patients sex and age, period of surgery leading to short bowel ( vs ), cause of bowel resection, length of remnant small bowel, radiographic abnormalities on remnant small bowel, existing ileocecal valve and cecum, presence of at least part of the colon in continuity, and, for survival analysis, PN dependence as defined above. Categories for age and remnant small bowel length were defined as approximate tertiles: 3 groups of equal size, with cutoffs chosen at 40 and 60 years for age and at 50 and 100 cm for small bowel lengths. If relative risks in 2 adjacent categories did not significantly differ, they were grouped together. 24 To identify independent factors contributing to PN dependence and survival, 2 Cox proportional hazard models 25 were then adjusted to the above-mentioned variables with an ascending stepwise procedure using BMDP statistical software. 26 In the multivariate procedure, P value of 0.10 was considered as the level of significance. Using the relative survival (RELSURV 1.0) program, 27 the patients age and sex and the risk factors selected with the Cox model were then tested for their significance on relative survival. 28 The latter was calculated as the observed-to-expected survival ratio in an age- and sex-matched group using French population statistics for the period provided by the Institut National de la Statistique et des Etudes Economiques. PN dependence was also studied using linear discriminant analysis 29 to determine the cutoff values of remnant short bowel lengths according to types 1, 2, or 3 of the digestive circuit and the absence or presence of radiographic abnormalities on remnant small bowel. Sensitivity of the model was defined as the proportion of

3 November 1999 OUTCOME IN ADULT SHORT BOWEL PATIENTS 1045 patients weaned off PN among those with a bowel length above the cutoff and specificity as the proportion of nonweaned patients among those with a bowel length below the cutoff. Comparison of small bowel lengths between the 3 types of digestive circuit was assessed by Mann Whitney rank sum test. Quantitative variables were expressed as median and ranges; relative risks (RRs) were provided with 95% confidence intervals (CIs). Results Patient Characteristics One hundred twenty-seven patients fulfilled inclusion criteria; 3 patients were lost to follow-up. Thus, 124 patients aged 52 years (range, 17 87) at time of short bowel constitution were available for analysis. Their demographic and digestive characteristics are shown in Tables 1 and 2, respectively. The median length of remnant small bowel was 63 (range, 0 150), 66 (0 150), and 85 (15 150) cm in digestive circuit types 1, 2, and 3, respectively (NS). The median length of remnant ileum, in continuity with ileocecal valve and cecum, present in only type 3 patients, was 30 (5 120) cm. Continuity of intestinal circuit was reestablished simultaneously to short bowel constitution in 54 cases (41 of type 2 and 13 of type 3 circuit) and after 3 months (range, 1 23) in 52 cases (37 of type 2 and 15 of type 3). Table 1. Demographic Characteristics of 124 Adult Patients With Nonmalignant Short Bowel Syndrome No. of Characteristics patients (%) Sex Male 62 (50) Female 62 (50) Age at time of short bowel constitution ( yr ) (34) (33) (34) Date of short bowel constitution (35) (65) Cause of bowel resection Mesenteric infarction 50 (40) Arterial/venous 41/9 Radiation enteritis 28 (23) Crohn s disease 11 (9) Postsurgical complications 9 (7) a Small bowel volvulus 8 (7) Benign tumors 5 (4) b Miscellaneous 13 (10) c a Six cases of peritonitis and 3 small bowel fistulas. b Including 3 cases of desmoid tumors associated with familial adenomatous polyposis coli. c Including 5 cases of small bowel obstructing bands and 2 cases of chronic intestinal pseudo-obstruction. Table 2. Digestive Characteristics of 124 Adult Patients With Nonmalignant Short Bowel Syndrome No. of Characteristics patients (%) Remnant small bowel length (cm) (35) (31) (34) Digestive circuit type of anastomosis End-enterostomy (type 1) 18 (14) Jejunocolic anastomosis (type 2) 78 (63) Jejunoileocolic anastomosis (type 3) 28 (23) Radiographic abnormal pattern of remnant small bowel Present a 24 (19) Absent 100 (81) Other digestive features Left colostomy 12 (10) Duodenopancreatectomy 3 (2) a Modified mucosal folds and/or nonocclusive stenoses in 14 of 28 patients with radiation enteritis, 4 of 11 with Crohn s disease, 3 of 41 with arterial ischemic enteritis as cause of bowel resection, and 3 of 13 with miscellaneous diseases; none of the patients had occlusive stenoses. PN Dependence Sixty patients (48%) were PN dependent and had permanent intestinal failure (56 could not be weaned off PN and 4 developed severe malnutrition within 1 year after PN). Sixty-four patients (52%) were weaned off PN and had transient intestinal failure. PN lasted for 44 (range, 1 160) and 0.5 (0.5 46) months in patients with permanent and transient intestinal failure, respectively. In the transient intestinal failure group, early weaning off PN with PN duration of 1 month after the last surgical modification of digestive circuit was achieved in 34 (27% of the whole group) cases, and late weaning after a PN duration of 3 (1.5 46) months in 30 (24%) cases. PN-dependence probabilities are shown in Figure 1. Figure 1. Probability of PN dependence (Kaplan Meir curve) in 124 adult patients with nonmalignant short bowel syndrome. Vertical bars indicate 95% CIs at 1, 2, and 5 years of follow-up. PN-dependence probabilities were 53% (95% CI, 44 62), 49% (40 58), and 45% (35 55) at 1, 2, and 5 years, respectively.

4 1046 MESSING ET AL. GASTROENTEROLOGY Vol. 117, No. 5 Variables that significantly influenced PN dependence in univariate and multivariate (Figure 2) analyses are shown in Table 3. In 95% of cases of transient intestinal failure, weaning off PN was achieved within 24 months of PN, and 94% of patients who were not weaned off PN after 2 years of PN were ultimately classified as having permanent intestinal failure. Cutoff values of remnant small Figure 2. PN dependence of 124 adult patients with nonmalignant short bowel syndrome. Significant factors for PN dependence were (A) postduodenal remnant small bowel length, with 5-year probabilities of 9% (95% CI, 0 18), 37% (19 55), and 83% (71 95) for remnant lengths of , 50 99, and 50 cm, respectively; (B) presence (type 1) or absence (types 2 and 3) of end-jejunostomy, with 5-year probabilities of 78% (54 100) and 39% (29 49), respectively; and (C) presence (type 3) or absence (types 1 and 2) of ileocecal valve and cecum, with 5-year probabilities of 15% (0 31) and 52% (41 63), respectively. Distributions were compared using the log rank test. bowel lengths that significantly differentiated patients with transient from those with permanent intestinal failure are shown in Table 4. Survival and Causes of Death Forty (32%) patients including 32 (53%) of the 60 with permanent intestinal failure and 8 (12.5%) of the 64 with transient intestinal failure died during followup. Causes of death (Table 5) were related to the primary disease having led to short bowel in 15 patients, 12 of whom died of extradigestive vascular complications. Survival probabilities are described in Figure 3. Variables that significantly influenced survival in univariate and multivariate analyses are shown in Table 3. In univariate analysis, survival probability was lower (P 0.001) in patients with permanent intestinal failure (87% [95% CI, 79 95], 73% [62 84], 61% [49 73], and 40% [25 55] at 1, 2, 5, and 10 years of follow-up, respectively) than in patients with transient intestinal failure (100%, 97% [93 100], 87% [78 96], and 80% [63 93], respectively). However, in multivariate analysis, PN dependence was no longer a significant factor of survival. Relative survival analysis showed that remnant small bowel length of 50 cm (RR, 7.7 [95% CI, ]), type 1 digestive circuit (RR, 6.2 [ ]), and arterial mesenteric infarction as a cause of short bowel (RR, 4.8 [ ]) remained significantly associated with decreased survival rate (Figure 4); age 60 was no longer significant (RR, 1.7 [ ]). Among the 40 patients with permanent intestinal failure aged 60, deemed as potential candidates for small bowel transplantation, survival probability was 87% (95% CI, 77 97), 77% (66 88), 62% (47 77), and 44% (36 62) at 1, 2, 5, and 10 years of follow-up, respectively. Discussion We report survival and PN-dependence probabilities of 75% and 45% at 5 years, respectively, in a cohort of 124 adults with nonmalignant short bowel syndrome, enrolled within a 13-year period of study. In multivariate analysis, survival was negatively related to digestive circuit type 1 (end-enterostomy), to small bowel length of 50 cm, and to arterial infarction as a cause for bowel resection, but not to PN dependence. After correction taking into account other causes of death through use of French life expectancy tables and a relative survival model, age was no longer a significant survival factor. Permanent intestinal failure probability was related to jejunal remnant length of 100 cm and digestive circuit of types 1 and 2, i.e., end-enterostomy and jejunocolic anastomosis, respectively.

5 November 1999 OUTCOME IN ADULT SHORT BOWEL PATIENTS 1047 Table 3. Univariate and Multivariate Analyses of Survival and PN-Dependence Factors in 124 Adult Patients With Nonmalignant Short Bowel Syndrome Survival PN dependence Univariate Multivariate Univariate Multivariate Demographic characteristics Home PN center NS a P 0.05 NS Date of short bowel constitution ( vs ) NS NS Age 60 yr at time of short bowel P ( ) P 0.02 NS Digestive characteristics Arterial mesenteric infarction P ( ) P 0.02 NS PN dependence P NS Length of remnant small bowel 50 cm b P ( ) P P ( ) P Length of remnant small bowel cm b NS P ( ) P Short bowel type 1 (end-jejunostomy) b P ( ) P P ( ) P 0.03 Short bowel type 2 ( jejunocolic anastomosis) b NS P ( ) P 0.03 a P 0.05 univariate analysis log rank test and P 0.10 in multivariate analysis (Cox model, with RR and 95% CI in parentheses). b In univariate and multivariate analyses, the compared remnant lengths were 50 and vs cm, respectively; short bowel types 1 and 2 were compared with type 3 ( jejunoileocolic anastomosis). We defined short bowel as a remnant small bowel length of 150 cm measured using opisometry, an accurate method for use on x-ray films. 18 This maximal length was in the range of that ( cm) used in previous reports on short bowel syndrome in adults. 10,11,19 Except for 3 patients who had no remnant duodenum, we Table 4. Cutoff Values of Postduodenal Remnant Small Bowel Lengths Separating Transient and Permanent Intestinal Failure According to the Short Bowel Circuit Types of Anastomosis and Presence or Absence of Radiographic Abnormalities in Remnant Small Bowel Entire group No radiographic abnormalities Radiographic abnormalities a Type 1: end-jejunostomy patients (n) Cutoff value (cm) b 100 Sensitivity c 3/4 Specificity d 14/14 Type 2: jejunocolic patients (n) e Cutoff value (cm) b Sensitivity c 29/36 25/28 6/10 Specificity d 32/42 26/32 6/8 Type 3: jejunoileocolic patients (n) f Cutoff value (cm) b Sensitivity c 16/18 17/17 4/4 Specificity d 4/10 4/5 2/2 a Modified mucosal folds and/or nonoccluding small bowel stenoses. b With a significant difference (P 0.05) using linear discriminant analysis. c Nonpermanent PN-dependent patients, i.e., with transient intestinal failure, among those with a remnant length above the cutoff value. d Permanent PN-dependent patients, i.e., with permanent intestinal failure, among those with a remnant below the cutoff value. e Ileocecal valve and cecum absent. f Ileocecal valve and cecum present. examined only postduodenal remnant length, a specification seldom provided in previously published series of short bowel syndrome in adults. 10,11,19 Of note, the 5-year survival was especially high (93%) and permanent intestinal failure especially low (9%) in patients with a cm small bowel remnant, suggesting that a length of 100 cm rather than 150 cm may accurately characterize the upper limit of small bowel length Table 5. Causes of Death in 40 Adult Patients With Nonmalignant Short Bowel Syndrome According to Transient Versus Permanent Intestinal Failure Causes of death Intestinal failure Permanent (n 32) Transient (n 8) Related to PN 7 (22%) 0 (0%) Septicemia 5 0 Liver failure 2 0 Not related to PN 25 (78%) 8 (100%) Related to short bowel 4 (13%) 2 (25%) Cachexia 2 1 Hypokalemia 1 0 Postoperative complications 1 1 Not related to short bowel Related to primary disease a 10 (31%) 5 (63%) Vascular disease b 8 4 Acute respiratory distress 1 c 0 Radiation enteritis 1 0 Amyloidosis 0 1 Miscellaneous 11 (34%) 1 (12%) Sepsis (not related to catheter) 5 0 Diabetes mellitus 2 0 Respiratory failure 2 0 Primary malignancy 1 0 Unknown 1 1 a Having led to short bowel constitution. b Heart failure (3 cases), stroke (4), myocardial infarction (2), sudden deaths (2), and ruptured aortic aneurysm (1). c Chronic intestinal pseudo-obstruction due to mitochondrial cytopathy.

6 1048 MESSING ET AL. GASTROENTEROLOGY Vol. 117, No. 5 associated with permanent intestinal failure in adult short bowel syndrome patients, whatever their circuit type of anastomosis. Our inclusion criteria allowed analysis of patients prognosis and PN dependence without interference from confounding variables, such as life-threatening nondigestive visceral failure and/or evolution or recurrence, during follow-up, of the primary malignancy which led to short bowel syndrome. Our patient population was representative of French adult patients receiving HPN. 7 The year 1980 was chosen as the time to start this study because it initiated the period of development of HPN authorized centers in France. 7,30 Indeed, in children with a remnant small bowel of 40 cm, overall nonactuarial survival rates of 42% and 94% were found before and after HPN was introduced in France, respectively. 30 This study extends to actuarial data some previously published nonactuarial figures showing overall survival rates of 66% 77% in adults 6,19 and of 54% 94% in children with short bowel syndrome, respectively A short bowel digestive circuit with jejunocolic anastomosis (type 2), in which at least part of the colon is in continuity, was found to be associated with higher survival and transient intestinal failure probabilities, as described in previous nonactuarial studies. 12,19 A digestive circuit with jejunoileocolic anastomosis (type 3), in which remnant ileum and ileocecal valves are in continuity, further enhanced these patients probabilities of only transient intestinal failure. 30 We found arterial mesenteric infarction to be associated with a significantly poorer prognosis than other causes of small bowel resection; the fact that cardiovascular diseases were the primary cause of death supports a previous observation that extensive atheromatosis plays a negative contributive role in the overall prognosis of HPN patients. 1,2,7 In our study, PN-related complications accounted for 22% of deaths in patients with permanent intestinal failure, but PN dependence itself was not an independent survival factor, a finding suggesting the positive role of tertiary care centers in the management of HPN patients. 3,34 Up to 81% of our patients had no evidence of radiographic Figure 3. Probability of survival (Kaplan Meier curve) in 124 adult patients with nonmalignant short bowel syndrome. Vertical bars indicate 95% confidence intervals at 1, 2, 5, and 10 years of follow-up. Survival probabilities were 94% (95% CI, 90 98), 86% (80 92), 75% (67 83), and 60% (49 71) at 1, 2, 5, and 10 years, respectively. Figure 4. Survival rate of 124 adult patients with nonmalignant short bowel syndrome. Significant factors were (A) main types of primary disease leading to small bowel resection; (B) postduodenal remnant small bowel length, with 5-year survival rates of 93% (95% CI, ), 79% (66 92), and 57% (43 71) for remnant lengths of , 50 99, and 50 cm, respectively; and (C) presence (type 1) or absence (types 2 and 3) of end-jejunostomy, with 5-year survival rates of 44% (21 67) and 80% (72 88), respectively. Survival distributions were compared using the log rank test.

7 November 1999 OUTCOME IN ADULT SHORT BOWEL PATIENTS 1049 abnormalities on remnant small bowel, and none had occlusive stenoses. In HPN patients with nonmalignant disease and occlusive stenoses of the remnant small bowel, 5-year survival has been reported to be less than 40%, regardless of primary intestinal disease and remnant small bowel length. 7 Both observations suggest that a shorter but functional small bowel is associated with higher survival than a longer, but nonfunctional or chronically occluded, small bowel remnant. This PN-dependence analysis suggests that the probability of weaning off PN was significantly related to intestinal factors only: a remnant postduodenal small bowel 100 cm and short bowel digestive circuit types including at least part of the colon in continuity. This points to the probable importance of using a classification considering both remnant length and the 3 main digestive circuit types of anastomosis in the analysis of short bowel syndrome. 10,19,35 The cutoff value of small bowel remnant length that significantly separated patients with permanent and transient intestinal failure also varied according to digestive circuit types; it was 100 cm in patients with end-enterostomy, a finding concurring with the cm previously reported to be associated with a positive water-energy balance under oral feeds only and with subsequent successful weaning off PN. 11,12 The figures of such cutoff values of small bowel remnant length (65 and 30 cm) in patients with jejunocolic and jejunoileocolic anastomosis, respectively, but no evidence of radiographic residual bowel lesions support an energysparing effect of oral feeds through at least part of a remnant colon in continuity 12,36 38 and concur with previously published lengths. 12,19,39,40 In patients with similar short bowel digestive circuit types but evidence of radiographic residual lesions, the highest cutoff value (90 cm) we found, separating patients with permanent and transient intestinal failure, presumably reflected a lower oral intake and/or a lower absorptive capacity of the remnant bowel. Six percent and 19% of the patients who were ultimately shown as having only a transient intestinal failure were weaned off PN after 3 6 and 7 46 months of HPN, respectively. In contrast to previous findings, 41 this result suggests that digestive adaptation may occur after the early months following resection in a substantial number of adult patients, and also supports other recent reports suggesting that digestive adaptation may be accomplished after 1 3 years in adults 12 and 1 4 years in children. 31 Of note, free oral alimentation was encouraged in our patients receiving HPN; along with subsequent hyperphagia, 20,31 it presumably helped development of their maximal residual absorptive capacity. 42 Finally, 95% of our patients who ultimately had transient intestinal failure were weaned off PN within 2 years and 94% of those not weaned after 2 years were ultimately classified as having permanent intestinal failure; such a 2-year PN limit may well serve to separate adult short bowel patients with transient from those with permanent intestinal failure. 43 For the latter patients, other treatment options instead of HPN have to be considered, 11,43 e.g., combination of growth hormone, glutamine, and a modified diet, 13,15,16 surgical intestinal reconstruction, 17,39 or small bowel transplantation. 8,44 The present data may contribute to a more rigorous approach in selecting adult patients for these treatments, especially small bowel transplantation. 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8 1050 MESSING ET AL. GASTROENTEROLOGY Vol. 117, No. 5 Segmental reversal of the small bowel as an alternative to intestinal transplantation in patients with short bowel syndrome. A report of 11 cases (abstr). Clin Nutr 1998;17(suppl 1): Byrne TA, Persinger RL, Young LS, Ziegler TR, Wilmore DW. A new treatment for patients with short bowel syndrome. Growth hormone, glutamine and a modified diet. Ann Surg 1995;222: Scolapio JS, Camilleri M, Fleming CR, Oenning LV, Burton DD, Sebo TJ, Batts KP, Kelly DG. Effect of growth hormone, glutamine, and diet on adaptation in short bowel syndrome: a randomized, controlled study. Gastroenterology 1997;113: Panis Y, Messing B, Rivet P, Coffin B, Hautefeuille P, Matuchansky C, Rambaud JC, Valleur P. Segmental reversal of the small bowel as an alternative of intestinal transplantation in patients with short bowel syndrome. Ann Surg 1997;225: Nightingale JMD, Bartram CI, Lennard-Jones JE. 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Gastroenterology 1996; 110: Received March 4, Accepted August 3, Address requests for reprints to: Bernard Messing, M.D., Department of Hepatogastroenterology and Nutrition support, Hôpital Lariboisière, 2 rue Ambroise Paré, Paris Cedex 10, France. bernard.messing@lrb.ap-hop-paris.fr; fax: (33) Presented in part at the 1996 American Gastroenterological Association meeting and the 1997 World Intestinal Transplantation Congress and published in abstract form (Gastroenterology 1996;110[suppl:A346]; Transplant Proc 1998;30:2548). The authors thank J. Barbier, M. Beliah, J. J. Bernier, Y. Bouhnik, B. Coffin, M. Lémann, P. Hautefeuille, V. de Ledhingen, R. Modigliani, Y. Panis, J. C. Rambaud, and P. Valleur for follow-up of the patients; and J. Arsham and D. Pryce for the English revision of the manuscript.

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