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Gastrointestinal signs and a need for nutritional management may persist long term in dogs and cats undergoing resection of the ileocolic junction: 35 cases (2008–2020)

Catherine N. StecykDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA

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Lisa M. FreemanDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA

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Cynthia R. L. WebsterDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA

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Dominique G. PenninckDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA

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Kady MarinoDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA

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John BergDepartment of Clinical Sciences, Cummings School of Veterinary Medicine, Tufts University, North Grafton, MA

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Abstract

OBJECTIVE

To evaluate the effects of ileocecocolic junction (ICJ) resection on gastrointestinal signs, biochemical parameters, and nutritional variables in dogs and cats.

ANIMALS

20 dogs and 15 cats that underwent ICJ resection between January 2008 and June 2020.

PROCEDURES

Medical records of dogs and cats that underwent ICJ resection were reviewed, and clinical signs, laboratory abnormalities, and nutritional information were obtained. Additional follow-up information was obtained by contacting primary care veterinarians or owners. A subset of dogs (n = 6) and cats (2) were evaluated in the hospital via clinical examination, clinicopathologic testing, nutritional testing, and abdominal ultrasound.

RESULTS

Twenty dogs and 15 cats underwent resection of the ICJ for treatment of a variety of conditions. Ten of 20 dogs (50%) and 11/15 cats (73%) were reported by their owners to have a good long-term outcome based on the lack of long-term gastrointestinal signs or the ability to control gastrointestinal signs with diet and supplements alone. Despite owner-reported good outcomes, long-term diarrhea, weight loss, and muscle loss were common. Of the 6 dogs evaluated in the hospital, 3/6 (50%) had muscle loss, 2/6 (33%) had low taurine concentrations, and 1 dog each had low cobalamin, folate, 25-hydroxyvitamin D, and ionized calcium. Neither of the 2 cats evaluated in the hospital had nutritional abnormalities identified.

CLINICAL RELEVANCE

Owners should be informed of the possibility of long-term gastrointestinal clinical signs and the potential need for long-term nutritional management after ICJ resection.

Abstract

OBJECTIVE

To evaluate the effects of ileocecocolic junction (ICJ) resection on gastrointestinal signs, biochemical parameters, and nutritional variables in dogs and cats.

ANIMALS

20 dogs and 15 cats that underwent ICJ resection between January 2008 and June 2020.

PROCEDURES

Medical records of dogs and cats that underwent ICJ resection were reviewed, and clinical signs, laboratory abnormalities, and nutritional information were obtained. Additional follow-up information was obtained by contacting primary care veterinarians or owners. A subset of dogs (n = 6) and cats (2) were evaluated in the hospital via clinical examination, clinicopathologic testing, nutritional testing, and abdominal ultrasound.

RESULTS

Twenty dogs and 15 cats underwent resection of the ICJ for treatment of a variety of conditions. Ten of 20 dogs (50%) and 11/15 cats (73%) were reported by their owners to have a good long-term outcome based on the lack of long-term gastrointestinal signs or the ability to control gastrointestinal signs with diet and supplements alone. Despite owner-reported good outcomes, long-term diarrhea, weight loss, and muscle loss were common. Of the 6 dogs evaluated in the hospital, 3/6 (50%) had muscle loss, 2/6 (33%) had low taurine concentrations, and 1 dog each had low cobalamin, folate, 25-hydroxyvitamin D, and ionized calcium. Neither of the 2 cats evaluated in the hospital had nutritional abnormalities identified.

CLINICAL RELEVANCE

Owners should be informed of the possibility of long-term gastrointestinal clinical signs and the potential need for long-term nutritional management after ICJ resection.

The ileocecocolic junction (ICJ) is comprised of the ileum and the ileocolic valve, each of which has specific functions.1 The ileum is the short, terminal portion of the small intestine and plays important roles in the absorption of bile acids, proteins, fats, fat-soluble vitamins, cholesterol, and cobalamin.1 The ileocolic valve is a muscular sphincter that separates the distal ileum from the proximal colon and regulates the speed of intestinal transit.1 It functions to control movement of chyme from the terminal ileum into the ascending colon while preventing reflux of contents from the colon into the ileum.2,3

In humans, surgical resection of the ileum can lead to several important physiologic and pathologic alterations. Bile acids, which are critical to the digestion and absorption of fats, are synthesized in hepatocytes from cholesterol, conjugated with taurine or glycine, stored in the gallbladder, and excreted into the duodenum in the fed state.4 The majority of secreted bile acids are actively reabsorbed in the ileum.5 Resection of all or a portion of the ileum may therefore cause depletion of bile acids and impair digestion and absorption of fats, resulting in steatorrhea and malabsorption of the fat-soluble vitamins A, D, E, and K.57 Ileal resection may also result in a deficiency in cobalamin, which is largely absorbed in the terminal ileum.8 In the presence of steatorrhea, calcium in the stool may preferentially bind to fat rather than to oxalates prior to excretion.4 This increases the amount of oxalates absorbed in the colon, increasing the risk of formation of oxalate urinary calculi.9 About 1/3 of human patients with ileal resection develop cholesterol or pigment gallstones associated with disruption of the enterohepatic circulation of bile acids and bilirubin.9 Beyond the loss of the ileum, removal of the ICJ in humans can accelerate fecal transport, leading to diarrhea, steatorrhea, and malabsorption of nutrients such as folate, cobalamin, and 25-hydroxyvitamin D.4,6,7 The procedure may also result in reflux of colonic contents, ileal mucosal inflammation, and small intestinal bacterial overgrowth and dysbiosis.2,10 Also, jejuno-colonic anastomosis in humans often results in gastric acid hypersecretion, especially if a large portion of the jejunum is resected.11 Due to these alterations, humans with jejuno-colonic anastomosis typically require treatment with histamine H2 blockers, diets reduced in fat and oxalates, and supplementation of fiber, vitamin B12, and fat-soluble vitamins.11

In dogs and cats, resection of the ICJ with the ileum (jejuno-colonic anastomosis) or without the ileum (ileo-colonic anastomosis) is occasionally required to treat conditions such as neoplasia, intussusception, foreign body obstruction, and feline idiopathic megacolon.1214 Currently, limited clinical information is available concerning the short- and long-term consequences of ICJ resection in dogs and cats, making it challenging to provide owners with accurate expectations regarding clinical signs, gastrointestinal function, and overall prognosis after surgery. While some outcomes may be similar to what is found in human patients, it is unknown whether dogs and cats develop calcium oxalate urolithiasis, gallstones, or nutritional deficiencies. In addition, some of the metabolic differences between dogs and cats compared to humans may make other complications more likely after ICJ resection (eg, taurine deficiency in the cat). In a recent study12 evaluating outcomes in cats treated with subtotal colectomy for idiopathic megacolon, the ICJ was removed in 41 of 160 cats (25.6%). Cats that had the ICJ resection had a significantly greater risk for long-term liquid feces and fair or poor owner assessments of outcome compared with cats that did not have this segment removed.12 An experimental study15 of 5 cats demonstrated weight loss after ICJ resection. In other existing case series1618 of dogs and cats that had ICJ resections, concurrent extensive small or large intestinal resection makes it difficult to interpret the effects of removal of the ICJ independently from the extensive intestinal resection. Experimental studies1922 have shown an increase in bacterial proliferation in the terminal ileum and faster intestinal transit time following loss of the ICJ in dogs. Overall, previous studies have provided limited information regarding long-term outcome or nutritional status. Optimal diet and supplement recommendations for dogs and cats with ICJ resection are not well established, but clinical recommendations may include diets reduced in fat and supplementation of taurine, fiber, vitamin B12, and fat-soluble vitamins, along with higher-than-average calorie intake. However, subjectively, patients are highly variable in the nutritional profile of the diet and supplements required to maintain good stool quality.

The purpose of this study was to evaluate clinical signs of gastrointestinal dysfunction as well as key nutritional and laboratory data in dogs and cats after ICJ resection. We hypothesized that indicators of gastrointestinal dysfunction, clinical signs (eg, chronic diarrhea, chronic vomiting, weight and muscle loss), or laboratory abnormalities (eg, anemia, hypoalbuminemia, low taurine), would be observed.

Materials and Methods

Patient population

Medical records of dogs and cats presented to Cummings School of Veterinary Medicine at Tufts University’s Foster Hospital for Small Animals or Tufts Veterinary Emergency Treatment and Specialties between January 1, 2008 and June 1, 2020 were electronically searched using the terms ICJ, duodeno-colonic, jejuno-colonic, ileo-colonic, and anastomosis. Dogs and cats were eligible for inclusion in the study if they had undergone duodeno-colonic, jejuno-colonic, or ileo-colonic resection and anastomosis at either of the 2 hospitals and if follow-up information was available from the medical record or from contacting the primary care veterinarian or owner for data from a time point at least 2 months after surgery. Animals were excluded if they died or were euthanized within 14 days of surgery. The study included a retrospective evaluation of data as well as an in-hospital evaluation of a subset of dogs and cats.

Retrospective data collection

Data were collected from medical records at 2 time points using a standardized data form: prior to surgery (time 0) and at each patient’s most recent evaluation that occurred at least 2 months after surgery (time 1). At each of the 2 time points, data collected were signalment, breed, body weight, body condition score (BCS),23 and muscle condition score (MCS).23 Clinical signs, including vomiting, diarrhea, and hyporexia, as well as laboratory parameters that are potentially associated with chronic gastrointestinal dysfunction, were recorded (ie, packed cell volume, lymphocyte count, albumin, globulin, and cholesterol). In addition, indication for surgery, surgical procedure performed, and major surgical complications were recorded. Information on diet, dietary supplements, and medications at time 1 were recorded, although complete information was not available from the medical records for most subjects and had to be obtained from primary care veterinarians or owners. If multiple diets were being fed, the one providing the largest percentage of calories to the subject was recorded as the main diet.

All owners were contacted by telephone or email to obtain perceptions of their animal’s outcome and any information missing from the medical records. An animal was considered to have a good outcome if the owner reported normal to near-normal stool consistency, no vomiting, and no need for treatment other than dietary management or nutritional supplements. An animal was considered to have a poor outcome if the owner reported that it continued to have diarrhea or weight loss or if treatment other than dietary management and nutritional supplements was required to maintain normal to near-normal stool consistency.16

In-hospital assessment

All owners who could be contacted were invited to return for an in-hospital assessment of their animal’s clinical signs, clinicopathologic abnormalities, and concentrations of key nutrients representing malnutrition or gastrointestinal dysfunction. At this visit (time 2), body weight, BCS, MCS, presence or absence of vomiting, fecal score,24 or hyporexia was recorded. Owners provided information on clinical signs, diet, supplements, and medications prior to the hospital visit via an online survey (Qualtrics XM software; Qualtrics). Blood was collected for a complete blood count and serum biochemistry profile (Clinical Pathology Laboratory, Cummings School of Veterinary Medicine, Tufts University). Key nutrients tested included cobalamin and folate (Gastrointestinal Laboratory College of Veterinary Medicine, Texas A&M University), plasma and whole blood taurine (Amino Acid Laboratory, School of Veterinary Medicine, University of California Davis), 25-hydroxyvitamin D (as a marker for fat-soluble vitamin depletion), parathyroid hormone (PTH), and ionized calcium (Veterinary Diagnostic Laboratory, Michigan State University College of Veterinary Medicine). A complete abdominal ultrasound was performed by one of the authors (DP) to evaluate the gastrointestinal tract and surgery site and to assess the patient for cystoliths or choleliths.

Statistical analysis

Continuous data are presented as median (range), and categorical variables are presented as absolute numbers and percentages. Continuous clinicopathologic data were dichotomized based on reference ranges (ie, within or outside the reference range) for statistical comparison of these data between time 0 and time 1. McNemars’s tests were used to compare the frequency of each clinical sign and laboratory abnormality between time 0 and time 1.

Results

Signalment and surgical findings in dogs

Thirty dogs were considered for inclusion in the study, but 6 dogs were excluded because they did not survive to 14 days after surgery, and 4 were excluded because they lacked follow-up data beyond 2 months postoperatively, leaving a study population of 20 dogs. Median age at the time of surgery was 4.5 years (range, 0.1 to 15.6 years). There were 8/20 (40%) castrated male dogs, 6/20 (30%) spayed female dogs, 5/20 (25%) intact male dogs, and 1/20 (5%) intact female dog. The most common breeds were German Shepherds (n = 4), Labrador Retrievers (3), Golden Retrievers (3), mixed breed dogs (3), with 1 of each of the following: Beagle, Bullmastiff, Dachshund, French Bulldog, Great Dane, Siberian Husky, and Old English Sheepdog. At the time of surgery, median body weight was 21 (range, 3.3 to 59.8 kg), median BCS was 5 (range, 1 to 8), and 6/18 dogs had muscle loss. Indications for surgery included neoplasia (7/20 [35%]), intussusception (7/20 [35%]), and 1 of each of the following: intestinal volvulus, focal necrotizing inflammation, focal pyogranulomatous inflammation, dehiscence of a previous enterotomy, cecal ulceration, and mesenteric root abscess. Neoplasms were further classified as gastrointestinal stromal tumor (4/7), adenocarcinoma (2/7), and carcinoid (1/7). Fourteen of the 20 dogs (70%) underwent a jejuno-colonic anastomosis, 5/20 dogs (25%) underwent an ileo-colonic anastomosis, and 1 dog (5%) underwent a duodeno-colonic anastomosis. Five of the 20 dogs (25%) required a second surgery: 3 of 20 (15%) had secondary procedures performed within 3 days postoperatively due to dehiscence of the original anastomosis site, and 2 of 20 (10%; both with intussusception) required a second resection and anastomosis procedure that included intestinal enteroplication within 2 weeks due to recurrence of the intussusception.

Clinical signs in dogs

The most common clinical signs at the time of surgery included diarrhea (12/20 [60%]) and vomiting (16/20 [80%]; Table 1). Median time from surgery to time 1 was 655 days (range, 69 to 3,939 days). At time 1, weight loss (10/16) and muscle loss (7/10) were the most common clinical findings. It appeared that vomiting was well controlled and appetite improved in many patients at time 1, although the only statistically significant reduction identified in the frequency of clinical signs between time 0 and time 1 in dogs was for vomiting (P = .001).

Table 1

Pre- and postoperative values for key clinical parameters in 20 dog and 15 cats with ileocecocolic junction resection.

Clinical sign Preoperative (time 0) Postoperative (time 1)* P value
Dogs
   Weight loss N/A 10/16 (63%) N/A
   Body condition score < 4/9 3/19 (16%) 3/18 (17%) 1.00
   Muscle loss 6/18 (33%) 7/10 (70%) .10
   Diarrhea 12/20 (60%) 8/20 (40%) .16
   Vomiting 16/20 (80%) 5/20 (25%) .001
   Hyporexia 8/20 (40%) 4/20 (20%) .10
Cats
   Weight loss N/A 5/10 (50%) N/A
   Body condition score < 4/9 6/13 (46%) 3/7 (43%) 1.00
   Muscle loss 7/12 (58%) 3/4 (75%) 1.00
   Diarrhea 6/15 (40%) 3/15 (20%) .26
   Vomiting 9/15 (60%) 5/15 (33%) .16
   Hyporexia 8/15 (53%) 4/15 (27%) .16

Data are given as number of animals with the specified clinical sign/number of animals examined (percentage).

N/A = Not applicable.

*

Time 1 was the last/most-recent postoperative reevaluation.

Weight loss was defined as ≥ 0.20 kg in dogs and ≥ 0.05 kg in cats.

Any muscle loss (mild, moderate, or severe).

Laboratory abnormalities in dogs

Lymphopenia was the most common abnormality at both time 0 (7/16) and time 1 (6/15; Table 2). No statistically significant differences were identified in the frequency of any laboratory abnormality between the time 0 and time 1, although hypoalbuminemia and anemia resolved in many dogs.

Table 2

Pre- and postoperative values for key laboratory parameters in 20 dogs and 15 cats with ileocecocolic junction resection.

Laboratory value Preoperative (time 0) Time 1* P value
Dogs
   Anemia 6/20 (30%) 3/17 (18%) .26
   Lymphopenia 7/16 (44%) 6/16 (38%) .41
   Hypoalbuminemia 5/16 (31%) 1/16 (6%) .08
   Hypoglobulinemia 6/16 (38%) 2/16 (13%) .66
   Hypocholesterolemia 0/16 (0%) 1/13 (8%) N/A
Cats
   Anemia 5/15 (33%) 4/9 (44%) 1.00
   Lymphopenia 5/15 (33%) 3/9 (33%) .66
   Hypoalbuminemia 1/15 (7%) 0/7 (0%) N/A
   Hypoglobulinemia 0/15 (0%) 0/7 (0%) N/A
   Hypocholesterolemia 0/15 (0%) 0/7 (0%) N/A

Data are given as number of animals with the specified laboratory abnormality/number of animals examined (percentage).

N/A = Not applicable.

*

Time 1 was the last/most-recent postoperative reevaluation.

Nutritional information in dogs

Dietary information at time 1 was available for 18/20 dogs (90%). Ten of 18 dogs ate veterinary diets, while 8/18 ate an over-the-counter commercial dog food. The veterinary diets included reduced fat, easily digestible diets (5/18), increased fiber diets (2/18), hydrolyzed diets (2/18), and a diet designed for dogs with liver disease (1/18). Seven of the 18 dogs with dietary information received injectable cobalamin supplementation, 3/18 received long-term taurine supplementation, and 1/18 received fiber supplementation.

Outcome and owner perception of outcome in dogs

At the time of follow-up, 8/20 dogs had been euthanized (n = 6) or died (2) due to clinical signs consistent with gastrointestinal dysfunction. Of these 8 dogs, 3 died of known gastrointestinal cancer. Six dogs were euthanized (n = 3) or died (3) of causes other than gastrointestinal disease. Median survival time for all dogs was 919 days (range, 11 to 4,249 days). Four of 20 dogs (20%) were still alive, and the remaining 2 dogs (10%) were lost to follow-up. Perception of outcome was provided by owners of 18 dogs. Ten of the 18 owners reported good outcomes, indicating normal to near-normal stools with no treatment or with dietary management (diet or supplements) alone. Eight of 18 owners reported poor outcomes, indicating that diarrhea never resolved. The 2 dogs lost to follow-up were categorized as having poor outcomes based on their need for nutritional supplementation and gastrointestinal medications to maintain good stool quality from the last available information.

In-hospital assessments in dogs

Owners of 6 dogs agreed to an in-hospital assessment of gastrointestinal status (time 2; Table 3). Three of these 6 dogs were eating an over-the-counter commercial diet, while 2/6 were eating a reduced fat, easily digestible diet, and 1/6 was eating a hydrolyzed diet. The median interval between surgery, and this assessment was 715 days (range, 278 to 1,695 days). Vomiting was uncommon at time 2, but diarrhea was common with 4/6 dogs having a fecal score > 5/7.24 Anemia, lymphopenia, hypoglobulinemia, and hypocholesterolemia were uncommon at both time points.

Table 3

Comparison of clinical and laboratory parameters in 6 dogs that returned for a final postoperative reevaluation after ileocecocolic junction resection (n = 6).

Variable Preoperative (time 0) Reevaluation (time 2)*
Weight (kg) 22.5 (5.0–38.7) 31.3 (10.0–42.1)
Body condition score (9-point scale) 4 (2–7) 7 (3–7)
   Body condition score < 4/9 1/6 1/6
Muscle condition score
   Normal 4/6 3/6
   Mild muscle loss 2/6 2/6
   Moderate muscle loss 0/6 1/6
   Severe muscle loss 0/6 0/6
Diarrhea 5/6 4/6
   Fecal score > 5/7 N/A 4/6
Vomiting 6/6 1/6
Hyporexia 2/6 0/6
Hematocrit (reference range, 39–55%) 39 (27–59) 49 (34–57)
   Anemia 1/6 1/6
Lymphocytes (reference range, 1.1–4.8 k/μL) 1.69 (0.35–2.58) 1.29 (0.64–1.91)
   Lymphopenia 1/5 2/6
Albumin (reference range, 2.8–4.0 g/dL) 2.6 (2.1–3.3) 3.7 (3.3–3.9)
   Hypoalbuminemia 3/5 0/6
Globulin (reference range, 2.3–4.2 g/dL) 2.7 (2.1–4.2) 2.4 (2.2–3.2)
   Hypoglobulinemia 1/5 2/6
Cholesterol (reference range, 82–355 mg/dL) 168 (104–220) 168 (99–190)
   Hypocholesterolemia 0/6 0/6

Data are given as number of animals with the specified clinical sign or laboratory abnormality/number of animals examined. For continuous data, values represent median and range.

N/A = Not available.

*

Time 2 was the in-hospital clinical reevaluation conducted as part of the study.

At the time of the reevaluation at our hospital, 2/6 dogs had low whole blood and plasma taurine concentrations; neither dog was receiving taurine supplementation (Table 4). One dog had a low cobalamin concentration despite cobalamin supplementation. One dog each had low folate, 25-hydroxyvitamin D, and ionized calcium concentrations. No dog had an abnormal PTH. On abdominal ultrasound, the resection anastomosis site was identified in 2/6 dogs and focal thickening with loss of layering was noted in 1/6 dogs. The colon was thickened with maintained layering in 1/6 dogs. The gastrointestinal tract was otherwise normal. There were no cystic calculi or choleliths in any dog.

Table 4

Diet and supplement information and nutritional testing in 6 dogs and 2 cats that returned for an in-hospital clinical reevaluation after ileocecocolic junction resection.

Patient Abnormal clinical signs Abnormal laboratory results Abnormal nutritional testing Diets Supplements
Dog 1 Fecal score 6/7 Hypoglobulinemia (2.2 g/dL)a None Veterinary hydrolyzed dry B12c
Lymphopenia (0.64 k/μL)b Fiber
Dog 2 Mild muscle loss None None Veterinary reduced-fat dry B12c
Probiotic
Taurine
Dog 3 BCS 3/9 None Cobalamin < 150 ng/Ld Veterinary low-fat dry B12c
Moderate muscle loss 25-Hydroxyvitamin D = 22 nmol/Le,f
Fecal score 7/7
Dog 4 Mild muscle loss Lymphopenia (0.97 k/μL)b Plasma taurine = 35 nmol/mLg Over-the-counter dry None
Fecal score 5/7 Whole blood taurine = 169 nmol/mLg
Vomiting
Dog 5 None Anemia (34%)h None Over-the-counter dry Probiotic
Dog 6 Fecal score 5/7 Hypoglobulinemia (2.2 g/dL)a Folate = 5.1 μg/Li Over-the-counter dry B12c
Plasma taurine = 31 nmol/mLg
Whole blood taurine = 151 nmol/mLg
Ionized calcium = 1.48 nmol/Le,j
Cat 1 None None None Over-the-counter wet B12c
Cat 2 Vomiting None None Over-the-counter dry B12c

B12 = Vitamin B12. BCS = Body condition score.

a

Globulin (reference range, 2.3–4.2 g/dL).

b

Lymphocytes (reference range, 1.1–4.8 k/μL).

c

All B12 supplementation was administered subcutaneously.

d

Cobalamin (reference range, 251–908 ng/L).

e

These patients had parathyroid hormone values within the reference range.

f

25-Hydroxyvitamin D (reference range, 109–423 nmol/L).

g

Taurine (plasma reference range, 60–120 nmol/mL; whole blood reference range, 200–350 nmol/mL).

h

Hematocrit (reference range, 39–55%).

i

Folate (reference range, 7.7–24.4 μg/L).

j

Ionized calcium (reference range, 1.25–1.45 mmol/L).

Signalment and surgical findings in cats

Twenty-two cats were considered for inclusion in the study, but 4 cats were excluded because they did not survive to 14 days after surgery, and 3 cats were excluded because they lacked data beyond 2 months postoperatively, leaving a study population of 15 cats. Median age at the time of surgery was 12.5 years (range, 4.9 to 15.7 years). There were 9/15 spayed female cats, 5/15 castrated male cats, and 1/15 intact male cat. Most cats were domestic short or longhair cats (n = 13), with 1 Balinese and 1 Siamese. Median body weight at the time of surgery was 3.8 kg (range, 2.5 to 7.5 kg), median BCS was 4 (range, 2 to 9), and 7/12 cats had muscle loss. Reasons for surgery included neoplasia (n = 12 [80%]), intussusception (2 [13%]), and cecal abscess (1 [7%]). Neoplasms were further classified as adenocarcinoma (7), lymphoma (3), carcinoma (1), and mast cell tumor (1). Eight of 15 cats had a jejuno-colonic anastomosis performed, and 7/15 cats had an ileo-colonic anastomosis performed. No cats had surgical complications requiring a second procedure. Median time from surgery to time 1 was 629 days (range, 133 to 2,143 days).

Clinical signs in cats

The most common clinical signs in cats at the time of surgery were vomiting (9/15) and hyporexia (8/15; Table 1). At time 1, weight loss (5/10) and muscle loss (3/4) were common, while clinical signs of vomiting, hyporexia, and diarrhea had decreased in several cats. However, statistically significant differences were not noted in the frequency of any clinical sign between the preoperative timepoint (time 0) and time 1.

Laboratory abnormalities in cats

Anemia and lymphopenia were both present in 5/15 of cats at the time of surgery, but unlike dogs, hypoalbuminemia was rare (Table 2). No statistically significant differences were noted in the frequency of any laboratory abnormality between the preoperative time point (time 0) and time 1.

Nutritional information in cats

Long-term dietary information was available for 14/15 cats. Twelve of 14 cats ate over-the-counter dry or wet commercial cat foods, while 1/14 ate an easily digestible veterinary diet and 1/14 was fed a veterinary critical care diet through an esophagostomy tube. Three of the 14 cats with dietary information received injectable cobalamin supplementation. No cats received long-term supplementation with taurine or any other dietary supplements.

Outcome and owner perception of outcome in cats

At the time of follow-up, 7/15 cats had been euthanized (n = 6) or died (1) due to clinical signs consistent with gastrointestinal dysfunction. All 7 of these cats had neoplastic conditions at the ICJ. Six of 15 cats had been euthanized (n = 4) or died (2) of causes other than gastrointestinal disease. Median survival time for all cats was 697 days (range, 42 to 2,532 days). Two of 15 cats remained alive. Perception of outcome was provided by owners of all 15 cats. Eleven of 15 owners reported good outcomes, indicating normal to near-normal stools with no treatment or with dietary management alone. Four of 15 owners reported poor outcomes, indicating that diarrhea never resolved.

In-hospital assessments in cats

Owners of 2 cats agreed to an in-hospital reassessment (time 2; Table 4). Both of these cats were eating over-the-counter commercial diets. The time intervals between surgery and this assessment were 399 and 1,608 days. Neither cat had abnormal nutrient testing results, although both were receiving cobalamin supplementation. The resection-anastomosis site was seen in both cats on abdominal ultrasound. Diffuse jejunal thickening (up to 3.5 mm) was present in both cats, and additional multifocal circumferential jejunal lesions were observed in 1 cat (including the resection and anastomosis site). Cytology and PCR for antigen receptor rearrangements of these lesions ruled out a neoplastic etiology. One cat had gallbladder sludge, bilateral chronic nephropathy changes, and numerous primarily hyperechoic nodules disseminated throughout the liver, consistent with cystadenomas. No gallbladder or urinary bladder stones were seen.

Discussion

The results of this study indicate that evidence of long-term gastrointestinal dysfunction is common in dogs and cats after undergoing ICJ resection. Despite this, 50% of dog owners and 73% of cat owners reported good long-term outcome with signs controlled to their satisfaction with no intervention or with diet and supplements alone. It is possible that some owners felt their pet’s quality of life was good despite the presence of biochemical abnormalities or occasional soft stools. For the purpose of this study, gastrointestinal dysfunction was defined by multiple indicators including clinical signs (eg, vomiting, diarrhea, hyporexia), physical exam findings (poor BCS and muscle loss), and biochemical abnormalities (eg, low protein, vitamin D, cobalamin, or taurine). The current study demonstrated that a substantial proportion of these patients continued to have exhibited signs of gastrointestinal dysfunction at long-term time points after ICJ resection.

Numerous studies have demonstrated the importance of preservation of the ICJ during intestinal resection.15,22,2527 The ICJ is an important neuronal regulator of colonic motility and intestinal transit, and ICJ resection can alter the intrinsic neuronal activity of the gut, contributing to decreased intraluminal colonic water absorption, diarrhea, and subsequent weight loss.3 Dogs with ICJ resection also have higher levels of coliform bacteria in their jejunum compared to dogs with either proximal or distal small intestinal resections that maintain the ICJ.22 This small bowel overgrowth can lead to modulation of intestinal luminal contents such as hydroxylation of short-chain fatty acids and deconjugation of bile acids, which serve as secretagogues in the colon. The increased levels of short-chain fatty acids can also attenuate ghrelin-mediated signaling in the gut.28 Ghrelin receptors play a key role in maintaining energy balance and centrally modulating food intake28; therefore, suppression of this signaling has the potential to have significant consequences on metabolism, weight loss, and muscle loss and may explain the changes seen in the current study.

Since the colon is an important site of water absorption and electrolyte balance for cats and dogs,12,17,29 chronic gastrointestinal signs in some patients could have been related to the amount of colon resected along with the ICJ. Due to the retrospective nature of the study, information regarding the exact proportions of the small and large intestine removed along with the ICJ was not available. It is reasonable to suspect that patients with more extensive colonic resections would suffer from chronic diarrhea compared to those with very small colonic resections due to reduced water absorption. However, jejuno-colonic anastomosis in humans is commonly associated with long-term gastrointestinal signs and malnutrition, even in the absence of extensive colonic resection, due to the loss of the sphincter function of the ICJ regulating the speed of intestinal transit.1

The laboratory parameters evaluated in the current study were chosen based on their presumed likelihood to be abnormal in the presence of chronic gastrointestinal dysfunction or malnutrition (ie, anemia, lymphopenia, hypoproteinemia, hypoglobulinemia, and hypocholesterolemia), although none are sensitive or specific. Many of these parameters were abnormal in both dogs and cats preoperatively. At time 1, some of the abnormalities like hypoalbuminemia and hypoglobulinemia, important indicators of chronic malabsorption, were less common. However, anemia was present in 3 of 17 dogs and 4 of 9 cats, and lymphopenia was present in 6 of 16 dogs and 3 of 9 cats at time 1. These changes could be related to the ICJ resection or to other chronic medical conditions. These results need to be viewed with the caveats that the time from surgery to time 1 was highly variable and short in some animals and that values were not measured in all cats and dogs. Therefore, further assessment of these parameters in dogs and cats after ICJ resection is warranted.

Although evaluation of select data from complete blood count and biochemistry profiles from all dogs postoperatively demonstrated metabolic abnormalities were relatively uncommon, when further nutritional evaluation was carried out in a subgroup of these dogs (time 2), more abnormalities were revealed. These included low taurine concentrations in 2/6 dogs, and 1 dog each with low cobalamin (despite supplementation), low folate, low 25-hydroxyvitamin D, and low ionized calcium concentrations. Similar nutritional abnormalities have been reported in humans with jejuno-colonic anastomosis.1 This suggests that nutritional abnormalities present in humans with jejuno-colonic anastomosis can be seen in dogs undergoing ICJ resection. Previous studies30 have demonstrated that dogs with chronic enteropathies can have lower 25-hydroxyvitamin D concentrations as compared to normal dogs, and the pathogenesis of this is thought to be multifactorial.31 These factors could include reduced dietary intake and fat malabsorption/maldigestion.31 Further research is necessary, but supplementation of key nutrients (eg, taurine, vitamin B12) and monitoring concentrations of other nutrients (eg, fat-soluble vitamins) are warranted after ICJ resection.

An additional important finding of the current study was that the long-term nutritional needs were not adequately addressed in many patients. Many patients had ongoing gastrointestinal dysfunction without retrospective evidence that the owners received a nutrition consultation on the use of targeted diets or supplements. Since the results of this study demonstrated that biomarkers of gastrointestinal dysfunction were common in dogs and cats long term, the importance of postoperative nutritional management should be discussed with owners prior to surgery. Postoperatively the dogs and cats should be proactively monitored by regular assessment of body weight, BCS, and MCS, and pertinent biochemical parameters (PCV and lymphocyte counts) and by monitoring and supplementing nutrient concentrations as needed (eg, cobalamin, taurine, vitamin D, and fat-soluble vitamins). Dogs and cats appear to be highly variable in their response after ICJ resection or extensive intestinal resection, with some having normal stools and weight/muscle maintenance relatively soon after surgery with standard over-the-counter diets, while others require a great deal of trial and error to find the right combination of diet, calories (often requiring higher-than-average calorie intake to maintain weight), supplemental fiber, and nutrient supplementation. Interestingly, in contrast to some humans with ICJ resection, the development of calcium oxalate urocystoliths or pigment gallstones was not observed in our group of dogs and cats, although only a small number of animals underwent evaluation for these findings.

This study had numerous limitations. These included incomplete medical record information, differences in surgical and postoperative management protocols, and a wide range of follow-up times. The prolonged follow-up period in some patients may have resulted in the loss of data due to poor owner recall or loss to follow-up. The number of animals available for in-hospital assessment was limited by a variety of factors including loss of patients due to death or euthanasia, especially in those that had surgeries in the earlier part of the study time frame, and COVID-19-related issues impacting in-hospital research. Baseline values for the patients’ cobalamin, folate, 25-hydroxyvitamin D, ionized calcium, PTH, and taurine concentrations were also not available, and some of these patients may have had nutritional deficiencies preoperatively. These changes observed may have been due to uncontrolled gastrointestinal disease such as neoplasia, independent of ICJ resection. All patients with neoplastic diagnoses had focal tumors resected at the time of their surgery, but occult recurrent or metastatic disease could have had an influence on biochemical abnormalities such as anemia or on clinical findings such as poor body condition score and weight loss. The doses of supplements (eg, cobalamin, taurine) that patients were receiving were also unknown, making it impossible to know if the treatment was adequate for their needs. Additionally, 25-hydroxyvitamin D was the only fat-soluble vitamin examined in the current study. The impact of vitamin K loss on bleeding has been shown in other veterinary studies,32,33 and it remains unclear if patients undoing ICJ resection are at an increased risk for coagulopathy secondary to hypovitaminosis K. Finally, the small number of cases limited statistical power.

In summary, the results of the present study suggest that, while most patients were reported by their owners to have a good outcome, long-term diarrhea, weight loss, and muscle loss were relatively common. Therefore, owners should be informed of the potential for long-term adverse gastrointestinal clinical signs. In addition, proactively monitoring body weight, BCS, and MCS and adjusting nutrient concentrations (eg, cobalamin, taurine, vitamin D, and fat-soluble vitamins) should be considered essential in any patient undergoing ICJ resection.

Acknowledgments

In the last 3 years, Dr. Freeman has received research funding from, given sponsored lectures for, and/or provided professional services to Aratana Therapeutics, Elanco, Guiding Stars LLC, Nestlé Purina PetCare, P&G Pet Care (now Mars), and Royal Canin. In the last year, Dr. Webster has received funding from the American Kennel Club and Alcor Industries. The authors thank Jim and Celeste Stoff for their financial support of the study.

The authors declare that there were no conflicts of interest.

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Contributor Notes

Corresponding author: Dr. Stecyk (catherine.stecyk@gmail.com)