Postoperative colic is commonly recognized after abdominal surgery in horses,1–3 and more recently, the incidence of colic following nonabdominal surgeries and general anesthesia without surgery has been reported.4–9 The authors are unaware of any studies reporting the incidence and risk factors for colic in horses hospitalized for ocular disease or undergoing ocular surgery. This information would help clinicians educate their clients, identify horses at risk of developing colic, and therefore implement appropriate preventative measures.
Horses requiring hospitalization and treatment of ocular disease are likely to be exposed to many risk factors for colic that have been previously reported. These include changes in management, exercise, diet, stabling, and recent transport.8,10–12 It is likely that ocular pain may further exacerbate the risk of colic by causing sympathetic stimulation, thereby decreasing gastrointestinal motility.13 Horses with ocular disease commonly require prolonged treatment and often receive medications such as sedatives, NSAIDs, and topical application of atropine, all of which have been associated with changes in gastrointestinal motility or colic.4,14–19 Additionally, horses hospitalized for ocular disease may undergo general anesthesia, which is known to alter gastrointestinal myoelectrical activity.20,21 Together, these factors may predispose horses hospitalized with ocular disease to colic.
The objectives of the study reported here were to examine the incidence of colic in equids hospitalized for the treatment of ocular disease and to identify risk factors associated with colic in this population. Based on the factors already noted and clinical impression, the hypotheses were that equids hospitalized for ocular disease would have a higher incidence of colic than previously reported for those not hospitalized and that risk factors for colic would include the use of topically applied ophthalmic atropine, ocular surgery, and a longer duration of hospitalization.
Materials and Methods
A search of hospital records was performed to identify all equids that were admitted to the University of Georgia Veterinary Teaching Hospital for the treatment of ocular disease between January 1, 1997, and December 31, 2008. All equids hospitalized for > 24 hours for treatment of ocular disease were considered eligible for inclusion in the study; equids treated on an outpatient basis were excluded. Information from the first admission only was used for analysis in equids that were admitted on more than 1 occasion.
Medical records of equids fitting these inclusion criteria were evaluated. The signalment of each equid and information regarding the ocular disease, including the duration of clinical signs prior to admission, duration of hospitalization, and the diagnosis (keratitis, uveitis, eyelid disease, lens disease, glaucoma, or other), was recorded. In addition, treatment methods such as the use of a subpalebral lavage system, topically applied ophthalmic atropine, systemic administration of NSAIDs, and types of surgery with or without the use of neuromuscular blocking agents were also recorded. Ocular surgical interventions were further grouped into globe surgery, such as conjunctival grafting or enucleation, and adnexal surgery.
The medical records were also examined for any reports of equids with signs of colic during hospitalization defined as pawing, flank watching, having a flehmen response in the presence or absence of recumbency, or rolling. Equids with colic were grouped as those with signs of mild pain (intermittent pawing, flank watching, and flehmen response), moderate pain (increased intensity of mild pain signs and additional intermittent periods of recumbency), and severe pain (increased intensity of moderate pain signs but with frequent recumbency and rolling). All equids with colic were further grouped depending on the lesion location (stomach, small intestine, cecum, large intestine, or small colon) and type of lesion (inflammatory, nonstrangulating, strangulating, or nonspecific).
The medical records were also used to establish whether equids with signs of colic were treated medically or surgically or were euthanatized. Equids were then grouped as those that survived to discharge from the clinic and those that did not survive to discharge because of death or euthanasia (on humane grounds or because of a poor to grave prognosis or financial constraints).
Statistical analysis—An exact test of independence was used to evaluate the univariable associations between categorical predictor variables and the probability of developing colic. Logistic regression was used for the multivariable analysis, with the occurrence of colic being considered a dichotomous outcome. Multivariable model selection was performed following a maximum main-effects model that included all predictor variables that were associated with colic (P < 0.2) in the univariable analysis. Variables were removed from the multivariable model in a stepwise fashion on the basis of their level of significance until only those with a value of P < 0.1 remained. After reaching a preliminary main-effects model, the significance of all previously excluded variables was reevaluated by adding each one back to the model, and all possible 2-way interactions between significant main-effects were considered. The most appropriate form of continuous predictor variables was determined by comparing Akaike information criterion for models that incorporated linear, quadratic, and categorized versions of the variables. The form of the predictor variable that yielded the lowest Akaike information criterion was preferred. Continuous variables included in their quadratic form were first centered by subtracting the population mean to reduce collinearity between the linear and squared terms. Data were screened for outliers by examining plots of the predicted probabilities versus Δ χ2, Δ deviance, and Δ beta statistics. Goodness of fit for the final model was evaluated by means of the Hosmer-Lemeshow goodness-of-fit test.22 All testing assumed a 2-sided alternative hypothesis, and P < 0.05 was considered statistically significant. Analyses were performed with commercially available statistical software.a
Results
The search identified 337 equids that were eligible for inclusion in the study. Twenty-three equids were admitted more than 1 time for the treatment of ocular disease during the study period.
Equids included in the study ranged from 1 month to 34 years old, with a mean ± SD age of 11.0 ± 7.6 years. Hospitalization times ranged from 1 to 84 days, with a mean ± SD of 9.9 ± 8.9 days. The frequency distribution of breeds in the study population was as follows: American Quarter Horse, 105 (31.2%); Thoroughbred, 66 (19.6%); Paint Horse, 32 (9.5%); warmblood, 26 (7.7%); Appaloosa, 20 (5.9%); pony, 19 (5.6%); Arabian, 18 (5.3%); Tennessee Walking Horse, 10 (3.0%); American Saddlebred, 8 (2.4%); draft horse, 8 (2.4%); Morgan, 7 (2.1%); mixed, 6 (1.8%); Friesian, 2 (0.6%); National Show Horse, 2 (0.6%); Paso Fino, 2 (0.6%); Spotted Saddle Horse, 2 (0.6%); donkey, 1 (0.3%); Lippizaner, 1 (0.3%); Racking Horse, 1 (0.3%); and unknown breed, 1 (0.3%). Additional data retrieved from the medical records were summarized (Table 1). Three (0.9%) equids hospitalized for ocular disease were administered neuromuscular blocking agents while under general anesthesia for ocular surgery, All equids received systemic administration of NSAIDs at various time points during hospitalization.
Univariable analysis of potential risk factors for colic in equids (n = 337) hospitalized for the treatment of ocular disease between January 1997 and December 2008; equids with missing information were excluded from statistical comparisons.
| Variable | Total No. of equids | No. of equids with colic (%) | P value* |
|---|---|---|---|
| Age category (y) | 0.020 | ||
| 0–1 | 50 | 13 (26.0) | |
| 2–20 | 248 | 45 (18.2) | |
| ≥ 21 | 37 | 14 (37.8) | |
| Sex | 0.893 | ||
| Female | 133 | 29 (21.8) | |
| Male | 203 | 43 (21.2) | |
| Breed | 0.846 | ||
| Quarter Horse | 105 | 21 (20.0) | |
| Thoroughbred | 66 | 16 (24.2) | |
| Other | 165 | 35 (21.2) | |
| Ocular disease | 0.258 | ||
| Keratitis | 235 | 51 (21.7) | |
| Uveitis | 47 | 13 (27.7) | |
| Other | 55 | 8 (14.6) | |
| Duration of ocular disease (d) | 0.193 | ||
| 0–30 | 249 | 53 (21.3) | |
| 31–365 | 38 | 5 (13.2) | |
| ≥ 366 | 44 | 13 (29.6) | |
| Hospitalization time (d) | < 0.001 | ||
| 1–4 | 89 | 4 (4.5) | |
| 5–7 | 77 | 12 (15.6) | |
| ≥8 | 162 | 54 (33.3) | |
| Subpalpebral lavage system | 0.228 | ||
| No | 193 | 37 (19.2) | |
| Yes | 141 | 35 (24.8) | |
| Atropine | 0.016 | ||
| No | 110 | 15 (13.6) | |
| Yes | 226 | 57 (25.2) | |
| Eye surgery | 0.895 | ||
| No | 152 | 33 (21.7) | |
| Yes | 185 | 39 (21.1) |
Exact test of independence.
Details of colic cases—Colic was diagnosed in 72 of 337 (21.4%) equids while they were hospitalized for the treatment of ocular disease. Clinical signs of colic were graded as mild for 43 (59.7%) equids, moderate for 21 (29.2%), and severe for 8 (11.1%). The type of colic was classified as nonstrangulating for 30 (41.7%) equids, inflammatory for 20 (27.8%; comprising 19 equids with colitis and 1 with anterior enteritis), nonspecific for 20 (27.8%), and strangulating for 2 (2.8%; comprising 1 equid with large intestine volvulus and 1 with small intestinal volvulus). The anatomic location of the problem was identified as the large intestine for 32 (44.4%) equids, nonspecific for 20 (27.8%), cecum for 10 (13.9%), small intestine for 4 (5.6%), stomach for 4 (5.6%), and small colon for 2 (2.8%). Sixty-three (87.5%) equids with colic received a combination of the following medical treatments for the colic episode: enteral administration of mineral oil and balanced isotonic electrolyte solution via a nasogastric tube, systemic administration of NSAIDs, IV fluid therapy, antispasmodic medications, or gastroprotectants.
Nine (12.5%) equids underwent abdominal surgery that was recommended for the persistence or recurrence of colic signs despite analgesia. Of these equids, 1 had a nonstrangulating lesion of the stomach (gastric impaction), 2 had nonstrangulating lesions of the small intestine, 1 had a strangulating lesion of the small intestine, 2 had nonstrangulating lesions of the large intestine, 1 had a strangulating lesion of the large intestine, and 2 had nonstrangulating lesions of the cecum. Of the 10 equids with cecal impactions, colic that was due to cecal disease was resolved surgically in 2 equids (by performing a typhlotomy to drain and lavage the cecum) and medically in 7 equids. One equid treated medically was euthanatized because of clinical evidence of a ruptured viscus subsequently confirmed as the cecum on necropsy. Surgical intervention had been offered for this equid; however, it was declined by the owner because of financial constraints. Ultimately, 67 equids with colic survived to discharge and 5 died or were euthanatized.
Analysis of risk factors for colic—Results from the univariable analysis of colic risk factors were summarized (Table 1). Age, hospitalization time, and the topical use of atropine were all significantly associated with colic in the univariable analysis. Compared with equids between 2 and 20 years of age, the probability of developing colic was higher for both younger (0- to 1-year-old) and older (≥ 21-year-old) equids. Likewise, the risk of colic increased as equids spent a longer time in the hospital and was higher for equids that were treated with topical application of ophthalmic atropine than for equids that were not treated. None of the other potential risk factors were significantly associated with the likelihood of developing colic.
The results of the multivariable analysis were summarized (Table 2). Only hospitalization time and age were significantly associated with colic in the multivariable analysis. The odds of developing colic were 3.7 times as great for equids that were hospitalized for 5 to 7 days as for equids that were hospitalized for 1 to 4 days, after adjusting for age. Similarly, the odds of developing colic were 11 times as great for equids that were hospitalized for 8 days or more as for equids that were hospitalized for 1 to 4 days, after adjusting for age. Subdividing the upper category of hospitalization time into categories of 8 to 14 days and 15 days did not improve model fit, and the coefficients for these 2 categories differed by < 10% (model not shown). Consequently, there was not a meaningful increase in the risk of colic for equids that had been hospitalized for more than 2 weeks, compared with the risk for equids that had been hospitalized for a period of 8 to 14 days.
Multivariable logistic regression model for the prediction of colic in equids (n = 326) hospitalized for the treatment of ocular disease between January 1997 and December 2008.
| Variable | Coefficient (SE) | OR (95% CI) | P value |
|---|---|---|---|
| Age* | 0.014 (0.019) | NC | 0.456 |
| (Age*)2 | 0.006 (0.002) | NC | 0.012 |
| Hospitalization time (d) | < 0.001 | ||
| 1–4 | Referent | Referent | |
| 5–7 | 1.311 (0.607) | 3.7 (1.1–12) | |
| ≥ 8 | 2.380 (0.544) | 11 (3.7–31) | |
| Constant | –3.401 (0.535) | NA | < 0.001 |
Mean centered age (ie, age in years minus 11.0).
CI = Confidence interval. Constant = Intercept term. NA = Not applicable. NC = Not calculated because age was included as a quadratic predictor.
The association between age and colic was nonlinear, and the best model fit was achieved by including age as a quadratic predictor. As in the univariable analysis, the probability of colic was higher for young and old equids than it was for those in the middle of the age distribution. For example, compared with an 11-year-old equid with ocular disease, a 6-month-old foal with ocular disease was 1.6 times as likely to develop colic, and a 25-year-old equid with ocular disease was 3.7 times as likely to develop colic, after adjusting for the duration of hospitalization. The effect of age was also illustrated (Figure 1) by plotting the predicted probabilities of developing colic for equids of different ages and hospitalization times on the basis of the final multivariable logistic regression model. Results of the Hosmer-Lemeshow test indicated that the final multivariable model provided a good fit to the data (χ2 = 4.55; 8 degrees of freedom; P = 0.80).
Predicted probability of developing colic by age and hospitalization time in 337 equids hospitalized for the treatment of ocular disease between January 1997 and December 2008.
Citation: Journal of the American Veterinary Medical Association 240, 12; 10.2460/javma.240.12.1488
Predicted probability of developing colic by age and hospitalization time in 337 equids hospitalized for the treatment of ocular disease between January 1997 and December 2008.
Citation: Journal of the American Veterinary Medical Association 240, 12; 10.2460/javma.240.12.1488
Predicted probability of developing colic by age and hospitalization time in 337 equids hospitalized for the treatment of ocular disease between January 1997 and December 2008.
Citation: Journal of the American Veterinary Medical Association 240, 12; 10.2460/javma.240.12.1488
Although topical application of atropine was associated with colic in the univariable analysis, it was not a significant (P = 0.52) predictor after adjusting for the effects of age and hospitalization time in the multivariable analysis (OR, 1.27; 95% confidence interval, 0.61 to 2.7 [model not shown]).
Discussion
The 21.4% incidence of colic signs in this population of equids hospitalized for ocular disease is high. The colic incidence density in primary care private practice has been reported as 10.6 colic cases/100 horse-years.11 In hospitalized horses undergoing anesthesia for nonabdominal surgical procedures, the incidence of colic ranges from 2.8% to 8.8%.5–7,9,23 Of horses undergoing anesthesia for nonsurgical procedures (eg, MRI), 1.5% had signs of postanesthetic colic.9 To the authors' knowledge, there is no study that has reported on the incidence of colic in equids hospitalized for ocular disease, making it impossible to compare this high incidence with other private practices and institutions. The incidence of colic in equids hospitalized for other conditions in this hospital is not available but is subjectively far lower than for equids hospitalized with ocular disease. The high incidence of colic for equids hospitalized with ocular disease does support our clinical impression and hypothesis that this group is at risk for developing colic signs when compared with reports of horses not hospitalized and those hospitalized for other conditions. However, this high incidence may be biased because our clinical impression may increase the intensity of monitoring in equids considered at risk. It is noteworthy that 59.7% of equids had, at worst, mild clinical signs of colic, which may have been overlooked in equids not considered at risk of colic or in horses not monitored continuously.
There are many potential risk factors that have previously been reported for colic in horses, including changes in management.8,10–12,24 These changes in management include increased concentrate intake,12 recent change in diet (especially within the preceding 2 weeks),10,24 withholding of food for 18 hours by use of muzzles,25 recent transport (especially as a cause of colonic obstruction and distension colic),8 stabling for 24 h/d (especially within 14 days after a housing change),8 change in weather (especially within 3 days after a weather change),10 crib biting and windsucking,8 a recent change in housing,10,26 a recent change in exercise (especially 1 week after the change; however, this may be linked with housing or feeding changes),8,10,27 decreased fecal output,4 and previous signs of colic.8,10–12,28 Many of the noted risk factors for colic in horses could contribute to the high incidence of colic in equids in the present study. All hospitalized equids underwent changes in management, including changes in stabling, exercise, feeding, and transportation.
Anesthesia itself alters myoelectrical activity of the intestine regardless of the anesthetic method used,21 and horses that undergo surgical intervention during anesthesia have a higher risk of colic than do horses anesthetized for nonsurgical procedures.9 Many of the equids in the present study (54%) underwent anesthesia and surgery for treatment of ocular disease; however, this was not found to be a factor significantly associated with colic in this group, regardless of the nature of the ocular surgery (globe or adnexal and enucleation).
The administration of certain medications has also been noted to alter myoelectric activity and contractility of the gastrointestinal tract. Systemic administration of NSAIDs has been shown to decrease the motility of the large intestine in vitro,17 and sympathomimetic drugs (α2-adrenoreceptor agonists) are known to decrease gastrointestinal motility.16,29 Although controversial, some studies5,9 have reported a higher incidence of postoperative colic in horses receiving opioids during anesthesia, compared with results of a study7 in which the drugs were not used. Finally, because of potent inhibition of intestinal motility,15,30 topical administration of atropine has been identified as a risk factor for colic14,19 and, specifically, reduced postoperative fecal output.4
All equids in the present study had received systemic administration of NSAIDs during hospitalization. These medications are known to have an inhibitory effect on gastrointestinal motility in vitro,17,18 and their use may have contributed to the high incidence of colic in our study. Unfortunately, NSAID administration could not be assessed as a risk factor for colic in the present study because all equids received this medication. Furthermore, despite the deleterious effects on the gastrointestinal tract, NSAID administration is important to decrease ocular pain in horses.31 As is reported for humans, the combination of pain, increased sympathetic tone, and increased endogenous catecholamines also decreases gastrointestinal motility.13 Managing pain and the associated stress response with NSAIDs is therefore essential despite potential adverse effects of these medications. Their use is also supported by a study4 in which the administration of phenylbutazone was shown to help maintain adequate fecal output after anesthesia and orthopedic surgery.
All equids in the present study were treated with various amounts of sedatives (ie, α2-adrenoreceptor agonists with or without opioids) to facilitate ocular examination during hospitalization. Despite the careful review of the medical records, sedation type, frequency, and dose for analysis could not be accurately assessed; however, it is possible that the repeated use of sedation may have contributed to the high incidence of colic in the present study. It may be beneficial to conduct prospective studies in which a more accurate record of sedation frequency, dose, and type are recorded. Feed is often withheld from horses requiring sedation to prevent complications such as esophageal obstruction. These irregularities in feeding practices may have also contributed to the high incidence of colic seen in equids in the present study because withholding food has previously been noted as a risk factor for colic.25 In the present study, although topical administration of atropine was associated with colic in the univariable analysis, it was not a significant predictor after adjusting for age and duration of hospitalization in the multivariable model. The point estimate for atropine use in the multivariable analysis did suggest that it was associated with an increase in the odds of developing colic, but this was not significant (P = 0.52). There is some individual susceptibility to the gastrointestinal effects of atropine, and the effects are dose dependent.32,33 Dosage and frequency of administration of atropine were not evaluated in the present study, although higher doses of atropine are likely to have a more deleterious effect on gastrointestinal motility than are low doses, and this may be worthy of further, more targeted clinical investigations. It should be noted that topical administration of 1% ophthalmic atropine according to most authors' recommendations (0.1 to 0.2 mL or 2 to 4 drops, q 4 to 24 h) equates to 2 to 16 mg/d. In a 450-kg (990-lb) horse, this is equivalent to 0.004 to 0.036 mg/kg/d (0.0018 to 0.016 mg/lb/d). At the upper dose range, if all atropine doses were systemically absorbed, intestinal stasis and abdominal pain could result; however, most horses in 1 study19 receiving atropine IV at 0.044 mg/kg (0.02 mg/lb) did not develop colic signs. In the present study, the lack of a significant effect of topical administration of atropine in the multivariable analysis suggests that judicious administration of atropine did not significantly increase the risk of colic in equids hospitalized for ocular disease.
The incidence of equids with colic that had cecal impactions (10/72 [13.9%]) was higher than that previously reported in horses admitted to referral centers because of signs of colic (up to 4.1%).34 Reported predispositions for cecal impactions include administration of NSAIDs, poor dentition, coarse roughage, changes in feed, decreased exercise, decreased water intake, and the presence of Anoplocephola perfoliata.35–41 Cecal impaction has also been found more frequently in horses treated for musculoskeletal abnormalities35 and after a previous exploratory celiotomy42 and is usually secondary to chronic pain.36 Cecal tympany has also been associated with the clinical and experimental administration of atropine.19 In the present study, 85% of all equids that were hospitalized for > 1 week were treated with atropine, and 80% of the cecal impactions were observed in equids that were hospitalized for > 1 week. The association between orthopedic pain and cecal impaction is well established, but results of the present study suggested that equids hospitalized with ocular disease have a higher incidence of cecal impaction than the general population. Clinicians should be aware of the potential risk for cecal impaction when managing equids with ocular disease because of the high mortality rate that has been reported for horses with cecal impaction.34,35,43,44
Identified risk factors for colic in equids hospitalized for ocular disease in the present study were age and duration of hospitalization. An increased risk of colic in older horses has already been reported.10,28,45 Older horses are also more likely to need surgical management of colic than younger horses.46 The authors of these studies10,28,45 hypothesized that this is because older horses have more opportunity to develop disease or be exposed to causal factors. Contrary to these findings, other studies have reported that horses > 10 years old are at a lower risk of developing colic than are those between 2 and 10 years old.47 A study11 on younger horses noted that horses 2 to 10 years of age had an increased risk of colic over those in the 0- to 2-year age bracket; yet a countrywide survey48 of all equids in the United States found a lower incidence of colic in equids < 6 months in age, compared with all other age categories. Finally, in a study26 comparing ages of horses that had signs of colic in primary care practice with control horses, no difference was noted. In the present study, the probability of developing colic concurrent with ocular disease was higher for equids 0 to 1 year old and ≥ 21 years old, compared with equids 2 to 20 years old. Younger and older equids may be unable to adapt to the management changes implemented to address ocular disease, and further investigations may be needed to establish methods of preventing colic in these at-risk age groups.
The association between increased duration of hospitalization for ≥ 8 days and increased risk of colic supports our hypothesis; however, the reason for this is unknown. It may be associated with the severity of the ocular disease (because equids with more severe ocular disease are likely to be hospitalized for longer periods), a more prolonged change in management, or an increased administration of medications over a longer duration of time, or it may simply be the result of having more time at risk for being recognized as a case. The retrospective nature of the present study prevented assessment of an ocular pain score, which may be useful to assess the effect of the severity of ocular pain on incidence of colic in future prospective studies.
In conclusion, the present study showed that equids hospitalized for ocular disease have a higher incidence of colic (21.4%), compared with the incidence of colic previously reported in horses not hospitalized or undergoing hospitalization and general anesthesia for other reasons. The identified risk factors for colic included the age of the horse (0 to 1 year and ≥ 21 years old) and an increased length of hospitalization (≥ 8 days). Findings in the present study may assist clinicians who treat equids with ocular disease to identify potential risk factors for the development of colic, which may lead to the implementation of aggressive prophylactic measures. Finally, it would be valuable to collect similar information from other institutions and implement prospective studies aimed at enhancing our ability to decrease the incidence of colic in equids hospitalized for ocular disease.
Stata, version 11.1, StataCorp LP, College Station, Tex.
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