Criteria for Selection of Cases

Medical records of all dogs and cats examined at the Foster Hospital for Small Animals at the Cummings School of Veterinary Medicine at Tufts University or at the Angell Animal Medical Center between March 1998 and August 2004 that underwent resection of ≥ 50% of the small intestine were included in the study. Possible cases were identified by reviewing the surgery logs of residents at both institutions, the itemized invoices of abdominal surgeries performed during the study period, and the records of all nutritional consultations requested during this period. Cases for which the medical record could not be located were excluded.

Procedure

Medical records included in the study were reviewed with the help of a standardized data sheet. Data obtained from the medical records included age, breed, sex, initial clinical signs (ie, clinical signs prior to intestinal resection), underlying abnormality necessitating resection, percentage of intestine resected (ie, estimated percentage reported by the attending surgeon at the time of surgery), anastomotic technique, nutritional support provided during the hospitalization period, and duration of hospitalization. Owners or referring veterinarians were contacted to obtain information on long-term outcome. Outcome was based on the owner's perception of the animal's current clinical signs, if any, and the need for medical or nutritional treatment to control clinical signs. An animal was considered to have a good outcome if the owner reported that it had normal to near-normal fecal consistency when at home and that no treatment other than dietary management was required. An animal was considered to have a poor outcome if the owner reported that it continued to have diarrhea or weight loss.

Statistical analysis—Summary statistics were calculated, and continuous data were examined graphically. Continuous data that were normally distributed are presented as mean ± SD; continuous data that were not normally distributed are presented as median and range. Data that were not normally distributed were logarithmically transformed prior to analysis. Proportions of animals that were discharged from the hospital or had a good outcome were compared between categories (ie, sex, species, underlying reason for resection, use of parenteral nutrition, and section of intestinal tract resected) by use of the Fisher exact test. Independent t tests were used to compare survival time between categories for factors that consisted of only 2 categories (ie, sex, species, and use of parenteral nutrition), and ANOVA was used to compare survival time between categories for factors that consisted of ≥ 3 categories (ie, underlying reason for resection and section of intestinal tract resected). Whether there was a difference in the percentage of intestine resected between animals that were or were not discharged from the hospital or between those that had a good or poor outcome was determined by use of independent t tests. The Pearson test was used to test for correlations between age and survival time and between percentage of intestine resected and survival time. All analyses were performed with commercial software.^a For all analyses, a value of P < 0.05 was considered significant.

Results

The initial review identified 25 dogs and cats that underwent resection of ≥ 50% of the small intestine during the study period. However, medical records for 5 of these animals could not be located, and these 5 cases were excluded from the study. Thus, 20 cases (13 dogs and 7 cats) met the criteria for inclusion.

Dogs included in the study were significantly (P = 0.02) older (median, 4 years; range, 1 to 13 years) than cats (median, 1 year; range, 3 months to 4 years). The only dog breed represented more than once was the Labrador Retriever (n = 3); the only cat breed represented more than once was the domestic shorthair (5). There were 8 male dogs (6 castrated), 5 female dogs (all spayed), 3 male cats (2 castrated), and 4 female cats (2 spayed).

Vomiting was the initial (ie, prior to intestinal resection) clinical sign in all 20 animals. In all 7 cats, intestinal resection was performed because of linear foreign bodies. Reasons for intestinal resection in the dogs included linear foreign bodies (n = 5), mesenteric volvulus (2), a solitary foreign body with perforation of the intestine (2), intussusception (1), a solitary foreign body with vascular compromise (1), dehiscence of a previous gastrointestinal tract surgery site (1), and a stromal gastrointestinal tract tumor (1).

Mean ± SD percentage of intestine resected was 68 ± 14% (range, 50% to 90%). Mean percentage of intestine resected in the cats (81 ± 8%; range, 70% to 90%) was significantly (P = 0.001) greater than mean percentage of intestine resected in the dogs (61 ± 12%; range, 50% to 80%). In 5 of the 7 cats, only the jejunum was resected, whereas in 1 cat, the duodenum and jejunum were resected, and in the remaining cat, the jejunum and most of the ileum were resected, leaving the ileocolic valve. In 7 of the 13 dogs, only the jejunum was resected, whereas in 4 dogs, the duodenum and jejunum were resected; in 1 dog, the jejunum and a portion of the ileum were resected, and in the remaining dog, the jejunum and entire ileum, including the ileocolic valve, were resected. In 3 dogs, the remaining ends of the intestine were anastomosed in a side-to-side fashion with a stapling device.^b,c In the remaining dogs and all cats, the remaining ends of the intestine were anastomosed in an end-to-end fashion with simple interrupted sutures of monofilament synthetic suture material.^d,e

Parenteral nutritional support was administered in the immediate postoperative period to 4 dogs and 1 cat. This consisted of partial parenteral nutrition in 3 dogs, total parenteral nutrition in 1 cat, and partial parenteral nutrition followed by total parenteral nutrition in 1 dog. Median duration of parenteral nutritional support was 3 days (range, 2 to 7 days). In 10 dogs and 6 cats, oral feeding was reinstituted; various commercial diets^f-l were used, including a reduced-fat, easily digestible diet (n = 10); an adult maintenance diet (3); a calorically dense diet (2); and a high-fiber diet (n = 1). Median time to restoration of oral feeding after surgery was 2 days (range, 1 to 8 days). The remaining 4 animals had no record of eating during the hospitalization period after surgery. Two dogs were not fed while hospitalized because of the severity of their illness. Both of these dogs developed septic peritonitis after surgery and were euthanized 3 days after surgery.

Median duration of hospitalization was 3 days (range, 3 to 9 days) for the cats and 4 days (range, 2 to 11 days) for the dogs. Three dogs died or were euthanized without being discharged from the hospital. Two dogs were euthanized 3 days after surgery because of dehiscence of the surgical site and development of septic peritonitis; 1 dog died of acute respiratory distress syndrome 5 days after surgery. The remaining 10 dogs and 7 cats were discharged from the hospital.

Follow-up information was available for all 10 dogs and for 5 of the 7 cats that were discharged from the hospital; the remaining 2 cats were lost to follow-up. Median survival time for the 15 animals for which follow-up information was available was 828 days (range, 7 to 1,957 days). Median survival time for dogs (995 days; range, 7 to 1,271 days) was not significantly (P = 0.75) different from median survival time for cats (774 days; range, 31 to 1,957 days). Seven dogs and 4 cats were still alive at the time of the present study.

Eight of the 10 dogs for which follow-up information was available were reported by their owners to have had good outcomes. All 8 dogs were reported to have had soft feces for at least the first few days after surgery, but only 2 were reported to have soft feces at the time of final follow-up, and owners of both dogs reported that they did not consider their dogs to have diarrhea. The remaining 6 dogs did not have any signs of gastrointestinal tract disease at the time of final follow-up. One dog with a good outcome was euthanized 2 years after surgery because of congestive heart failure secondary to dilated cardiomyopathy. The remaining 7 dogs with a good outcome were still alive at the time of the present study, and information on diet was available for 5 of the 7. Three dogs were eating an adult maintenance diet, 1 was eating a senior maintenance diet, and 1 was eating a novel ingredient diet.

The remaining 2 dogs for which follow-up information was available had poor outcomes. One of these was euthanized 6 months after surgery because of chronic diarrhea and weight loss. The other was euthanized 7 days after surgery (1 day after being discharged from the hospital) because of diarrhea and straining to defecate.

Four of the 5 cats for which follow-up information was available were reported by their owners to have had good outcomes. One cat had loose feces for 3 to 4 months after surgery but reportedly had soft but formed feces at the time of final follow-up. The second cat reportedly had formed but voluminous feces with a foul odor. The third cat had diarrhea for approximately 2 years after surgery but reportedly had formed feces, albeit foul smelling, at the time of final follow-up. The fourth cat reportedly did not have any clinical signs of gastrointestinal tract disease. Information on diet was available for 3 cats; 2 were eating a commercial canned adult maintenance diet, and 1 was eating a commercial dry adult maintenance diet.

The remaining cat for which follow-up information was available had a poor outcome. This cat was euthanized approximately 4 weeks after surgery because of persistent diarrhea and dehydration.

One of the 2 cats lost to follow-up was known to be alive at least 12 days after surgery. The other reportedly had continued weight loss 1 month after surgery, despite a ravenous appetite, but was lost to further follow-up.

Neither the proportion of animals that were discharged from the hospital or that had a good outcome nor survival time was significantly different between dogs versus cats, male versus female animals, underlying reason for resection, animals that received or did not receive parenteral nutrition, or section of intestinal tract resected. The percentage of intestine resected and age were not significantly different between animals that were or were not discharged from the hospital or between those that had a good or poor outcome. Survival time was not significantly correlated with age at the time of surgery or percentage of intestine resected.

Discussion

Results of the present study suggest that most animals that underwent extensive small bowel resection had a good long-term outcome and few had persistent signs consistent with SBS. Only 3 of 15 animals in the present study that were discharged from the hospital and for which long-term follow-up information was available had a poor outcome. Although outcome was a subjective evaluation based on owner perception of fecal quality and need for medical or nutritional treatment, the high percentage of animals with a good outcome was a positive and unexpected result of the study. In general, most animals had diarrhea or loose feces for a few weeks or months after surgery but eventually developed normal fecal consistency or had only mild clinical signs that were acceptable to the owner (eg, occasional soft feces, voluminous feces, or foul-smelling feces). In contrast, only 2 of 7 dogs described in previously published reports^8–11 had an acceptable outcome, and 1 of these required substantial nutritional support after surgery. Unfortunately, in the present study, we were unable to identify any factors that could be used to predict which animals would be more likely to have a good rather than a poor outcome.

Estimated percentage of small intestine that was resected was not significantly associated with outcome in the present study. This was consistent with a previous observation¹¹ that outcome in dogs undergoing extensive small intestinal resection was not consistently associated with length of intestine removed but contrasts with reports^1–3,12 from the human literature, which suggest that substantial alterations in nutrient absorption will occur with removal of ≥ 50% of the small intestine. However, values for percentage of intestine resected that were used in the present study were the estimated percentages reported by the attending surgeons at the time of surgery, and the length of the intestine remaining after resection was not always recorded at the time of surgery. Contrast radiography^9,11 could have been used to better estimate the amount of remaining intestine in these cases, and more exact measurements may have helped to identify a critical limit for intestinal resection in dogs and cats associated with development of clinical signs similar to SBS in people. It seems unlikely that the better results for dogs and cats in the present study, compared with results for human patients, could be explained by a greater ability for the intestine to adapt in dogs and cats. Although it has been postulated that younger animals may be more likely to undergo intestinal adaptation,¹³ in people, extent of intestinal adaptation has not been correlated with age.¹⁴ Similarly, in the present study, mean age of animals with a good outcome was not significantly different from mean age of animals with a poor outcome.

The importance of retaining the ileocolic valve during extensive small intestinal resection has been reported,¹⁵ and there is evidence from previous case reports¹¹ that removal of the ileocolic valve may adversely affect outcome by contributing to the development of chronic diarrhea. In the present study, a portion of the ileum was resected in only 3 animals and the ileocolic valve was removed in only 1. Therefore, we could not determine whether removal of a portion of the ileum or removal of the ileocolic valve would be associated with a poorer outcome, although this has been demonstrated in previous studies.^15–19

Treatment of SBS in dogs has been aimed at providing adequate nutritional support and controlling diarrhea and other manifestations of SBS until intestinal adaptation can occur. Intestinal adaptation begins within days after surgery^3,20 and results in restoration of the absorptive capacity of the intestine through compensatory growth of the remaining intestinal segment and an increase in mucosal surface area.^20,21 Dilatation, lengthening, and thickening of the intestine are observed, along with epithelial cell proliferation in intestinal crypts and migration of cells into intestinal villi.^{3,6,16,21–23} These adaptive changes have been found to be proportional to the amount of intestine resected, with the ileum demonstrating the most substantial adaptive response.^24,25 Methods to improve intestinal adaptation in human patients have been tested and include early provision of enteral nutrition, combined with administration of recombinant human growth hormone, glutamine, and fiber; however, the superiority of 1 method over another has not been determined.^3,13,26–30 A recent study³¹ evaluated the role of glutamine and human epithelial growth factor in transplanted ileal mucosa in dogs and found little beneficial effect.

Although provision of parenteral nutritional support during hospitalization was not significantly associated with outcome or survival time in the present study, the potential benefit of parenteral nutrition in providing essential nutrients during the early postoperative period should not be overlooked. Experimentally, it has been shown that resection of 85% to 95% of the small intestine in dogs can result in weight loss, despite increased caloric intake, but that postoperative IV provision of nutrition can improve the outcome.⁶ It is also well documented that parenteral nutritional support plays an important role in the short- and long-term management of people with SBS.^{2,14,17,20,32,33} During the adaptation period, human patients are typically provided parenteral nutritional support, with the goal of transitioning to enteral nutrition. However, full adaptation may take years, and some patients never have complete recovery of intestinal function and require long-term parenteral nutrition.^2,3,32,34 A previous study³⁴ found that 1- and 4-year survival rates in people with SBS receiving parenteral nutrition were 94% and 80%, respectively, and that death was most often a consequence of complications or underlying or residual disease. Only a small percentage of animals in the present study were provided parenteral nutritional support following surgery, and prospective studies with larger numbers of animals would be necessary to establish the true effects of parenteral nutrition in these animals. Enteral nutrition is known to have a positive effect on intestinal adaptation following extensive small intestinal resection, and attempts should be made to begin enteral nutrition as soon as possible after surgery.^17,29,35 This is particularly important in veterinary medicine because of the impracticality of providing parenteral nutritional support to dogs and cats at home.

One factor that may help explain why outcome in dogs and cats that undergo extensive intestinal resection is better than that in people is differences in underlying cause. In people, the most common reasons for extensive intestinal resection are neoplastic and inflammatory diseases, whereas dogs and cats rarely undergo extensive intestinal resection for these reasons. In people that have undergone extensive intestinal resection, the remaining intestine is often diseased, which could adversely affect its ability to adapt and overall outcome,¹⁶ although 1 study³⁶ did demonstrate a better adaptive response in conjunction with inflammatory conditions. In the present study, linear and solitary foreign bodies were the most common reasons for extensive intestinal resection. Thus, it is likely that the intestine was healthy prior to resection, which may have had a positive influence on outcome. Two of the dogs in the present study were euthanized because of dehiscence of the surgical site and septic peritonitis. Whether this was a result of underlying disease, surgical factors, or other factors that adversely affected healing (eg, poor nutritional status) was not clear.

There are a number of limitations to the present study, including the fact that some cases of extensive intestinal resection during the study period may have been inadvertently missed in our review of the medical records. In addition, medical records for 5 cases could not be located. Because this was a retrospective study, it was not possible to obtain all the desired data in a consistent manner from the medical records, including the exact length of intestine excised, body weight, body condition score, and information on oral intake and fecal output during hospitalization. A prospective study would have allowed for more accurate measurements of the portion of intestine that was resected. However, measuring the amount of intestine removed is inherently difficult because of alterations associated with muscle relaxation or constriction and postmortem changes.² It has been recommended to measure the amount of intestine remaining, as opposed to the amount removed, to better correlate clinical signs with the amount of remaining intestine.¹⁴

In summary, results of the present study suggest that owners should be made aware that any dog or cat in which ≥ 50% of the small intestine is resected is at risk for short- and long-term complications. However, 17 of the 20 (85%) animals in the present study were discharged from the hospital, and 12 of 15 animals that were discharged and for which long-term follow-up information was available had a good outcome. We were not able to detect any association between outcome and age, percentage of intestine resected, or underlying cause, although this may have been related to the low number of cases in the study. Prospective studies are needed to identify treatments that will enhance intestinal adaptation and optimize outcome after extensive intestinal resection in dogs and cats.