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Thompson JS, Langnas AN. Surgical Approaches to Improving Intestinal Function in the Short-Bowel Syndrome. Arch Surg. 1999;134(7):706–711. doi:10.1001/archsurg.134.7.706
Copyright 1999 American Medical Association. All Rights Reserved. Applicable FARS/DFARS Restrictions Apply to Government Use.1999
Nontransplantation surgical approaches to improve intestinal function in patients with the short-bowel syndrome have a satisfactory outcome in selected patients.
Ninety adult (aged >18 years) patients with intestinal remnants shorter than 180 cm were evaluated between 1980 and 1998.
Main Outcome Measures
Clinical improvement (reduction in parenteral nutrition, resolution of anatomical problems, decreased symptoms, or improved oral intake) and postoperative morbidity and mortality rates.
There were 17 deaths within 30 days after resection. Thirty-seven (51%) of the surviving 73 patients underwent 43 procedures to improve intestinal function. Fourteen procedures (33%) were intended to expand intestinal surface area by restoring intestinal continuity (n=10), recruiting additional length (n=3), or longitudinal lengthening (n=1). Twenty-six procedures (60%) aimed to alter intestinal function, either by relieving obstruction (n=10), repairing fistulas (n=8), slowing transit (n=4), eliminating diseased bowel (n=3), or improving motility (n=1). Three patients had stomas created to improve oral intake and relieve perianal symptoms. Postoperatively, 2 anastomoses leaked, 2 fistulas recurred, and there was 1 death (mortality, 2%). Thirty-seven procedures (86%) resulted in clinical improvement. Eleven (46%) of the 24 patients receiving parenteral nutrition were able to discontinue it and 5 patients were able to reduce the amount of parenteral nutrition received. Twelve procedures that increased surface area (86%) and 22 procedures that addressed functional problems (85%) resulted in clinical improvement. Success was lowest (50%) in patients having procedures to prolong transit time.
Various nontransplantation surgical procedures have a role in improving intestinal function in short-bowel syndrome. These procedures usually result in clinical improvement in properly selected patients. Success is lowest for procedures designed to prolong intestinal transit time; thus, these procedures should be used only in carefully selected patients.
EXTENSIVE intestinal resection can result in the short-bowel syndrome (SBS). There have been many recent advances in the medical management of this condition, including provision of parenteral nutrition (PN), selection of the optimal diet for a given patient, pharmacologic treatment of fluid and electrolyte secretion, and the use of specific nutrients and growth factors to stimulate intestinal absorption and adaptation.1,2 However, while the appropriate diet, nutritional support, and various pharmacologic manipulations can maximize function of the intestinal remnant, there is often a role for surgical intervention in those patients who have continued malabsorption, a need for specialized nutritional support, or intestinal complications.1,2
The goals of surgical treatment include expanding intestinal surface area or improving function of the intestinal remnant. The surgical approach depends on the remnant length and caliber, intestinal function, presence of intestinal complications, and the status of nutritional support. While intestinal transplantation might eventually become the optimal surgical treatment for patients with SBS, current results restrict its use to carefully selected patients who are permanently dependent on PN and develop life-threatening complications.2-4 The aim of the present study was to evaluate the role and outcome of various nontransplantation surgical approaches to improving intestinal function in adults with SBS.
This was a retrospective review of 90 consecutive adult (aged >18 years) patients undergoing treatment for SBS between 1980 and 1998 at the University of Nebraska Medical Center (University Hospital and Omaha Veterans Affairs Hospital). Short-bowel syndrome was defined as an intestinal remnant shorter than 180 cm with associated malabsorption (diarrhea, steatorrhea, or metabolic abnormalities). Intestinal length was determined from operative notes, intraoperative measurements, and radiographic determinations as available. There were 42 men and 48 women, with an age range of 18 to 84 years. Mesenteric vascular disease and cancer and its treatment with radiation were the most common causes of resection (Table 1). Patient characteristics are presented in Table 2. Twenty patients (22%) were older than 70 years. Three fourths of patients were receiving PN. Thirty-one patients (34%) had an intestinal remnant shorter than 60 cm. Only 23 patients (26%) had an intact ileocecal junction and 55 (61%) had a stoma. Seventeen patients died within 30 days of the resection leading to the SBS.
Medical management included PN as necessary, optimizing enteral intake, and treatment of gastric hypersecretion, diarrhea, steatorrhea, and bacterial overgrowth as appropriate with histamine-receptor antagonists, proton-pump inhibitors, antidiarrheal agents, cholestyramine, and antibiotics. Patients were considered for surgical therapy if they required PN or had continued significant malabsorptive symptoms. Thirty-seven (51%) of the 73 surviving patients underwent operative procedures to improve intestinal function. Follow-up of patients undergoing operative procedures ranged from 7 to 192 months, with 20 patients (54%) followed up for more than 5 years.
Operations included all nontransplantation procedures performed to improve intestinal function, expand intestinal surface area, and treat intestinal complications. Our overall surgical strategy in these patients has been described previously.3 Stricturoplasty was performed by means of a Heineke-Mikulicz–type enteroplasty at the stenotic region of the intestine.5 Serosal patch was performed by suturing adjacent serosal surfaces over intestinal defects.5 Artificial valves were created by distal intussusception of a segment of small intestine.3 Ten-centimeter reversed segments were employed. Intestinal lengthening involved longitudinal transection of the intestine between the mesenteric and antimesenteric edges and anastomosis of these parallel intestinal segments.6 Clinical improvement was defined as reducing (>25%) or discontinuing PN requirements while maintaining body weight, resolving a specific anatomical problem (eg, obstruction or fistula, as demonstrated clinically and radiographically), ameliorating symptoms of malabsorption (eg, diarrhea or metabolic abnormalities such as hypocalcemia), or significantly improving (>25%) oral intake. Statistical comparisons were made using χ2 analysis, with P<.05 signifying statistical significance.
Thirty-seven (51%) of the 73 patients surviving more than 30 days underwent operative procedures. Patients with remnants shorter than 60 cm were less likely to undergo operation (P<.05) (Table 2). Patients undergoing operation were more likely to have a stoma (P<.05).
The 37 patients underwent 43 operative procedures to improve intestinal absorption (Table 3). These procedures were performed within 12 months of resection in 20 patients (47%). Fourteen (33%) of these procedures were undertaken to expand intestinal surface area. Twenty-six procedures (60%) aimed to improve intestinal remnant function. Three patients (7%) had stomas created to improve oral intake and relieve perianal symptoms. Postoperatively, 2 anastomoses leaked, 2 fistulas recurred, and there was 1 death (mortality, 2%).
Procedures to expand intestinal surface area included restoring intestinal continuity, recruiting additional intestine, and the intestinal lengthening procedure. Ostomy closure was performed in 10 patients with stomas and remnants ranging from 30 to 180 cm. Eight of these patients had anastomosis to a remnant of left colon. In 3 patients additional intestine was recruited proximal to a stoma including right colon, left colon, and 60 cm of small intestine with right colon, respectively. One adult patient with segmental dilatation of a 120-cm remnant underwent intestinal lengthening of a 25-cm segment.
Procedures to improve intestinal function included either relieving obstruction, repairing fistulas, slowing intestinal transit, eliminating diseased bowel, or improving motility. Six of the 10 patients with obstruction had a stricturoplasty performed. Lysis of adhesions, limited resection, colostomy formation, and stoma revision were performed in the other 4 patients. Three of 8 fistulas were repaired by a serosal patch and the others were resected. Two reversed segments and 2 intestinal valves were created to slow intestinal transit time in patients with remnants of 100, 120, 150, and 180 cm, respectively. Three patients with intractable Crohn disease underwent limited resection. One patient underwent tapering of a dilated segment of intestine to improve motility.
Overall, 37 (86%) of the procedures resulted in clinical improvement ( Table 4). Eleven (46%) of the 24 patients receiving PN were able to discontinue it and 5 reduced the amount of PN. Twenty-eight procedures (65%) resulted in improved oral intake. Thirty-six procedures (84%) resulted in improvement of malabsorptive and obstructive symptoms. Twelve procedures that increased surface area (86%) resulted in clinical improvement. Two patients undergoing stoma closure had unsatisfactory results; one had an anastomotic leak and the other elected to have a stoma reinstated because of severe diarrhea and perianal complications. Twenty-two procedures (85%) that addressed functional problems resulted in clinical improvement. Two fistulas recurred and 1 persisted after further operative attempts at repair. Success was lowest (50%) in patients having procedures to prolong transit time. One of the reversed segments was taken down for persistent nausea and pain. One patient with a valve had no improvement in diarrhea. Stoma formation resulted in improved oral intake and improvement in perianal complications in all 3 patients undergoing the procedure. Of those patients undergoing operation, 2 have subsequently undergone intestinal transplantation and 3 are awaiting transplantation.
In the present study, one half of adult patients undergoing intestinal resection that resulted in SBS underwent surgical procedures to improve intestinal absorption. These patients were more likely to have a longer intestinal remnant and an ostomy than those not undergoing operation. The most common operations were restoration of intestinal continuity and procedures to relieve obstruction and repair enterocutaneous fistulas. However, a smaller group of patients were candidates for more specialized procedures designed to improve the function of the intestinal remnant.
Ostomy closure should be considered in patients with significant small intestinal remnants and intact colon distal to a stoma. Restoring intestinal continuity will increase absorption and prolong transit time in many patients.7 We performed ostomy closure in only one fourth of patients with stoma. Most of our patients had only a remnant of left colon distally. However, jejunocolic anastomosis is functionally equivalent to adding 25 to 30 cm of small intestine length.8 Short-chain fatty acids reaching the colon are a potential source of additional calories.9 Four of our 6 patients receiving PN were able to eliminate or reduce PN after ostomy closure. However, patients with a short remnant (<60 cm) may have severe diarrhea with resultant perianal complications and reduced oral intake if continuity is maintained. In 3 of our patients colostomy formation was undertaken to relieve perianal symptoms and permit greater oral intake, including 1 patient who had previously had an ostomy closed. Reconnecting the colon introduces the risk of nephrolithiasis as well.10 Unfortunately, we found that only one fourth of our patients with stomas were candidates for ostomy closure.
Other procedures to expand intestinal surface area are applicable to a small group of patients. Occasionally a significant segment of small intestine will have been bypassed in previous procedures and can be restored to continuity. The intestinal lengthening procedure has been performed in many children, but adults seem to be less likely to develop dilated intestinal segments.3 Our 1 adult patient who underwent intestinal lengthening was able to reduce PN requirements after the procedure.
Patients with SBS frequently require surgery for intestinal complications.11 Obstruction and fistula formation were common problems in our study. Both conditions reduce oral intake, cause significant symptoms, and may increase the risk of sepsis. Chronic intestinal obstruction increases the mortality rate in patients receiving long-term PN.10 Operative resolution of these problems resulted in improved intestinal function for most patients in our study. In patients with short intestinal remnants, procedures such as stricturoplasty and serosal patching need to be considered to avoid further resection.5
While the goal in patients with SBS is generally to minimize further resection, in some circumstances resecting diseased bowel will improve intestinal function.12 Radiation-induced enteritis, intestinal pseudo-obstruction, and Crohn disease may contribute to impaired motility and absorption. In our study, limited resection of segments with Crohn disease that had been intractable to medical treatment had a beneficial effect in 3 patients.
Surgeons have been interested in operations to prolong intestinal transit for more than 100 years.13,14 However, there have been few well-performed studies of these procedures. We created reversed segments and intestinal valves in only 4 adult patients. Unfortunately, these procedures had the lowest success rate, with only 2 patients benefiting with either a decrease in PN requirements or resolution of diarrhea. In other reports these procedures have been performed at the same time that intestinal continuity was reestablished.13 We have preferred to determine the beneficial effect of restoring continuity prior to considering procedures to prolong transit time, since restoring continuity will often result in functional improvement.
Our experience suggests that various nontransplantation surgical procedures have a role in improving intestinal absorption in SBS. These procedures usually result in clinical improvement for most properly selected patients. Success is lowest for procedures designed to prolong intestinal transit time. Patients with very short remnants (<60 cm) are less likely to tolerate ostomy closure or to benefit from procedures that result in modest improvements in transit time and surface area. Thus, these procedures should be given careful consideration and performed only in highly selected patients. Patients who continue to receive PN after operative treatment may become candidates for intestinal transplantation.
Presented at the 106th Scientific Session of the Western Surgical Association, Indianapolis, Ind, November 16, 1998.
Corresponding author: Jon S. Thompson, MD, Department of Surgery, 600 S 42nd St, Omaha, NE 68198-3280 (e-mail: Jthompso@mail.unmc.edu).
Merril T. Dayton, MD, Salt Lake City, Utah: Dr Thompson and his colleagues at the University of Nebraska have previously published a large series on SBS that included a combination of pediatric and adult patients. However, that initial publication in 1995 included predominantly pediatric patients. The present series is an update on the adult portion of their series, in which they have doubled the number of adults reported. This is a retrospective chart review of 90 patients who were left with less than 180 cm of small intestine after their initial devastating operation. There was a 19% mortality in this series, most within the mesenteric ischemia group. This paper focuses on the remaining 73 patients, 50% of whom underwent some kind of operative procedure within 12 months of the initial one. In the manuscript the procedures were divided into 2 general categories, those that expand intestinal surface and those that alter or improve intestinal function. Under the first category, those that expand intestinal surface, the procedures really involved recruiting bowel that had been bypassed and was merely being included back into the alimentary canal again. Under those that improved intestinal function, most of the procedures were those done to relieve obstruction, treat fistulae, or to resect severely diseased bowel (in the case of Crohn disease).
Their results demonstrate that, in 86% of procedures, they had a successful outcome as measured by the ability to wean patients off of total parenteral nutrition (TPN) (which occurred in 46% of the patients who had been on TPN), improving oral intake, or ameliorating their bowel symptoms. The authors correctly point out that the least successful group was those who had had procedures done to decrease transit time.
I think that Dr Thompson and his colleagues at the University of Nebraska are to be commended for taking on a very difficult clinical problem, carefully studying it, and trying to make some suggestions that can improve our management of it. Indeed, Dr Thompson is considered one of the worldwide experts on this topic.
This retrospective study, however, confirms what I think Dr Thompson and his colleagues would agree with: we really haven't made much progress in managing the truly refractory, TPN-dependent patient with hopelessly inadequate amounts of small bowel for alimentation. Specifically, procedures to grow neomucosa, lengthen existing small-bowel remnants, and diminish intestinal transit time have been very disappointing and discouraging. Indeed, to this reviewer it appears that for this group of patients transplantation represents our best hope at present.
Most of the procedures performed in this series were done to eliminate the anatomical problems that most GI surgeons would intuitively perform, such as relieving obstruction, dealing with fistulae, and so forth.
I do have a few questions for the authors. Dr Thompson, you mentioned that you had selected 180 cm as the cut-off value for SBS. That seems a little generous to me. Would you comment on that, and what, in your mind, is really the critical length at which one is likely to see SBS? In that same vein, the manuscript is a little bit confusing because in Table 2 it talks about 3 different categories, those less than 60 cm, those 60 to 120 cm, and those greater than 120 cm. Would you talk about those values vs 180 cm and how they were used to compile this patient population?
The manuscript also mentions that 27% of the patients with SBS were not even on TPN. Do you continue to track these patients once they are nutritionally independent? Are they considered SBS if in fact they don't even require TPN?
One of your findings was that those who had less than 60 cm of remaining small intestine were least likely to undergo an operative procedure. Why is that? It seems like that group might stand to benefit the very most from procedures that would improve absorption.
And, finally, you made reference to this but as you know Wilmore and colleagues suggested that a combination of growth hormone, glutamine, and a high-carbohydrate diet would help wean patients off of TPN quicker. Do you use this in your patient population and have you found it to be successful?
Frank G. Moody, MD, Houston, Tex: I would like to have Dr Thompson focus on a couple of unique things that they have done here. Specifically, to tell us about the bowel that is dilated, which they divided and then put in the series, or they imbricated it in order to improve its motility. Did these maneuvers in fact change motility or absorption? Can you give us a little bit more detail on that small group of patients?
Fabrizio Michelassi, MD, Chicago, Ill: It is not easy to find appropriate outcome parameters to measure success or failure. In this vein, what parameters, Dr Thompson, can we choose to quantitate functional results? It's obvious that, if a patient does not need TPN after surgery, this is a successful outcome. But to quantitate amelioration of diarrhea, I think it is quite difficult. How did you do that? Did you measure how much antidiarrheal medications these patients were using postoperatively? The other issue to remember is that amelioration comes over time. Did you measure amelioration at specific time intervals from the surgery, and have you actually studied the correlation between time and amelioration?
Would you comment on the role of glutamine enterally administered, either preoperatively or postoperatively?
Dr Thompson: Let me start with Dr Dayton's questions. I have used 180 cm for these studies, but it does give a skewed view compared with what we consider the real severe SBS patients. I have been impressed over the years that there is no magic cut-off number, and I am sure you have all had similar experiences where you will see patients who have 2 ft of small bowel that seem to defy our knowledge and do very well and likewise patients with longer remnants who don't do as well. So this is an attempt to capture all of those patients. The patients that we include here who have 180 cm are likely for example to have had irradiated bowel and the underlying disease affects bowel function. That's why I have included this group of patients, and I try to stratify the patients in the tables. The group with less than 60 cm is clearly the most challenging group, the group that is going to be the most likely to need intestinal transplantation or long-term TPN. Admittedly, the classic definition is less than 120 cm.
The reason that we don't operate on more of the patients with less than 60 cm probably reflects a bias that we have. I used to recommend that if someone has a remnant less than 90 cm that we shouldn't put their intestine back in continuity. They are going to have diarrhea; they are going to be miserable. What I have learned is there are a lot of advantages to having the intestinal remnant in continuity and I think now would say even people down to the 60-cm range probably almost automatically should be considered to be put back into continuity to see if that will improve their absorptive capacity. As you get much shorter than that, the success will be lower. Clearly these patients with short remnants are at risk for the same complications but perhaps get intestinal complications less frequently as well.
Part of the difficulty in both assessing the outcome, which is really the essence of several of the questions, and in choosing what procedures to do in these patients, is that it is a very heterogeneous group. The goals of the surgical therapy are very different for these different groups of patients. A lot of these procedures have been performed, but it is not clear in some cases if the patient was going to benefit from the very beginning. A good example of this is the intestinal lengthening procedure that Dr Moody brought up. These have been performed, predominantly in the pediatric population, and while you can lengthen the remnant 5 cm or 10 cm, you can predict from the outset that that's not going to improve their overall clinical situation. We should not undertake these procedures unless there is something to gain. There are some benefits to reducing TPN. Certainly ameliorating symptoms is also an important goal but clearly in terms of long-term function and survival, getting patients off TPN has to be the most important goal.
We have investigated several of these procedures, as you know, Dr Moody, in the laboratory. It has actually been fairly difficult to tell in the short-term laboratory studies if any of these procedures are of great benefit. Early on they cause problems with ileus and poor intake. They also tend to alter the hormonal response to resection. There is a great need on the clinical side to study these patients over time and see how beneficial the procedures are.
I am very aware of Dr Wilmore's work with glutamine and growth hormone. Dr Grosfeld and I just last week spent a week in Japan at a conference discussing a lot of these issues, and I feel I am learning more about this all of the time. My general concept about intestinal adaptation has been that at the time of a massive resection a signal is sent into motion, a genetic signal, almost immediately, which sets into progress a response that leads to a variety of other responses. This leads to increased proliferation, structural adaptation, an altered hormonal response, induction of growth factors, changes in growth factor receptors, and so forth.
My view had generally been that this was a time-limited response, that after a period of several months, this response was over and couldn't be regained. This was a golden period that you had to stimulate intestinal adaptation. The more we learn about this suggests that this might be a narrow view, although I think for the most part it's true. As we discussed at this conference, perhaps different growth factors and nutrients are going to behave differently. Epidermal growth factor, for example, a growth factor I have been very interested in, clearly should be given around the time of resection for it to have its maximal response. Its primary role is an induction of this early growth response. It may be, however, there are other factors such as growth hormone and glutamine that work via different pathways that would allow them to have some improvement in intestinal function at a later period of time. Whereas endothelial growth factor can be given at one point in time and give sustained permanent effect on adaptation, perhaps these other growth factors and nutrients would need to be given more continuously and once they were discontinued, the effect might be lost.
Another issue you all addressed is that we don't have good ways, and this gets back to your question, Dr Michelassi, of analyzing what these agents do to the gut over the short term. Except for histology, there are few parameters to know if in fact you are augmenting the structure and function. Short of doing whole-body absorption studies, it's very difficult to make sense out of the isolated studies that we do about an enzyme level or transport of a specific nutrient in vitro. I think we all agree there is much work to do in this area to develop better radiologic techniques. We have looked at a number of different functional tests over the years and have found none of them to be entirely satisfactory. Thus, for this group of patients, which is very heterogeneous and with end points that are very diverse, our methods of assessment are in some cases fairly subjective. You know if you have decreased or eliminated someone's TPN, that is fairly finite. Alleviation of diarrhea becomes more difficult and we are left with more of a quality-of-life determination with the patients.
This is still a very fruitful area for investigation. There certainly have been a number of advances. I have still tried to be fairly conservative in my approach to all of these procedures so that we don't harm these patients.