Surgical treatment for acute small intestinal obstruction caused by Parascaris equorum infection in 15 horses (2002–2011)
Reasons for performing study: There is a consensus in the veterinary literature that Parascaris equorum (ascarid) impaction carries a poor prognosis. Hence surgery is often delayed and foals are often subjected to euthanasia after diagnosis of ascarid impaction is established. Our clinical impression was that ascarid impaction carries a better prognosis than previously reported.
Objectives: Our expectation was that manually evacuating the impaction into the caecum, thus refraining from opening the small intestine, would improve the prognosis for survival of horses with ascarid impaction. The aim of this study was to examine medical records of horses treated surgically for ascarid impaction, record their clinical findings and evaluate the association of outcome with the method of relieving the impaction.
Methods: The medical records of all horses presented to our hospital between October 2002 and December 2011 that underwent exploratory celiotomy for ascarid impaction were reviewed. Information retrieved from the medical record included surgical findings, surgical technique, complications, short- and long-term survival. The association between categorical variables was assessed using the Fisher's exact test. A P value <0.05 was considered statistically significant.
Results: Fifteen horses fulfilled the inclusion criteria. Eighty percent of horses (12/15) survived to discharge and 60% (6/10) survived for at least one year. Five horses are doing well but are still in convalescence. Horses that underwent small intestinal enterotomy or resection and anastomosis (n = 5) were less likely to survive to discharge (P = 0.022).
Conclusions: In our study, manual evacuation of ascarid impaction into the caecum, while refraining from opening the small intestine resulted in significantly improved survival in horses with ascarid impaction.
Potential relevance: Refraining from opening the small intestine may be the key to improving surgical outcome in horses with ascarid impaction.
Infection with Parascaris equorum (ascarid) is a common disease among horses less than 1-year-old, with a reported prevalence around 30% . Due to emerging resistance of P. equorum to commonly used anthelmintics the prevalence of the disease is likely to increase . Clinical signs may include lethargy, anorexia, decreased weight gain, hypoproteinaemia, coughing, nasal discharge and colic . The colic signs result from acute small intestinal obstruction caused by a large burden of the parasite. In most cases the colic is associated with recent administration of anthelmintic medication  and is also often associated with stressful conditions such as weaning and transportation. Horses with impaction of the small intestine caused by P. equorum commonly suffer from secondary intestinal abnormalities caused by luminal obstruction, including small intestinal volvulus or intussusception .
Surgical treatment for ascarid impaction has a high incidence of complications including septic peritonitis; intestinal rupture; focal, necrotising enteritis and intestinal adhesions, which lead to rates of mortality that range from 73 to 92% [4,5]. In a study of 12 horses suffering from small intestinal obstruction caused by ascarids, the only surviving foal was the one in which small intestinal enterotomy was not performed . Based on this information and our clinical experience we hypothesised that manually evacuating the impaction into the caecum, thus avoiding small intestinal enterotomy or small intestinal resection and anastomosis, would substantially improve the prognosis for survival of horses with small intestinal obstruction caused by P. equorum. The aim of this study was to examine the medical records of all horses treated surgically at our hospital for impaction of the small intestine by ascarids to determine their clinical findings and to evaluate the association between the outcome and the method of relieving the impaction.
Material and methods
The medical records for all horses presented to our referral hospital between October 2002 and December 2011 that underwent exploratory celiotomy for impaction of the small intestine with ascarids were reviewed. Information retrieved from the medical records included age, gender, breed, duration of colic prior to admission, vital signs upon presentation, mucous membrane, volume of gastric reflux, selected blood test results (e.g. packed cell volume, total solids, white blood cells count, urea and lactate), season of the year when the horse was admitted, history of administration of anthelmintic medication, surgical findings, surgical technique, duration of hospitalisation, short- and long-term complications, short- and long-term survival and cause of death.
Season was defined as follows: autumn (September to November), winter (December to February), spring (March to May) and summer (June to August). A diagnosis of ascarid impaction was based on history and typical clinical signs and confirmed at surgery.
The impaction was resolved using one of the following surgical techniques: 1) manually milking the small intestinal content into the caecum using a liberal amount of 1% SCMC (Sodium-carboxy-methyl-cellulose) applied topically as a lubricant; 2) similar technique combined with typhlotomy; 3) small intestinal enterotomy and 4) resection and anastomosis of the impacted segment. Anastomosis was performed using a single layer full thickness simple interrupted pattern with a monofilament synthetic absorbable suture material. Closure of enterotomies of the small intestine and caecum were achieved by suturing the wall of the intestine in 2 layers with a monofilament synthetic absorbable suture material. The first layer was a full thickness simple continuous pattern and the second layer was a continuous, Cushing pattern. Pelvic flexure enterotomy was performed in some horses and was closed in a similar fashion. Omentectomy was performed, in some horses by dividing the greater omentum to several segments and ligating each segment with a double transfixation ligation.
The final outcome was defined as death during hospitalisation, survival to discharge (short-term survival, STS) or survival for at least one year after surgery (long-term survival, LTS). Long-term follow-up was obtained by telephone interview of the owners.
Normality of distribution was assessed using the Shapiro Wilk test. Continuous variables (e.g. length of hospitalisation) were compared between the groups using the Mann–Whitney U test. The association between categorical variables (e.g. use of omentectomy vs. not) was assessed using the Chi-square or the Fisher's exact test. A P value <0.05 was considered statistically significant and statistical analysis was performed using a commercial software (SPSS 17 for Windows, Chicago, Illinois)a.
Fifteen horses fulfilled the inclusion criteria and were included in the study (Table 1). Median age was 10 months (range 3 months to 5 years) and median bodyweight was 213 kg (range 120–450 kg). Breeds included Arabians (9) American Quarter Horse (2), Andalusian, American Paint Horse, Friesian and mixed breed (one each).
Table 1. Summary of techniques, findings, complications and results of surgery for 15 horses with ascarid impaction
| 1||18 m||Fall||2002||SI enterotomy||None||Adhesions||Alive||Dead|
| 2||4 m||Summer||2003||SI enterotomy||None||Caecal rupture||Dead||Dead|
| 3||2 y||Fall||2004||SI enterotomy||None||None||Alive||Alive|
| 4||3 m||Summer||2005||R&A||None||Septic peritonitis||Dead||Dead|
| 5||3 m||Fall||2007||R&A||Intus.||Septic peritonitis||Dead||Dead|
| 6||8 m||Fall||2009||Typhlotomy||None||None||Alive||Alive|
| 7||10 m||Spring||2009||None||None||None||Alive||Alive|
| 8||5 y||Summer||2009||None||SIV||None||Alive||Alive|
| 9||10 m||Spring||2009||None||SIV||None||Alive||Alive|
| 10||4 m||Fall||2010||PF enterotomy||None||None||Alive||Alive|
| 11||6 m||Summer||2011||None||None||Inc. hernia||Alive||NA|
| 12||2.5 y||Fall||2011||PF enterotomy||None||None||Alive||NA|
| 13||2.5 y||Fall||2011||None||LCV||None||Alive||NA|
| 14||9 m||Fall||2011||Typhlotomy||SIV||Inc. Infection||Alive||NA|
| 15||6 m||Winter||2011||None||None||Inc. Infection, Phleb.||Alive||NA|
Median time between onset of clinical signs of colic and admission was 8 h (range, 5–36 h). Eighty percent of horses (12/15) received anthelmintic medication within the 24 h prior to onset of clinical signs.
Mucus membranes were discoloured in 11/15 cases, of which 7 were hyperaemic. Nasogastric intubation yielded gastric reflux in 6/15 cases with a median reflux volume on arrival of 2 l (range 0–4 l). Distended loops of small intestine were seen on ultrasonographic examination of the peritoneal cavity in 10/11 cases and in 2 cases the presence of intraluminal worms was recorded.
Surgical findings and management
Additional findings during surgery included: small intestinal volvulus (3 horses), large colon volvulus (180°) and small intestinal intussusception at the impacted region (one horse each). In 8 horses the impaction was resolved by manually milking the content into the caecum using a liberal amount of 1% SCMC as a lubricant; in 2 horses a similar technique was used combined with typhlotomy, in 3 horses small intestinal enterotomy was performed and in 2 horses resection and anastomosis of the impacted segment was performed. Omentectomy was performed in 7 horses and pelvic flexure enterotomy was performed in 2 horses.
Post operative complications
Complications occurred in 6 horses and included caecal rupture, small intestinal adhesions causing colic, jugular thrombophlebitis, incisional hernia, body wall haematoma causing anaemia (one horse each), small intestinal leakage leading to septic peritonitis and incisional infection (2 horses each).
Three horses died while hospitalised, one because of caecal rupture and 2 had septic peritonitis resulting from intestinal leakage at the site of small intestinal anastomosis. The horse with the intussusception was treated by resection and anastomosis and did not survive to discharge. Five of the horses were still in early convalescence (between 3 and 9 months after surgery) at the time of writing and were doing well.
All 4 nonsurvivors underwent either small intestinal enterotomy (2/4) or resection and anastomosis (2/4). All cases in which the impaction was resolved by milking the ascarids from the small intestine into the caecum, without the need to open the intestine, are alive to date. All 3 horses that had small intestinal volvulus were alive at the time of writing (4 months to 3 years after surgery). All horses managed surgically since 2009 were alive at the time of writing (10 cases); neither resection and anastomosis nor enterotomy were performed in any of these horses.
Eighty percent (12/15) of the horses in this study survived to discharge. Horses were more likely to survive to discharge if admitted from 2009 to date when compared with horses who presented prior to 2009 (P = 0.022). Duration of colic prior to referral was not different between horses admitted prior to 2009 (range 5–36 h, median 8 h) and horses admitted after 2009 (range 5–24 h, median 7.5 h) (P = 0.665). Horses surviving to discharge were more likely to be older (range 4–60 months, median 10 months) than nonsurvivors (range 3–4 months, median 3 months) (P = 0.004). Duration of colic prior to referral was not different between survivors to discharge (range 5–36 h, median 8 h) and nonsurvivors (range 5–10 h, median 8 h) (P = 0.61). Horses that suffered from ascarid impactions complicated by small intestinal volvulus or intussusceptions were not less likely to survive to discharge than horses with simple impactions (P = 0.637). Horses that underwent small intestinal enterotomy or resection and anastomosis were less likely to survive to discharge (P = 0.022); while pelvic flexure enterotomy or typhlotomy did not have a significant effect on survival to discharge (P = 1.0). In the short-term the use of omentectomy was not different between survivors and nonsurvivors (P = 0.2); while intraoperative use of SCMC was more prevalent in horses surviving to discharge (P = 0.044).
Sixty percent (6/10) of horses survived long-term. One died 4 months after discharge due to small intestinal adhesions. Only one of the horses (1/5) that had either a small intestinal enterotomy or resection and anastomosis had survived long-term. Use of SCMC had a positive association with long-term survival (P = 0.048). Horses that had omentectomy appeared to have improved long-term survival (4/4, 100%) than horses that did not have omentectomy (2/6, 33%); however, this association was not significant (P = 0.076).
In this study, the survival rate of horses after surgery for small intestinal obstruction caused by P. equorum is markedly higher than previously reported [4,5]. Eighty percent of horses survived to discharge and 60% survived long term. This incidence of long-term survival is clearly different from earlier reports in which only 10 or 27% of horses undergoing surgery for ascarid impaction survived long term [4,5]. Our hypothesis that refraining from creating a small intestinal enterotomy or from resecting the impacted segment of small intestine would improve the prognosis for survival proved to be correct. The short-term survival was significantly worse in horses that underwent small intestinal enterotomy or resection and anastomosis. All horses that died had undergone small intestinal enterotomy or resection and anastomosis. The simple surgical technique of manually evacuating the impaction into the caecum, using SCMC as a lubricant, was successful in all cases in which the technique was used. It is of interest that, since 2009, all horses that had surgery for ascarid impaction survived to discharge and horses admitted since 2009 had better short-term survival than those admitted prior to that. Because duration of colic prior to admittance was identical before and after 2009, this can be ruled out as a contributing factor. Since 2009 we have made a conscious decision to avoid opening the small intestine even at the risk of prolonging surgery and using extensive handling of the small intestine. This less invasive technique was probably the primary reason for the relatively high survival rate in our study. The decreased survival rate in horses undergoing small intestinal enterotomy may be a reflection of the severity of the disease as opposed to the actual procedure of opening the intestine . Our clinical experience, however, does not support that assumption as we have not seen less severe ascarid impactions in recent years. Nevertheless, we consciously strive to avoid enterotomy in cases where this procedure would have been performed in other situations.
According to Proudman et al. , duration of colic prior to surgery has a significant effect on survival, which correlates well with the improved survival rates we have encountered in recent years. We conclude that this improvement in survival after colic surgery is largely attributed to horses being referred earlier . In this study, time to referral was not associated with outcome. This may be due to the overall reduced time to referral that we see in our colic population because of improved referring veterinarian and owner awareness of the importance of the issue. In a study from 1996, median time to referral in a group of foals with ascarid impaction was 22.5 h with a 10% long-term survival rate . In a study performed a decade later in foals with ascarid impaction, the median time to referral was 12 h and the long-term survival was 27% . In the latter study, foals presenting within 12 h from showing first clinical signs of colic appeared to have a better survival rate (10/12) than foals arriving later (4/13 survivors). In our study, the duration of colic was shorter (median 8 h) which may have contributed to our improved long-term survival (60%); highlighting the importance of early treatment.
One of the potential reasons for the higher survival rate of horses in which diagnosis and enterotomy was not performed relates to the potential toxic effect of P. equorum on the intestinal serosa. This toxic effect may encourage adhesion formation and thus may have a negative effect on survival . This highlights a need for further research into the direct effects of P. equorum on small intestinal adhesion formation.
Intraoperative use of SCMC has been shown to decrease adhesion formation and improve survival rate following small intestinal surgery in horses [8,9]. As horses in which SCMC was used had significantly better short- and long-term survival than horses not receiving SCMC, it appears that SCMC in this case series had a positive effect on survival probably by reducing adhesion formation. Adhesions are a major fatal complication after colic surgery, they are more prevalent in foals  and, at least according to Cribb et al. , there is higher prevalence of adhesions after surgery for correction of ascarid impaction. Milking the impacted worms into the caecum often requires rather prolonged and aggressive handling of the small intestine. Serosal trauma by abrasion is an established model of intestinal adhesion formation and SCMC has been shown in this model to markedly decrease adhesions . Using a lubricant such as SCMC subjectively decreases the serosal trauma during the procedure and may decrease the likelihood of adhesion formation. We believe that the use of SCMC is an essential component of successful manual evacuation of ascarid impaction and is an important factor in the success achieved in this case series.
Omental adhesions have been previously demonstrated to cause colic  and omentectomy has been shown to reduce the adhesion formation rate in horses undergoing abdominal surgery . In this study, omentectomy did not have a significant effect on survival, despite the fact that all horses having omentectomy survived to discharge and all horses having omentectomy with sufficient follow-up time, survived long term. The lack of significance is likely due to the small number of cases in each group. Nevertheless, confounding variables such as the year the animal was admitted and performance of small intestinal enterotomy, prevented us exploring the individual effect of omentectomy in the current study.
According to Cribb et al. , simple ascarid impaction results in a significantly higher survival rate than impactions complicated by small intestinal volvulus or intussusception. In the current study, horses having concomitant surgical lesions such as small intestinal volvulus or intussusception did not differ in their short-term survival from horses with simple impactions. This provides at least some credence to our clinical impression that the intraoperative technique used has a more significant bearing on the outcome of the case than the presence of concurrent lesions. However, it is possible that the complicated cases in our case series were less severe than the ones seen by Cribb et al. .
Sixty percent (9/15) of the horses in our study were Arabians whereas in a recent study describing surgical colic in the same referral centre only 25% of the cases were Arabians . This difference in the breed distribution is significant (P = 0.003). These results may indicate that Arabian horses have a predilection for developing impaction of the small intestine with ascarids. Conversely, since most of the horse breeding industry in Israel involves Arabian horses and as ascarid impaction is more prevalent in relatively young horses , it may not be surprising to find overrepresentation of Arabian horses with the disease. In a recent retrospective study on ascarid impaction in horses, Standardbred horses were overrepresented ; however, in another study, no breed predilection was found .
The median age of horses in our study was 10 months, 27% of the horses were 2 years of age and older (4/15), with the oldest being 5-years-old. This age distribution is markedly different than previously reported. In 2 earlier retrospective studies of horses with small intestinal impaction with ascarids, the median/average age of affected horses was 5 months and in neither of these reports was a horse older than 2 years [4,5]. The presence of older horses in the present study may reflect delayed use of anthelmintic drugs leading to accumulation of worms and impaction; however, most horses had well scheduled deworming histories according to their owners. There was a significantly better survival rate for older foals in our study. Thus, the older age of the whole study population probably had a positive effect on the general survival rate. It has been shown previously that as foals mature they can better withstand abdominal surgery .
As horses mature, they acquire immunity against P. equorum and, therefore, intestinal impaction with ascarids is typically a disease uncommonly encountered in horses older than one year . There is growing evidence of a worldwide increase of resistance of P. equorum to commonly used anthelmintic drugs, especially macrocylic lactones, such as ivermectin . Changes in the characteristic host's age have been recently shown in horses with Oxyuris equi infection . These changes have been caused by decreased parasite immunogenicity leading to diminished acquired immunity by the host . Decreased immunogenicity of P. equorum may be responsible for the atypical distribution of age of horses in this study. If that is indeed the case, the combination of increasing resistance to anthelmintics and decreasing efficacy of acquired immunity may cause small intestinal impaction with ascarids to become more prevalent among horses of all ages.
The high percentage (80%) of horses that received an anthelmintic drug within 24 h prior to onset of clinical signs is consistent with the findings of a recently published study . It appears that ascarid impaction commonly occurs when a foal that is heavily infected with P. equorum is treated with an anthelmintic drug that either kills or paralyses the worms . In man, such a correlation between deworming and ascarid impaction has been well demonstrated . Some studies recommend using an anthelmintic that acts slowly (benzimidazole) as opposed to pyrantel and ivermectin that affect the neuromuscular system and paralyse the worms . To decrease the risk of ascarid impaction, it is recommended to initiate anthelmintics treatment as early as 8 weeks and to repeat deworming every 8 weeks for a year . The choice of anthelmintic should be based on the indigenous pattern of efficacy and not on random selection, otherwise resistance may develop leading to an increase in ascarid burden and the risk for impaction. Ideally, a routine Faecal Egg Count Reduction Test should be performed in order to monitor anthelmintic programme efficacy and adjust the programme according to test results .
Our study has 2 major limitations, the first being the small number of cases, which limits comparisons between groups. Due to the study size we cannot draw conclusive treatment recommendations for the general population based on our results. The other limitation is that, as of 2009, our technique for surgical management of ascarid impaction has been rather uniform. Thus it is impossible to ascertain the effect of individual variables on the outcome. Only a prospective controlled randomised study would be able to determine the contribution of individual variables such as enterotomy, omentectomy, use of SCMC and the horse's age on the outcome.
In conclusion, the results of the current study show that ascarid impaction surgery in the horse may not necessarily carry as poor a prognosis as formerly reported. The more favourable prognosis for horses with ascarid impaction compared with previous studies is attributed to earlier surgical intervention, more mature horses, the use of SCMC and refraining from performing a small intestinal enterotomy.
Authors' declaration of interests
The authors are not aware of any conflict of interest regarding the manuscript.
The authors would like to thank all referring veterinarians for their essential contribution and the hard work invested in these cases by the technicians, interns and residents of the department.
Dr. Tatz is responsible for all parts of the study, Dr Kelmer responsible for all parts aside from data collection, Dr. Milgram for study execution, data interpretation and manuscript preparation, Drs. Berlin and Steinman for data interpretation and preparation of the manuscript and Dr. Segev for data analysis and interpretation and manuscript preparation.
a SPSS for Windows, IBM, Chicago, Illinois, USA.