Increased intestinal absorption by segmental reversal of the small bowel in adult patients with short-bowel syndrome: a case-control study13

lien Amiot, Carmen Stefanescu, Sabrina Layec, Laura Beyer, Olivier Corcos, Arnaud Alves, Xavier Dray, Aure de ric Bretagnol, Yoram Bouhnik, Bernard Messing, Yves Panis, Nathalie Kapel, and Francisca Joly Benoit Cofn, Fre
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ABSTRACT Background: Segmental reversal of the small bowel (SRSB) is proposed in patients with short-bowel syndrome (SBS) as a rehabilitative therapy, but its effects on absorption have not been studied. Objective: We aimed to determine intestinal macronutrient absorption and home parenteral nutrition (HPN) dependence in SBS patients with intestinal failure. Design: We included in a retrospective study all consecutive patients who had an SRSB between 1985 and 2010 and underwent a study of macronutrient absorption. Patients were matched to SBS controls with the same digestive characteristics. Energy and macronutrient absorption were measured. The dependence on HPN was expressed by the number of infusions per week and by the calories infused daily divided by the basal energy expenditure multiplied by 1.5. Results: Seventeen patients who had an SRSB were matched to 17 control patients. Intestinal absorption was higher in the SRSB group for total calories (69.5% compared with 58.0%), fat (48.4% compared with 33.2%), and protein (62.7% compared with 53.4%) (P , 0.05). Median oral autonomy was 100% 6 38.4% in the SRSB group, whereas it was 79% 6 39.6% in the control group (P , 0.05). The number of calories infused was lower in the SRSB group (500 6 283 compared with 684 6 541; P , 0.05), as was HPN dependence (33% 6 20% compared with 48% 6 38%; P , 0.05) at the time of the study. Conclusion: SRSB allows a gain in macronutrient absorption, which is associated with a lower HPN dependence. To our view, SRSB should be integrated in intestinal rehabilitative adult programs. Am J Clin Nutr 2013;97:1008. INTRODUCTION

colon in continuity), jejuno-colonic (type II, some colon in continuity), and jejuno-ileal (type III, the full colon in continuity), with a minimum of 100, 60, and 35 cm of normal small bowel, respectively (3, 4). The colon plays a role in uid and electrolyte reabsorption and in the recovery of energy from unabsorbed carbohydrates by the adaptation of colonic ora, which increases production and absorption of short-chain fatty acids (57). Thus, restoring continuity of the intestinal tract allows a decrease in the volume of parenteral infusions (8). Indeed, when intestinal failure is denitive, medical or surgical rehabilitation must be considered. Nevertheless, for cases with a very short segment of intestine and no colon in continuity, intestinal transplantation should be discussed (9, 10). Surgical reconstruction of the remnant small bowel by antiperistaltic jejunal segment, ie, inversion and reanastomosis of the distal jejunal segment, has been proposed for treatment of SBS in patients with a resected ileum and ileocecal valve (8). The goal is to increase the contact time between the intestinal epithelium and nutrients by creating retrograde peristalsis. Clinical evaluation of this technique is anecdotal and is often based on clinical cases or small series.
From the Departments of Gastroenterology and Nutrition Support (SL, OC, A Amiot, CS, YB, BM, and FJ) and Colorectal Surgery (LB, FB, and pitaux de Paris and the DeYP), Beaujon Hospital, Assistance PubliqueHo nis Diderot University, Paris, France; the Digestive and Nutritional Rehabilitation Unit, Clinique Saint-Yves, Rennes, France (SL); the Department of te de Nacre Hospital, and Caen University, Caen, Digestive Surgery, Co ` re HospiFrance (A Alves); the Department of Gastroenterology, Lariboisie pitaux de Paris and the Denis Diderot University, tal, AssistancePublique Ho Paris, France (XD); the Department of Hepato-Gastroenterology, Louis pitaux de Paris and the Denis Mourier Hospital, Assistance PubliqueHo Diderot University, Paris, France (BC); and the Laboratory of Functional -Salpe trie ` re Hospital and Rene Descartes University, Paris, Coprology, Pitie France (NK). 2 There was no funding source. 3 Address correspondence to F Joly, Department of Gastroenterology and pitaux de Paris, Nutrition Support, Beaujon Hospital, Assistance PubliqueHo ne ral Leclerc, 92110 Clichy-La Garenne, France. E-mail: 100, Boulevard du Ge francisca.joly@bjn.aphp.fr. 4 Abbreviations used: BEE, basal energy expenditure; HPN, home parenteral nutrition; PN, parenteral nutrition; SBS, short-bowel syndrome; SRSB, segmental reversal of the small bowel. Received May 6, 2012. Accepted for publication September 19, 2012. First published online November 14, 2012; doi: 10.3945/ajcn.112.042606.
1

Intestinal failure is dened as reduced intestinal absorption requiring macronutrients and/or water and electrolyte supplements to maintain health or growth (1). The most frequent cause of intestinal failure is short-bowel syndrome (SBS)4, which occurs after extensive intestinal resection. Intestinal failure may be considered transient or permanent depending on anatomic factors and the capacity of adaptation, such as hyperphagia (2, 3). The ability to wean from home parenteral nutrition (HPN) within the rst 25 y after digestive continuity has been established and reects this adaptive process (3). Weaning is achieved depending on the different remaining lengths of small bowel and the 3 main types of SBS: end-jejunostomy (type I, no

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Am J Clin Nutr 2013;97:1008. Printed in USA. 2013 American Society for Nutrition

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We previously reported a patient who was rapidly and permanently weaned off parenteral nutrition (PN) after interposition of segmental reversal of the small bowel (SRSB) (11). We conrmed these results in a series of 8 patients (12). On the basis of these cases, we have continued to propose SRSB in all patients with an indication for surgical reestablishment between the jejunum and the colon and with ,70 cm of small bowel. Because these procedures are often performed during the adaptive phase after resection, the efcacy of SRSB may interfere with spontaneous adaptation (8). Therefore, to evaluate intestinal absorption after this surgical procedure, we compared patients with a jejunal antiperistaltic segment with matched SBS patients without a jejunal antiperistaltic segment to determine 1) the effect of SRSB on macronutrient absorption in SBS patients with intestinal failure and 2) the effect of SRSB on HPN dependence.
SUBJECTS AND METHODS

patients who were candidates for a jejuno-colonic reestablishment with a small-bowel length inferior to 70 cm, had a segmental reversal of the small bowel. Except for the surgical strategy at the time of digestive reestablishment, medical follow-up was identical before and after 1997. Furthermore, the study of metabolic absorption was performed by the same laboratory and with the same technique, with no difference between the 2 periods for data collection regarding macronutrient intake (14). Methods Surgical interventions An extensive description of the SRSB surgical technique was described previously (12). Briey, the 1015-cm long distal intestinal segment was sectioned and rotated over 1808 , and end-toend anastomosis was performed between the reversed intestinal segment and the distal jejunum orally and the proximal remaining colon caudally. Inversion and reanastomosis were performed, and the blood supply was preserved. In the control group, end-to-end anastomosis between the distal jejunum and the proximal colon was performed as usual. The date of entry into this study was the date when bowel continuity was reestablished. Absorption study

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A case-control study was performed. Patients were enrolled from the register of HPN-dependent patients with SBS at the tertiary care center for HPN at Beaujon Hospital (France). All patients had undergone extensive small-bowel resection with no surgical resection of the stomach, duodenum, or pancreas. Subjects SBS patients with SRSB Inclusion criteria for SBS patients were as follows: 1) SBS type II with a postduodenal remnant jejunum ,150 cm, no remnant ileum and reestablished jejuno-colonic continuity for $6 mo, with a segmental reversal of the intestine between the jejunum and colon, and 2) a metabolic study performed $6 mo after the segmental reversal was performed. Exclusion criteria were as follows: 1) upper gastrointestinal tract surgery, 2) remnant ileum and/or ileocecal valve, 3) radiation enteritis and active Crohn disease, 4) organ failure other than gastrointestinal, 5) progressive neoplasia, 6) intestinal stula, 7) symptomatic mesenteric ischemia, 8) treatment with the recombinant human growth hormone or glucagonlike peptide-2 in the past 12 mo, 9) BMI (in kg/m2) .30, 10) age .80 or ,18 y, and 11) sepsis in the 4 wk before the study. Control group Criteria for inclusion and exclusion in this group were identical except for the presence of a reversal segment. All patients received gastric antisecretory drugs, but none received pancreatic enzymes or somatostatin analogs. The eligibility of matched controls was managed by an independent investigator using our local database. The investigator dened a control SBS patient for each patient with a reversed segment, with the same small-bowel length (65 cm), the same type of jejuno-colonic anastomosis, and, when possible, the same etiology leading to SBS. Surgical reports were reviewed to collect measurement of postduodenal remnant small-bowel lengths and remaining colon in continuity, expressed as the percentage of the usual length according to the method of Cummings et al (13). The choice of investigator was blinded for other clinical criteria. Except for 2 patients who were operated on in another hospital but followed in our unit after surgery, all control patients were operated on before 1997. Actually, after this period and our rst series of 8 patients indicating a benet of this technique (12), all

At least 6 mo after bowel continuity reestablishment, all patients underwent a 6-d metabolic study to evaluate intestinal macronutrient absorption as described previously (14). At the time of the metabolic study, all patients were clinically stable, dened by the absence of modication of the PN regimen for 6 wk or recent complication. The rst 3-d equilibrium period conrmed that patients were continuing their spontaneous intake of energy, carbohydrates, lipids, proteins, and bers, and absorption was measured for the last 3 d. Unrestricted intake was measured by the amount or weight and calculated with Bilnut software (P Bourgerette, M Rolshansen, BILNUT 4.0; Nutrisoft). Stool samples were collected daily and frozen at 208 C. Protein, lipid, and total energy were measured by nitrogen elemental analysis (N analyzer Flash EA1112; Thermo Scientic) (15), the method of Van de Kamer, and bomb calorimetry (PARR 1351 bomb calorimeter; Parr Instrument Company), respectively (16). Quantication of carbohydrate-derived energy was calculated by subtracting the energy associated with the protein and lipid components from the total energy. The calorie-conversion factors used were 4.2, 9.35, and 5.65 kcal/g for carbohydrates, lipids, and proteins, respectively (17). The coefcient of net intestinal absorption represented the proportion of ingested energy not recovered in stool output. The net absorption of protein and fat was calculated by subtracting the amount excreted in feces (Out) from the amount ingested (In). The coefcient of net digestive absorption expressed as a percentage of protein and fat represented the proportion of ingested calories not recovered in fecal output: Net digestive absorption (%) = (In Out)/In. The coefcient of net carbohydrate digestive absorption was calculated from the difference between total calories and fat plus protein calories. Ingesta The daily intake of total calories, proteins, carbohydrates (total, complex, and simple), lipids, bers, and alcohol were calculated with Bilnut software during the last 3 d of the absorption study. Our group previously reported that intake measured by amount or

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weight was not signicantly different from measurement by duplicated meals and left over in SBS patients (14). The oral intake was expressed as kilocalories per day. Oral autonomy was expressed as the percentage of total calories absorbed (proportion of ingested calories and of the main energy sources not recovered in stool output) divided by the basal energy expenditure (BEE) multiplied by 1.5. BEE was assessed with Harris-Benedict equations by using a normalized body weight to obtain a BMI equal to 25 [male: BEE = 66.47 + (13.75 3 weight) + (5 3 height) 2 (6.76 3 age); female: BEE = 655.1 + (9.56 3 weight) + (1.85 3 height) 2 (4.68 3 age) (weight in kg, height in cm, and age in y)]. Dependence on PN As previously used in studies on macronutrient absorption in SBS patients, dependence on PN was expressed as the percentage of total daily energy given via HPN divided by the basal metabolic rate assessed by the Harris-Benedict equation multiplied by 1.5, a coefcient that corresponds to an estimate of total energy expenditure in SBS patients (18, 19). Dependence on PN, expressed by this criterion, was reported at the time of the metabolic study. We also reported the number of infusions per week at the time of absorption study. HPN-free survival During follow-up, we reported the number of patients who remained weaned off PN in each group. The HPN free survival rate was calculated from the date of HPN start to end of follow-up or to death. Complications in the reverse group Postoperative morbidity was dened according to Dindos classication (20). Major complications were dened as those requiring surgical, radiologic, or endoscopic intervention (Dindo III); life-threatening complications requiring intensive care manTABLE 1 Demographic and digestive characteristics of the population1

agement (Dindo IV); and death (Dindo V). The rate sepsis line was reported and expressed as number per 1000 catheter-days. Statistical analysis Quantitative variables were expressed as medians (ranges) or as means 6 SDs. Wilcoxons matched-pair signed-rank test was used to compare continuous variables between the 2 groups. All patients were followed up until death or until January 2011, when the data were collected. The duration of HPN was calculated from the date of the start of HPN, up to death, denitive end of HPN, or end of the follow-up. Survival free of HPN was calculated by using the Kaplan-Meier method. Survival free of HPN was compared by using the log-rank test, with P values of 0.05 considered to be statistically signicant. Statistical analyses were performed by using Stata 11 (StataCorp LP).
RESULTS

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Patients From 1985 to 2010, 38 patients had SRSB in our center. A complete metabolic study was performed in 17 patients who completed the inclusion criteria. Population and surgical circuit Demographic and surgical characteristics of the population at the time of the metabolic study are reported in Table 1. No statistical difference was found between the SRSB and control groups for the remnant length of postduodenal small bowel, age, or the percentage of colon. Median small-bowel length was 35 (range: 970) cm and 40 (range: 080) cm in the SRSB and control groups, respectively. The delay between the metabolic study and date of entry was higher in the control group: 47 (range: 5227) mo compared with 16 (range: 6131) mo (P , 0.05).

SBS patients with SRSB (n = 17) Sex Male Female Age at metabolic study (y) Small-bowel length (cm) Length of the reversed segment (cm) Type of anastomosis (n) Right jejuno-colonic anastomosis Jejuno-transverse anastomosis Left jejuno-colonic anastomosis Etiology of the SBS (n) Mesenteric infarction Surgical complications Crohn disease Volvulus Other benign diseases Delay between the jejuno-colonic reestablishment and the absorption study (mo)
1

SBS patients without SRSB (n = 17) 8 9 47 (2468) 40 (080) 6 9 2 9 3 2 3 0 47 (6227)*

13 4 52 (2180)2 35 (970) 10 (815) 6 9 2 12 1 1 0 3 16 (6131)

*Signicantly different from SBS patients with reversed segment, P , 0.05 (Wilcoxons matched-pair signed-rank test). SBS, short-bowel syndrome; SRSB, segmental reversal of the small bowel. 2 Median; range in parentheses (all such values).

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Ingesta and fecal weight Ingesta and daily fecal output are reported in Table 2. The median of ingesta and daily fecal weights were not statistically different between the 2 groups.

pressed as % of total energy absorbed divided by BEE multiplied by 1.5) was 100% 6 38.4% in the SRSB group, whereas it was 79% 6 39.6% in the control group (P , 0.05). HPN dependence

Intestinal caloric absorption and oral autonomy The results of intestinal absorption are reported in Figure 1. Intestinal energy absorption was signicantly higher in the SRSB group than in the control group for total energy (69.5% compared with 58.0%), lipids (48.4% compared with 33.2%), and proteins (62.7% compared with 53.4%) (P , 0.05). Intestinal absorption rates for each SRSB patient and the matched control are reported in Table 2. Median oral autonomy (ex-

When bowel continuity was surgically reestablished, all patients required HPN (rhythm of infusions between 6 and 7/wk). During the metabolic study, SRSB patients received a median of 3.0 6 1.68 compared with 3.5 6 2.10 infusions/wk (P , 0.2). Daily infused energy was lower in the SRSB group (500 6 283 compared with 684 6 541; P , 0.05). HPN dependence was lower in the SRSB group (33% 6 20% compared with 48% 6 38%; P , 0.05). HNP dependence and infused energy are reported in Table 3.
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TABLE 2 Intake and net absorption in patients with and without SRSB1 Remnant jejunal length cm SBS patients with SRSB Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Case 10 Case 11 Case 12 Case 13 Case 14 Case 15 Case 16 Case 17 Median Mean 6 SD Controls Control 1 Control 2 Control 3 Control 4 Control 5 Control 6 Control 7 Control 8 Control 9 Control 10 Control 11 Control 12 Control 13 Control 14 Control 15 Control 16 Control 17 Median Mean 6 SD 35 55 20 15 55 70 60 60 40 35 25 20 60 25 9 65 30 35 40 6 19.6 40 40 20 15 60 80 63 45 40 40 20 30 70 20 0 70 10 40 39 6 23.4 Remaining colon % 50 86 50 86 50 50 35 50 50 35 86 86 50 50 86 86 50 50 61 6 20.1 50 86 50 86 50 64 35 50 50 35 86 86 50 50 93 86 50 50 62 6 20.1 Fecal weight g/d 2855 1160 2735 451 1448 410 555 720 1070 851 842 5514 2244 649 1407 1800 2100 1160 1577 6 1276.1 1800 1678 2030 810 519 432 1817 3720 1891 1154 2500 4494 340 2210 1100 1800 1803 1800 1760 6 1145.2 Oral intake kcal/d 2437 1878 1780 2500 2800 3200 3610 2284 3023 2000 2666 4854 3564 1421 1600 2610 1510 2500 2573 6 896.8 3210 2895 1890 2383 3564 2298 1704 4162 3712 1680 2900 4524 1475 4260 1370 2675 615 2675 2666 6 1133.4 Net absorption kcal/d 1681 1652 907 1975 1932 3040 3178 1530 2261 1760 1999 2427 2530 994 640 1540 710 1760 1809 6 742.5 1187 955 680 1763 2619 1907 664 2746 2227 1226 1073 2081 1209 2470 441 1310 325 1226* 1508 6 727.4 Oral autonomy % 100 71 50 123 107 146 149 97 144 85 104 133 124 54 35 68 35 100 96 6 38.4 53 44 39 105 89 97 36 168 100 80 53 111 70 104 30 91 14 79* 78 6 36.9

1 *Signicantly different from SBS patients with SRSB, P , 0.05 (Wilcoxons matched-pair signed-rank test). SBS, short-bowel syndrome; SRSB, segmental reversal of the small bowel.

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FIGURE 1. Macronutrient absorption in SRSB patients and controls. Total absorption represented the proportion of ingested energy not recovered in stool output. The absorption of proteins and lipids was calculated by subtracting the amount excreted in feces from the amount ingested. The carbohydrate absorption was calculated from the difference between total calories and fat plus protein calories. Data were compared by using Wilcoxons test with P values of 0.05 considered to be statistically signicant. Macronutrient absorption was signicantly increased in the SRSB group for total energy (P , 0.02), lipids (P , 0.05), and proteins (P , 0.05) but not for carbohydrates (P , 0.4). SRSB, segmental reversal of the small bowel.

Complications of the reverse procedure Complications are reported in Table 4. One patient received additional surgery at day 21 for acute acalculous cholecystitis (case 7). This patient, weaned off HPN, experienced 2 very late transient intestinal obstructions treated conservatively by a hypomagnesia correction. He required a sequential antibiotic therapy to treat bacterial overgrowth. Minor complications included one pneumonia and one transient intestinal obstruction treated conservatively. The median length of stay was 19.5 d (range: 653 d) in surgery followed by 30 d (range: 060 d) in the nutrition unit. No late surgery was required. The overall sepsis rate was 1.42/ 1000 catheter-days (range: 07.03/1000 catheter-days). Follow-up The duration of follow-up was determined according to the date when the last information was received, the date of death, or 1 January 2011. Median follow-up was 78 6 76 mo in the SRSB group and 167 6 90 mo in the control group. In the SRSB group, 7 of 17 patients were successfully weaned off PN compared with 6 of 17 in the control group (NS). The delay to wean from HPN was 20 6 10 compared with 12 6 93 mo, respectively (P , 0.2). HPN-free survival, represented in Figure 2, was similar in both groups. In the control group, case 10 was weaned off HPN 20 y after jejuno-colonic continuity because of a delayed increase in intestinal absorption because of recombinant growth hormone treatment begun in 2007.
DISCUSSION

This was the rst study to evaluate intestinal absorption in a large series of patients with SRSB. Our results showed that

digestive absorption of nitrogen, lipids, and total absorption was more improved in patients with jejuno-colonic anastomosis with the reversed segment than in those without the reversed segment. This improvement corresponded to a gain of 300 kcal/d, representing 20% of BEE. Because oral intake did not differ between the 2 groups, better absorption results in higher oral autonomy and a lower dependence on HPN. Animal studies have shown an increase in intestinal absorption, a decrease in weight loss, and an increase in survival with SRSB (21, 22). In addition, more recent data suggest that there are morphologic modications of the bowel mucosa. In pigs, changes included an increase in muscle thickness, crypt depth, villus height, and a decrease in caspase-3positive cells, indicating a decrease in apoptosis (23, 24). Although cases have been reported in humans, the results have been conicting, especially in relation to the possibility of transient improvement with a return to the previous condition (11, 2527). One of the risks appeared to be the development of occlusion. In a report of 30 cases by Thompson and Rikkers (28), the average effective length for reversal was dened as 10 cm for adults and 3 cm for children. In 1991, a case of SBS with 60 cm of residual small bowel and a jejuno-colonic anastomosis with a reverse intestinal segment was reported by our center. The patient presented with subclinical obstruction manometry, compensatory hyperphagia was preserved, and .85% global intestinal absorption allowing HPN to be withdrawn after 3 mo (11). On the basis of this observation, reconstructive surgery was proposed to SBS patients with permanent intestinal failure. Manometric recordings of small-bowel activity in patients with SRSB have shown that the surgery results in retrograde peristalsis. The rst 5 patients with SRSB underwent a small-bowel

INTESTINAL SEGMENTAL REVERSAL IMPROVES ABSORPTION

TABLE 3 HPN dependence at metabolic study1 HPN infusions no./wk SBS patients with SRSB (n = 17) Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Case 8 Case 9 Case 10 Case 11 Case 12 Case 13 Case 14 Case 15 Case 16 Case 17 Median Mean 6 SD SBS patients without SRSB (n = 17) Control 1 Control 2 Control 3 Control 4 Control 5 Control 6 Control 7 Control 8 Control 9 Control 10 Control 11 Control 12 Control 13 Control 14 Control 15 Control 16 Control 17 Median Mean 6 SD 3 4 5 2 4 4 0 0 2 2 0 0 3 3 3 3 0 3 2.24 6 1.68 2 4 3 4 0 0 6 0 3 6 5 0 4 5 5 2 4 3.50 3.09 6 2.11 Infused energy kcal/d 514 629 822 326 676 629 0 0 319 343 0 0 600 500 500 600 0 500 380 6 283 343 820 684 613 0 0 1450 0 589 1089 1100 0 921 1146 1500 400 1542 684* 717 6 541 HPN dependence % of BEE 36 42 64 26 50 36 0 0 27 21 0 0 40 36 37 33 0 33 26 6 20 22 45 53 48 0 0 103 0 35 95 73 0 69 63 113 34 100 48* 50 6 38 Infused volume mL/wk 4500 8000 14,000 4000 8000 8500 0 0 4000 4000 0 0 6000 4500 4500 6000 0 4500 4471 6 3851 14,840 8400 6000 7420 0 0 13,500 0 4500 9000 12,000 0 6000 10,000 10,000 4000 15,600 7420 7133 6 5243

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1 *Signicantly different from SBS patients with SRSB, P , 0.05 (Wilcoxons matched-pair signed-rank test). BEE, basal energy expenditure; HPN, home parenteral nutrition; SBS, short-bowel syndrome; SRSB, segmental reversal of the small bowel.

manometric study and were compared with 5 SBS type II patients without SRSB. In 1995, Cofn et al (29) found a decrease in phase III motor migrant complex with a retropropaged activity. In 1997, the series reported by Panis et al (12) showed an acceptable rate of complications and positive results for weaning from HPN for a mean length of small bowel of 46 (2570) cm. Three of 8 patients were completely weaned from PN, one continued electrolyte infusions only and the other 4 reduced their parenteral calorie intake. Note that the reduction of parenteral support occurred up to 4 y after surgery in this series. Our current study did not nd any signicant difference in survival free of HPN. However after 2 y, there was a trend toward improvement in the SRSB group. Presumably, intestinal adaptation continues to progress in this group with slower and later onset of hyperphagia and/or colonic hyperplasia. The later

weaning from HPN in the study by Panis et al suggests that adaptation probably interfered with the positive outcome of some patients and the results of the technique in our study. However, compared with published data and our personal experience in SBS patients without segmental reversal, weaning is rare in SBS patients with a remnant length ,70 cm (3, 30). Our results conrm the higher absorption suggested by Panis et al, who reported more frequent reduction of PN than would be expected with such a small length of bowel. Our hypothesis for the absence of difference in carbohydrate absorption between the SRSB group and the control group might be that jejuno-colonic reestablishment itself is responsible for a gain in their absorption, more important than for proteins and for lipids (31). The gain in carbohydrate absorption results mainly from the fermentation of the unabsorbed part of them in the remnant colon. Reversal of the

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TABLE 4 Surgical complications, line complications, and bacterial overgrowth in the reversal group1 Dindo classication Line complications (number/1000 catheter-days) 2.07 2.40 0.33 7.33 0.71 1.39 0 0 0 0.85 0 0 2.84 3.94 2.26 0 0 Bacterial overgrowth No No No No No Yes Yes4 No No No No No No No Yes No No

I Case Case Case Case Case Case Case Case Case Case Case Case Case Case Case Case Case 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17
1

II 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

IIIa 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

IIIb 0 0 0 0 0 0 13 0 0 0 0 0 0 0 0 0 0

IV 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

V 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0

0 0 0 0 12 0 0 15 0 0 0 0 0 0 0 0 0

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Major complications were dened as those requiring surgical, radiologic, or endoscopic intervention (Dindo III); lifethreatening complications requiring intensive care management (Dindo IV); and death (Dindo V). 2 Transient intestinal obstruction. 3 Acute cholescystitis at day 21. 4 Late transient intestinal obstruction facilitated by hypomagnesia and bacterial overgrowth. 5 Pneumonia.

small bowel slows down transit, which increases absorption of macronutrients in small bowel. Differences for proteins and lipids are higher than for carbohydrates because of the role of the colon in carbohydrates absorption, contrary to proteins and lipids, which depend on absorption in the small bowel only. Measures to optimize intestinal absorption include medical therapy and diet as well as certain specic surgical procedures (8, 9, 3235). This includes procedures, the goal of which is to prolong transit time as well as others that expand intestinal area. Lengthening procedures include the Bianchi procedure and serial transverse enteroplasty (36, 37), which both require a dilated small-bowel loop. The Bianchi operation converts a dilated short section of intestine into a narrower segment, twice the length, whereas serial transverse enteroplasty involves serial transverse applications of a linear stapler, which divides the bowel from the mesenteric and antimesenteric sides. The results of this procedure have been good in children, but there are few reports in adults. Although dilatation in children may be a result of natural adaptation and growth, it is relatively rare in adults. The major indication in the largest series of adult patients was obstruction secondary to strictures or in patients with intractable symptoms of bacterial overgrowth (38). A recent European prospective 5-y study compared 389 noncandidates and 156 candidates for intestinal transplantation (39). The authors concluded that HPN was conrmed as the primary treatment of intestinal failure, but desmoids and HPNrelated liver failure seem to constitute indications for life-saving intestinal transplantation. On the basis of these data and our results, we propose an algorithm for the management of SBS type II adult patients (Figure 3).

Segmental reversal of the small bowel has been proposed in our center since 1985 in patients with permanent intestinal failure when they are candidates for jejuno-colonic reestablishment. We estimate the probability of weaning from the length of the remnant small bowel and postabsorptive plasma citrulline concentrations (19, 40). The criteria for this indication are a remnant small bowel between 10 and 6080 cm in length, and the ideal length of the reversed segment is 10 cm. Although, in our study, the length of the remnant small bowel did not differ between the groups, if this study had been performed more recently, the groups would probably have been different, ie, a shorter intestine in the

FIGURE 2. Actuarial probability of HPN-free survival in SRSB patients and controls (P , 0.25). The duration of HPN was calculated from the date of HPN initiation, up to death, denitive end of HPN, or the end of follow-up (January 2011). Survival free of HPN was calculated by using the KaplanMeier method. Survival free of HPN was compared by using the log-rank test, with P values of 0.05 considered to be statistically signicant. HPN, home parenteral nutrition; SRSB, segmental reversal of the small bowel.

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FIGURE 3. Algorithm for management of adult patients with SBS type II. A high-risk patient was dened as an SBS patient at higher risk of death from the underlying disease. In the other cases, a jejuno-colonic anastomosis should be performed and trophic factors could be used in cases of permanent HPN dependence in patients with a postduodenal small bowel length .60 cm. In patients with a postduodenal small bowel length #60 cm, those with a dilated remnant small bowel could have a Bianchi procedure or step procedure in association with jejuno-colonic anastomosis and those without a dilated remnant small bowel could have an SRSB during the jejuno-colonic anastomosis. HPN, home parenteral nutrition; SBS, short-bowel syndrome; SRSB, segmental reversal of the small bowel.

patients with segmental reversal. We believe that the results on nutrient absorption support extending the indication for this procedure to patients with a very short bowel.
We thank Fatima Gandhour and Sophie Penven (dietitians) and Isabelle Pingenot (coordinator nurse of HPN program). The authors responsibilities were as followsFJ and BM: concept and design of the study; LB, A Alves, FB, and YP: surgical procedures; NK: sample analyses for macronutrient absorption; SL and FJ: data acquisition, analysis, and interpretation and drafting of the manuscript; XD and A Amiot: statistical analysis; and all authors: critical revision of the manuscript for important intellectual content. No conicts of interest were declared.

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