Comparison of patient outcomes following enterotomy versus intestinal resection and anastomosis for treatment of intestinal foreign bodies in dogs

Daniel J. Lopez From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Sarah A. Holm From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Barbara Korten From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Jared I. Baum From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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James A. Flanders From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Julia P. Sumner From the Department of Clinical Sciences, College of Veterinary Medicine, Cornell University, Ithaca, NY 14853.

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Abstract

OBJECTIVE

To quantify the relative risk of intestinal dehiscence in dogs undergoing intestinal resection and anastomosis (IRA), compared with enterotomy, for surgical management of small intestinal foreign bodies, and to evaluate the association between nasogastric tube placement for early enteral nutrition (EEN) and hospitalization time.

ANIMALS

211 dogs undergoing 227 surgeries for intestinal foreign body removal.

PROCEDURES

Medical records were reviewed for dogs undergoing a single-site sutured enterotomy or IRA for foreign body intestinal obstruction between May 2008 and April 2018. Multivariable logistic regression was used to quantify the association between surgical procedure and dehiscence. Multiple linear regression was used to quantify the association of nasogastric tube placement with total hospitalization time.

RESULTS

Dehiscence rates were 3.8% (7/183) and 18.2% (8/44) for enterotomy and IRA, respectively. Overall dehiscence rate for all surgeries was 6.6% (15/227). The odds of intestinal dehiscence for IRA were 6.09 times (95% CI, 1.89 to 19.58) the odds for enterotomy. An American Society of Anesthesiologists score > 3 (OR, 4.49; 95% CI, 1.43 to 14.11) and an older age (OR, 1.02 [95% CI, 1.01 to 1.02] for each 1-month increase in age) were significantly associated with greater odds of intestinal dehiscence, regardless of surgical procedure. Placement of a nasogastric tube was not associated with intestinal dehiscence or decreased total hospitalization time when controlling for the year of surgery.

CONCLUSIONS AND CLINICAL RELEVANCE

Patients undergoing IRA were at a significantly higher risk of intestinal dehiscence, compared with patients undergoing enterotomy. Although this finding should not be used to recommend enterotomy over IRA, this information may be useful in guiding owner expectations and postoperative monitoring.

Abstract

OBJECTIVE

To quantify the relative risk of intestinal dehiscence in dogs undergoing intestinal resection and anastomosis (IRA), compared with enterotomy, for surgical management of small intestinal foreign bodies, and to evaluate the association between nasogastric tube placement for early enteral nutrition (EEN) and hospitalization time.

ANIMALS

211 dogs undergoing 227 surgeries for intestinal foreign body removal.

PROCEDURES

Medical records were reviewed for dogs undergoing a single-site sutured enterotomy or IRA for foreign body intestinal obstruction between May 2008 and April 2018. Multivariable logistic regression was used to quantify the association between surgical procedure and dehiscence. Multiple linear regression was used to quantify the association of nasogastric tube placement with total hospitalization time.

RESULTS

Dehiscence rates were 3.8% (7/183) and 18.2% (8/44) for enterotomy and IRA, respectively. Overall dehiscence rate for all surgeries was 6.6% (15/227). The odds of intestinal dehiscence for IRA were 6.09 times (95% CI, 1.89 to 19.58) the odds for enterotomy. An American Society of Anesthesiologists score > 3 (OR, 4.49; 95% CI, 1.43 to 14.11) and an older age (OR, 1.02 [95% CI, 1.01 to 1.02] for each 1-month increase in age) were significantly associated with greater odds of intestinal dehiscence, regardless of surgical procedure. Placement of a nasogastric tube was not associated with intestinal dehiscence or decreased total hospitalization time when controlling for the year of surgery.

CONCLUSIONS AND CLINICAL RELEVANCE

Patients undergoing IRA were at a significantly higher risk of intestinal dehiscence, compared with patients undergoing enterotomy. Although this finding should not be used to recommend enterotomy over IRA, this information may be useful in guiding owner expectations and postoperative monitoring.

Introduction

Intestinal obstruction secondary to foreign body ingestion is a common indication for gastrointestinal surgery in dogs, often necessitating either enterotomy or IRA.1 The decision to perform an enterotomy as opposed to an IRA is made on the basis of intraoperative assessment of intestinal viability. Although seemingly intuitive that performing an IRA would lead to a higher dehiscence rate than performing an enterotomy, reports2,3,4,5,6,7,8,9,10 on intestinal dehiscence rates following these 2 procedures are varied. Several studies2,3,4,5,6,7,8,9 that examined dogs undergoing IRA for various indications report dehiscence rates of 8.8% to 15.4%, whereas a study10 that focused only on enterotomies for foreign bodies identifies a dehiscence rate of 2.0%. Interestingly, a report11 of small intestinal biopsies documents an intestinal dehiscence rate of 12%, which is more similar to dehiscence rates of IRAs. The wide range of intestinal dehiscence rates across studies precludes the ability to adequately evaluate the effect of IRA versus enterotomy on intestinal dehiscence, which is important, as it may help prognosticate the patient's recovery.

Several risk factors for postoperative intestinal dehiscence have been identified in the literature, including the presence of preoperative septic peritonitis,2,3,8,12 low serum albumin concentration,8,12 and hypotension.9,12 Patients with intestinal foreign bodies have been implicated as having either a protective12 or harmful association8 with intestinal dehiscence. Patients undergoing stapled anastomosis have demonstrated lower incidences of intestinal dehiscence, compared with those undergoing sutured anastomosis, in certain situations, especially when septic peritonitis is present.2,3 Overall, risk factors are not consistently repeatable across studies, as multiple interconnected factors likely play a role in intestinal healing.

Early enteral nutrition has been defined in human trauma patients as the administration of enteral support within 48 hours after trauma.13 The use of EEN following intestinal surgery has multiple proposed benefits in both dogs and people, including having a positive effect on mucosal cell health,14 intestinal motility,15 and intestinal healing,16 thereby reducing the risk of bacterial translocation and ameliorating the systemic inflammatory response.17 Clinical trials18,19,20,21 in human patients have confirmed that these proposed benefits translate to improved clinical outcomes, with reductions in infections, gastrointestinal and respiratory complications, mortality rate, and duration of hospital stay for acutely ill patients and patients undergoing gastrointestinal surgery. All these benefits could apply to dogs; however, the typical hospitalization period, range and incidence of postoperative morbidities, and level of patient compliance may all be substantially different in veterinary populations. Although retrospective observational studies22,23 in select populations have suggested a benefit to EEN in dogs, to our knowledge, no randomized controlled clinical trials have been performed.

To our knowledge, only a single study5 in dogs has documented an increased risk of intestinal dehiscence for patients undergoing IRA, compared with enterotomy, for all intestinal procedures; however, that study5 was performed in a nonuniform population, potential confounding factors were not controlled for, and the association was not quantified. Secondarily, we are unaware of any study evaluating the association between EEN implementation and both hospitalization time and intestinal dehiscence in dogs undergoing intestinal surgery for foreign body removal.

The purposes of the study reported here were to quantify the relative risk of intestinal dehiscence in dogs undergoing IRA, compared with enterotomy, for surgical management of small intestinal foreign bodies, while controlling for confounding variables, and to evaluate the association between nasogastric tube placement for EEN and hospitalization time. Our hypotheses were that there would be an increased rate of intestinal dehiscence in dogs undergoing IRA for foreign body removal, compared with those undergoing enterotomy, and that placement of a nasogastric tube with intent to provide EEN would have a positive association with outcome by decreasing postoperative total hospitalization time and decreasing the postoperative time until first voluntary food intake without impacting the overall dehiscence rate.

Materials and Methods

Animals

The electronic medical records at the Cornell University Hospital for Animals were reviewed for all dogs undergoing either single-site sutured enterotomy or IRA because of mechanical obstruction secondary to foreign body ingestion between May 1, 2008, and April 7, 2018 (Figure 1). Exclusion criteria included lack of adequate follow-up information and missing information regarding the following: type of surgical procedure, whether there was placement of a nasogastric tube, description of postoperative appetite, total hospitalization time, diagnosis of preoperative septic peritonitis, performance of a stapled anastomosis, multiple enterotomies or IRAs, or a combination of both enterotomy and IRA.

Figure 1
Figure 1

Flow diagram depicting how surgical events were selected for analysis, including surgical event identification, loss as a result of exclusion criteria, and classification made on the basis of surgical procedure.

Citation: Journal of the American Veterinary Medical Association 258, 12; 10.2460/javma.258.12.1378

Patients with a diagnosis of preoperative septic peritonitis and stapled anastomoses were specifically excluded from the study to create a patient population as uniform as possible to minimize the number of previously known confounding factors during analysis. Patients were not excluded if a gastrotomy was performed concurrently with either enterotomy or IRA. Adequate follow-up information was defined as clinical information obtained by documented communication (reexamination by a veterinarian or telephone or email correspondence with the owner) within a minimum of 5 days after the primary surgical intervention or development of intestinal dehiscence, with a note that the patient was doing clinically well. Dogs with multiple separate surgical events were included and evaluated as separate events as long as the surgical interventions occurred more than 4 weeks apart. All procedures were performed by a board-certified surgeon or surgical resident.

Data collection

Preoperative data—Data pertaining to each dog were derived from the medical record and included information on breed, sex, neuter status, serum biochemical variables, body weight, and age at the time of surgery.

Surgical data—Data pertaining to each surgical event included the year that surgery was performed, ASA score,24 experience level of surgeon (resident year or board-certified surgeon), anesthesia time, occurrence of intraoperative hypotension (mean arterial pressure, < 60 mm Hg),25 and patient's minimum recorded intraoperative body temperature. Details of the surgical procedure included procedure type (enterotomy vs IRA), number of enterotomies or IRAs, location of surgery, type of foreign material, method of intestinal closure (suture type, size, and pattern vs staples), and total procedure time. Any intestinal perforations found at the time of surgery were also recorded. Intestinal viability was identified by use of both visual and tactile sensation with regard to the intestinal color, presence of arterial pulsations, and identification of peristalsis.

Postoperative data—Postoperative data collection included duration of hospitalization, whether or not a nasogastric tube was placed at the time of surgery, and elapsed time to voluntary postoperative food intake. Intestinal dehiscence (defined by the finding of septic peritoneal fluid or visualization at surgery during initial hospitalization or upon representation to hospital after hospital discharge), time to postoperative intestinal dehiscence, and time of death were recorded.

Nasogastric tube placement

Patients underwent nasogastric tubea placement at the time of surgery at the discretion of the surgeon for the purpose of administration of EEN. Standard-of-care EEN protocol at our hospital included the administration of a commercially available liquid dietb at a third of the resting energy requirement commencing during the first 24 hours after surgery. This rate was increased by a third of the resting energy requirement every 24 hours, if tolerated by the patient, until the resting energy requirement was reached. Tube position was confirmed within the gastric lumen by palpation at the time of surgery or by postoperative radiography.

Statistical analysis

Continuous data were assessed for normality of distribution with the Shapiro-Wilk test. Descriptive population statistics at baseline were reported as frequency (%) for categorical data, mean ± SD for normally distributed continuous data, or median (IQR) for nonnormally distributed continuous data. A causal diagram was created (Figure 2) to identify putative factors confounding the relationship between procedure type and intestinal dehiscence. Associations between intestinal dehiscence and the variables identified to influence intestinal healing in the casual diagram were evaluated with the χ2 or Fisher exact test (if n < 5 for any cell) for dichotomous variables, Student t test for normal continuous variables, or Wilcoxon rank sum test for nonnormal continuous variables. A multivariable logistic regression model was used to quantify the association between surgical procedure and odds of intestinal dehiscence while controlling for the confounding variables previously identified as being associated with intestinal dehiscence (P < 0.05) as well as confounding variables affecting the decision to perform an IRA versus enterotomy as previously identified from the causal diagram. Missing data were incorporated as the mean or median value in multivariable logistic regression, depending on the distribution, if < 10% of the data set was missing. Violation of the independence assumption (for patients with multiple repeat visits) was controlled by means of robust variance estimation. Postestimation model checking was performed through evaluation of the area under the receiver operating characteristic curve.

Figure 2
Figure 2

Causal diagram created to identify confounding factors of surgical procedure on intestinal dehiscence. Arrowheads indicate the direction of a presumed influence of the factor in one box on that in another.

Citation: Journal of the American Veterinary Medical Association 258, 12; 10.2460/javma.258.12.1378

A multiple linear regression model was used to evaluate the association between nasogastric tube placement and postoperative hospitalization time. Assumptions of normality, linearity, multicollinearity, and heteroscedasticity were evaluated and deemed to be acceptable. All statistical calculations were performed with the aid of statistical software.c

Results

Study population

Of the 369 surgical events that were identified as an intestinal procedure for foreign body obstruction during the defined study period, 280 met the pre-defined follow-up criteria. Of the 280 surgical events with appropriate follow-up, 227 surgical events in 211 dogs met the remaining inclusion criteria for analysis. These 227 procedures were then used for statistical analysis (Figure 1).

Sex distribution was 144 (144/211 [68.2%]) male dogs and 67 (67/211 [31.8%]) female dogs. Of male and female dogs, 32 (32/144 [22.2%]) and 13 (13/67 [19.4%]) were sexually intact, respectively. On the basis of a historical 10-year male-to-female ratio of 1:1 at hospital admission, male dogs were 2.1 times as likely to be admitted for foreign body ingestion as were female dogs (mean 0.68; 95% CI, 0.62 to 0.75; P < 0.001). A total of 66 breeds were represented. Dogs were most commonly classified as either mixed-breed dog (49/211 [23.2%]) or Labrador Retriever (28/211 [13.3%]). Median age at the time of presentation was 4.0 years (IQR, 1.2 to 7.5 years). Median body weight at presentation was 24.9 kg (54.8 lb; IQR, 15 to 32.7 kg [33 to 71.9 lb]).

Surgical events

Of the 227 surgeries performed, 183 (80.6%) were a single enterotomy and 44 (19.4%) were a single IRA (Figure 1). The intestinal location of the foreign body was identified during the 227 surgeries as follows: duodenum, 18.1% (41/227); jejunum, 76.2% (173/227); ileum, 4.8% (11/227); and unspecified, 0.9% (2/227). A subset of dogs underwent 2 (10 dogs, 20/227 [8.8%]) or 3 (3 dogs, 9/227 [4.0%]) separate surgical events during the evaluated period.

Procedures were performed by a board-certified surgeon in 3.1% (7/225) of surgeries, third-year surgical resident in 24.4% (55/225) of surgeries, second-year resident in 38.7% (87/225) of surgeries, and first-year resident in 33.8% (76/225) of surgeries when data on dogs were available. There was no significant (P = 0.268) difference between surgical experience and whether enterotomy or IRA was performed. Median anesthesia time was 160 minutes (IQR, 130 to 200 minutes), and median procedure time was 100 minutes (IQR, 80 to 125 minutes). Enterotomy procedures were significantly (P < 0.001) shorter (median, 95 minutes; IQR, 80 to 115 minutes), compared with IRA (median, 150 minutes; IQR, 120 to 187.5 minutes).

At the time of surgery, 5.7% (13/227) of surgeries were found to have intestinal perforations. Dogs that had evidence of intestinal perforations were at significantly (P < 0.001) higher odds (OR, 17.6; 95% CI, 4.9 to 62.4) of undergoing an IRA, compared with dogs without evidence of intestinal perforation. A nasogastric tube was placed in dogs with the intent to provide EEN in 47.6% (108/227) of surgeries. Nasogastric tube placement was significantly (P < 0.001) more likely (OR, 13.8; 95% CI, 7.34 to 26.2) in the years 2015 and after (83/106 [78.3%]) than before 2015 (25/121 [20.7%]).

The dehiscence rate for enterotomy was 3.8% (7/183) and for IRA was 18.2% (8/44). The overall dehiscence rate for all surgeries was 6.6% (15/227). Nine of 15 (60%) dogs underwent a subsequent exploratory laparotomy, which confirmed the diagnosis of dehiscence. Following 4% (9/227) of surgeries, foreign body ingestion resulted in either death or euthanasia of the patient secondary to complications associated with surgery. Six of 9 dogs were euthanized because of intestinal dehiscence without repeated surgical intervention given suspected poor prognosis and owner financial constraints. The median duration until diagnosis of dehiscence was 87.1 hours (IQR, 59 to 106.4 hours) after initial surgery, with a maximum time of 132 hours.

Median time of total hospitalization was 75.8 hours (IQR, 55.0 to 98.8 hours). Median time of total hospitalization was significantly (P = 0.003) longer for patients undergoing IRA (96.9 hours; IQR, 68.8 to 121.9 hours) than for patients undergoing enterotomy (median, 72.7 hours; IQR, 54.3 to 95.8 hours). Median time to follow-up was 31 days (IQR, 12 to 394 days). Patient follow-up was obtained at recheck examination (90/227 [39.6%]), from phone or email record (83/227 [36.6%]), from unrelated future examination (36/227 [15.9%]), from time of hospital discharge (3/227 [1.3%]), or because of a diagnosis of an outcome of interest (ie, dehiscence; 15/227 [6.6%]).

Univariable analysis evaluating associations of IRA versus enterotomy with intestinal dehiscence

The odds of a patient undergoing IRA and then experiencing dehiscence were 5.59 (95% CI, 1.97 to 15.82; P = 0.002) times the odds of a patient undergoing enterotomy when confounding variables were not controlled. Confounding variables, including age, serum albumin concentration, ASA score > 3, surgery performed by a first-year resident, hypotension, hypothermia, placement of a nasogastric tube for EEN, linear foreign body, intestinal perforation, and serum total solids concentrations, were evaluated for association with intestinal dehiscence (Figure 2; Table 1).

Table 1

Evaluation of the association between confounding variables identified in Figure 2 and intestinal dehiscence in 211 dogs undergoing 227 surgeries for intestinal foreign body removal in the present study.

Intestinal dehiscence
Variables No. of dogs with variable recorded Absent Identified P value*
Age (m) 227 45.9 (14.6–86.7) 79.0 (47.5–114.1) 0.013
Serum albumin (g/dL) 120 3.28 ± 0.8 2.8 ±.28 0.083
Surgery performed by a first-year resident§ 227 71/76 (93.4) 5/76 (6.6) 0.616
Hypotension (MAP < 60 mm Hg)§ 224 101/108 (93.5) 7/108 (6.5) 0.675
Lowest intraoperative body temperature (°F) 218 95.75 ± 0.12 95.03 ± 0.43 0.153
ASA score > 3§ 205 23/29 (79.3) 6/29 (20.7) 0.001
Nasogastric tube placement for EEN§ 227 100/108 (92.6) 8/108 (7.4) 0.644
Linear foreign body§ 227 61/68 (89.7) 7/68 (10.3) 0.144
Intestinal perforation§ 227 11/13 (84.6) 2/13 (15.4) 0.208
Serum total solids (g/dL) 223 7.19 ± 0.07 7.25 ± 0.37 0.835

To convert body temperature from °F to °C, subtract 32 and multiply by 5/9.

Variables with values of P < 0.05 were targeted to be included within the final multivariable model.

Median (IQR).

Mean ± SD

Number of dogs (%).

MAP = Mean arterial pressure.

For the age variable, 212 dogs did not have intestinal dehiscence and 15 dogs did. For the serum albumin concentration variable, 111 dogs did not have intestinal dehiscence and 9 dogs did. For the lowest intraoperative body temperature variable, 206 dogs did not have intestinal dehiscence and 12 dogs did. For the serum total solids concentration variable, 209 dogs did not have intestinal dehiscence and 14 did.

Multivariable analysis evaluating the association of IRA versus enterotomy with intestinal dehiscence

Variables selected for the final multivariable model were determined from the causal diagram (Figure 2) and the documented associations with intestinal dehiscence (Table 1). Variables having an effect on the decision to perform an IRA versus enterotomy were included in the final multivariable model regardless of significance. Variables influencing intestinal healing capabilities without affecting surgical decision-making were included only if a significant association was identified with intestinal dehiscence.

The final multivariable model was developed (Table 2). The odds of a patient undergoing IRA and subsequently experiencing dehiscence were 6.09 times (95% CI, 1.89 to 19.58; P = 0.002) the odds of a patient undergoing enterotomy. In addition, the multivariable model identified an ASA score > 3 (OR, 4.49; 95% CI, 1.43 to 14.11; P = 0.010) and an older age (OR, 1.02; 95% CI, 1.01 to 1.02; P = 0.001) as being significantly associated with greater odds of intestinal dehiscence, regardless of surgical procedure. The value for the area under the receiver operating characteristic curve (0.82) of this model indicated very good discrimination.

Table 2

Multivariable model evaluating the association of surgical technique with intestinal dehiscence while controlling for identified confounding factors in 211 dogs undergoing 227 surgeries for intestinal foreign body removal in the present study.

Variables OR 95% CI P value* Robust SE
IRA (vs enterotomy) 6.09 1.89–19.58 0.002 3.63
ASA score > 3 4.49 1.43–14.11 0.010 2.62
Increasing age (mo) 1.02 1.01–1.02 0.001 0.01
Presence of linear foreign body 1.76 0.56–5.56 0.335 1.03
Presence of intestinal perforation 0.73 0.13–4.10 0.722 0.64
Surgery performed by a first-year resident 0.78 0.21–2.83 0.705 0.51

Values of P < 0.05 are considered significant.

Association of nasogastric tube placement with patient outcome variables

There were no significant differences between dogs with or without a nasogastric tube and postoperative intestinal dehiscence rates (P = 0.644) or time until first voluntary postoperative intake of food (P = 0.519). However, a longer time (hours) until voluntary postoperative food intake was significantly (P < 0.001) associated with higher odds (OR, 1.03; 95% CI, 1.01 to 1.05) of developing intestinal dehiscence. Patients that underwent nasogastric tube placement with intent for EEN did have a significantly (P < 0.001) shorter duration of hospitalization (median, 67.3 hours; IQR, 52.5 to 89.1 hours), compared with patients that did not undergo nasogastric tube placement (median, 85.6 hours; IQR, 67.6 to 102.1 hours).

Evaluation of patient variables at baseline (ie, age, body weight, serum albumin concentration, ASA score, hypotension, lowest intraoperative body temperature, serum total solids concentration, and sex) and surgery variables (ie, IRA performed, linear foreign body, intestinal perforation, year of surgery, procedure time, and anesthetic time) revealed that patients that underwent surgery in the later years (ie, 2015 and 2016) and patients with linear foreign bodies were significantly (P < 0.001 and P = 0.026, respectively) more likely to undergo nasogastric tube placement. Multiple linear regression with logarithmic transformations to control for normality demonstrated that the association between nasogastric tube placement and total hospitalization time was lost while controlling for both the year of surgery and the presence of a linear foreign body (P = 0.718).

Discussion

The primary purpose of this retrospective cohort study was to quantify the association between surgical procedure and intestinal dehiscence. The overall intestinal dehiscence rate was 6.6%, which is similar to previous reports of patients presenting primarily for intestinal foreign body obstruction.10 While attempting to control for confounding variables between procedure types in a homogenous population, patients undergoing IRA for intestinal foreign body obstruction were at significantly higher odds of developing postoperative intestinal dehiscence, compared with patients undergoing enterotomy for intestinal foreign body obstruction. Although the choice to perform an IRA must be dictated by assessment of intestinal viability, it is important to emphasize the need for meticulous surgical technique to minimize the effect of procedure itself on surgical outcome. Although additional methods for evaluation of intestinal viability, such as trans-serosal pulse oximetry, electromyography, Doppler ultrasonography, or IV administration of fluorescein dye, could be considered to justify performing an enterotomy over an IRA to mitigate the effect of surgical procedure, these modalities are not regularly used in routine practice and are not free of false-negative and false-positive results.26,27,28 However, the incorporation of these modalities could potentially reduce the negative impact of IRA by ensuring the complete removal of unhealthy intestine beyond that of visual and tactile inspection. Overall, the increased risk of dehiscence following IRA may help guide owner expectation following surgery.

While evaluating the association of surgical procedure in the multivariable model, an ASA score > 3 was retained as a significant factor associated with intestinal dehiscence secondary to foreign body obstruction. This is in support of a previous study5 in dogs documenting an increased risk of dehiscence in patients with an ASA score ≥ 3 for general intestinal surgery. An ASA score is a physical health status assessment independent of the surgical procedure to be performed, considering the overall systemic status of the patient.24 In humans, the ASA score has been demonstrated to be a predictor for both survival and complication rates in patients undergoing radical cystectomy for urothelial cancer29 as well as a predictor for the development of wound infection.30 Similar findings of increased risk of wound infection associated with ASA score have been described for dogs and cats.31 In addition, delayed wound healing was noted to be associated with ASA score in human patients undergoing plastic and reconstructive surgery or laparotomy.32,33 Although not a biochemical parameter, a higher ASA score may indicate that a patient is more likely to have systemic changes that may negatively affect healing capability. Although identification and evaluation of individual variables associated with intestinal healing, such as serum albumin concentration, may be more specific as markers of healing capabilities, the results of these previous studies support the use of ASA score as a controlling variable of healing capability in our multivariable model. In addition, this data set provides additional support for the use of ASA score as an associated factor for intestinal dehiscence.

Age also remained significantly associated with dehiscence in the multivariable model for surgical procedure in the present study. For each year increase in age, the odds of dehiscence increased by 1.24. In human medicine, aging has been documented to both impair and alter the wound-healing process of skin.34,35 Changes in the inflammatory, proliferative (fibroplasia and angiogenesis), and maturation phases associated with aging are likely present within the small animal patient as well and may affect intestinal healing. Further research is likely required in this area to evaluate the effects of aging on intestinal healing in dogs.

When the second objective of the present study was evaluated, patients that were targeted to receive EEN were found to have shorter hospitalization times. However, this association was lost when controlling for year. Therefore, the results of this study cannot definitively state that patients targeted for EEN have a shorter hospitalization duration. During the study period, there was a substantial shift in 2015 toward more routine placement of nasogastric tubes following gastrointestinal surgery at our institution. It is also possible that a shift was made at this time to favor earlier patient hospital discharge. Although not randomized, selection bias was less likely to occur in the present study than in previous reports because of a hospital-wide policy change.

In the veterinary literature, one study22 demonstrated a reduction in total time of hospitalization for patients with septic peritonitis when provided EEN. A second study23 found no differences in total time of hospitalization between patients undergoing early, late, or no enteral nutrition. Although an association between EEN and total time of hospitalization was lost in this study while controlling for year, this does not negate a potential effect that EEN may have on total time of hospitalization as a result of the lack of randomization and variable control. Given data in human medicine, previous veterinary literature,22 and the univariable analysis in the present study, a randomized prospective controlled trial for patients undergoing intestinal surgery is warranted with standardized hospital discharge criteria to definitively determine the effect of EEN on duration of hospitalization.

In addition to impacts on hospitalization duration, several interesting relationships have been explored when evaluating the impact of EEN on postoperative outcomes. Previously, several benefits of EEN on intestinal healing, including increased bursting pressure, improved collagen content, and increased perfusion, have been identified.16 In addition, EEN ameliorates the systemic inflammatory response and reduces the risk of bacterial translocation.17 Despite these benefits, a systematic review of human medicine found that the administration of EEN through a nasogastric tube did not have a protective effect on intestinal dehiscence.20 This is in agreement with our findings in the present study. However, this is inconsistent with a previous study8 in veterinary medicine that documented a higher dehiscence rate in patients that were targeted for supplemental alimentation. It is likely that in the aforementioned study,8 sicker patients were targeted for EEN. This may account for the differences in outcome. Further research on the effect of EEN and intestinal dehiscence is warranted. However, on the basis of the dehiscence rates in the present study, power analysis (α = 0.05 and β = 0.8) indicates each treatment arm would require > 4,100 surgical events to definitively evaluate this relationship.

Although the present study did not identify a positive association between nasogastric tube placement with intent for EEN and intestinal dehiscence rates, it did find that an early return to voluntary food intake was associated with a decreased dehiscence rate. This is consistent with a previous study23 that examined 56 dogs and found that dogs that ate voluntarily or were provided enteral nutrition were more likely to survive to hospital discharge than those that did not receive nutrition. Retrospectively, it is difficult to determine whether the association that we found was the result of improvement in the clinical status of the patient leading to improved appetite or whether early appetite improved clinical healing. Further evaluation of the effects of enteral nutrition on outcome variables through prospective randomized controlled trials is warranted.

There were several important limitations in the present study. The study was retrospective in nature, which has inherent limitations in the accuracy and completion of data collection and validity. Although data were collected on whether patients received a nasogastric tube or not, the consistency, duration, and reliability of caloric administration were not evaluated, and an assumption was that all patients received EEN according to a standardized protocol. In addition, a substantial proportion of patients did not have serum albumin concentrations available for analysis, precluding its use within the multivariable model. Albumin concentration is a well-documented prognostic indicator,9,12 and inclusion within the multivariable model would have been useful for further refining the association of surgical procedure with intestinal dehiscence. A randomized clinical trial assessing patient outcome following enterotomy versus IRA for the treatment of intestinal foreign bodies would be preferable to a retrospective analysis. However, randomizing patients to undergo either enterotomy or IRA would be unethical given the different indications for each procedure. Another major limitation to the present study was the selection bias introduced by the inclusion of dogs with follow-up limited to 5 days, as intestinal dehiscence has been documented to occur as late as 11 days.2 However, most often, intestinal dehiscence occurs from 72 to 96 hours in association with the lag phase of wound healing,1 and this fact is consistent with a recent report4 that indicated a mean of 3 days occured until dehiscence for hand-sutured intestinal anastomosis. Finally, in an effort to limit the effect of selection bias, information on surgeries was included only if the patient was doing clinically well at the time of documented follow-up.

Overall, patients undergoing IRA were at a significantly higher risk of intestinal dehiscence, compared with patients undergoing enterotomy, for foreign body removal, while confounding variables were controlled for. These findings should not be used to select a procedure. Instead, these findings may serve to inform both owners and surgeons of the impact of procedure on risk of intestinal dehiscence.

Acknowledgments

No external funding was used in this study. The authors declare that there were no conflicts of interest.

The authors thank Dr. Galina Hayes and Stephen Parry of the Cornell University Statistical Consulting Unit for their assistance on the statistical analysis.

Abbreviations

ASA

American Society of Anesthesiologists

EEN

Early enteral nutrition

IQR

Interquartile (25th to 75th percentile) range

IRA

Intestinal resection and anastomosis

Footnotes

a.

Nasogastric Tube, Mila International, Florence, Ky.

b.

Clinicare, Abbott Animal Health, Abbott Park, Ill.

c.

STATA, version 15.1, StataCorp LLC, College Station, Tex.

References

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