Symmers (1) documented that infection caused by Enterobius vermicularis (E. vermicularis) was reported in the literature as early as 1919. It is an obligate parasite and humans are the only known natural host. The life cycle of E. vermicularis is 2 to 4 weeks. Digestive secretions dissolve the egg-releasing larvae in the duodenum. Larvae then mature into adult worms that inhabit and mate in the terminal ileum, caecum and ascending colon. At night the female migrates to the rectum and lays her eggs in the anal canal. Infection then occurs either by the faecal–oral route or by retroinfection, in which the eggs hatch in the anus and the worms re-infect the colon by migration. There is an increased prevalence in children, overcrowded living conditions and developing countries (2).
There is much debate as to whether E. vermicularis causes serious disease in the gastrointestinal tract or is merely a “passenger.” Certainly, ectopic infections, seen mainly in females, can cause significant morbidity. Many patients are asymptomatic; however, the chief symptom is anal itch, which can manifest as irritability and insomnia. The most common complication is secondary bacterial infection of broken anal skin.
Many authors describe case reports of colitis secondary to E. vermicularis infection (3–5). Patients present with pain, rectal bleeding, fever, nausea, vomiting and increased frequency of stools, and in all instances symptoms resolve with antiparasitic therapy alone.
Our observation that a substantial number of children presenting with painless rectal bleeding were identified as having E. vermicularis at colonoscopy prompted a retrospective review of all of the colonoscopies performed at our unit during a 3-year period.
There are no UK published data on the prevalence and morbidity of enterobiasis in children. Armengol et al. published in abstract form a study of a population of 1917 Spanish children ages 6 to 10 from 1994 to 1996 (6). They found the prevalence of E. vermicularis to be 20% using stool analysis and the Sellotape test. Lacroix et al. published in abstract form a study of the prevalence of E. vermicularis in hospitalised children in Denmark (7). E. vermicularis was detected by the Sellotape test during the period 1996 to 1997. In 186 children ages 1 to 17, the prevalence of E. vermicularis was 22%.
E. vermicularis can be detected in saline swabs or by retrieving eggs from the perianal skin in the early morning (Sellotape test) and also by direct visualisation of the adult worms at colonoscopy. The infection is treated with mebendazole or piperazine. It is important to remember to treat family members to prevent reinfection and spread of disease and to implement routine hygiene measures, particularly hand-washing, following toileting and before mealtimes.
In our retrospective review we asked the following questions: What is the prevalence of E. vermicularis in children presenting with symptoms suggestive of inflammatory bowel disease? How reliable are conventional diagnostic methods (eg, saline swabs, Sellotape test) at detecting E. vermicularis? Is there a histological correlation with carriage of E. vermicularis? Do symptoms improve with antiparasitic therapy?
PATIENTS AND METHODS
The present study was retrospective in nature and data were analysed for the period May 1997 to December 1999. The demographic, laboratory and clinical information were obtained from case notes, endoscopy records and histopathology reports. Patients were identified as having E. vermicularis infestation by direct visualisation of the adult worms at colonoscopy. These subjects and their family members were treated with mebendazole, 100 mg, which was repeated after 2 weeks. Subsequently, a record of the clinical response to treatment was documented. Using direct visualisation of adult worms at endoscopy as the “gold standard,” we ascertained the accuracy of the Sellotape and saline swab tests at determining the presence of E. vermicularis. The Sellotape was applied to the perianal skin in the early morning, and then fixed to a microscope slide and examined. Saline swabs were moistened in saline, then wiped around the anal margin. In the laboratory, excess saline was drained into a tube and the damp swab pressed onto a microscope slide before discarding. Local research and ethical committee approval was granted for the study, and data analyses were performed using Microsoft Excel 97.
During the study period of 32 months from May 1997 to December 1999, 180 colonoscopic examinations were performed. The most common indications were rectal bleeding and suspected inflammatory bowel disease. E. vermicularis was identified macroscopically in 31 cases (17.2%) (Fig. 1). We were able to collect complete data on 26 of 31 children (83.9%) The mean age was 11.45 decimal years (range, 2.58–15.67). The male-to-female ratio was 1.4:1.
The symptom profile of patients with E. vermicularis were abdominal pain, 19 of 26 (73%); rectal bleeding, 16 of 26 (62%); chronic diarrhoea, 13 of 26 (50%) and weight loss, 11 of 26 (42%). Symptoms had been present for a mean of 17 months (range, 2 weeks–5 years). No patients experienced the classic symptoms of perianal itch and probably represent a specific subgroup of patients colonised by the parasite.
No patient had significant anaemia. Two patients demonstrated a peripheral eosinophilia. Ova, cysts and parasites were identified in none of the saline swabs analysed in 20 patients. Sellotape testing was underused, performed in only 4 patients and was negative in all.
Of the 26 children, 21 demonstrated histopathological evidence of nonspecific colitis (ie, shallow mucosal ulceration with segmental subepithelial bleeds, eosinophilic infiltration and mild focal inflammation). Two children demonstrated normal mucosa.
All children found to have E. vermicularis were treated with mebendazole, 100 mg, which was repeated after 2 weeks. A positive clinical response was seen in 19 of 23 patients (83%) over a variable follow-up period of 1 to 5 years. None of the patients subsequently developed inflammatory bowel disease. Three of the original 26 patients were lost to follow-up.
Although most patients infected with E. vermicularis are asymptomatic, there are a few case reports in the literature of E. vermicularis causing serious disease. Avolio et al (2) reported 13 cases of E. vermicularis presenting as perianal abscess or granuloma, all of which required surgery. They suggested routine screening for E. vermicularis in all children presenting with this condition.
Ajao et al (8) described E. vermicularis causing symptoms of appendicitis in a 14-year-old boy. Histology of the appendix was normal; however, presence of the pinworm in the lumen of the appendix may produce the clinical picture of appendicitis. Perforation of the appendix can facilitate the spread of E. vermicularis into the peritoneal cavity, where it may go on to produce granulomata in the liver, spleen or kidney.
Tandan et al. (9) described a case of pelvic inflammatory disease thought to be caused by enterobius in a 13-year-old girl. She also had peritonitis manifesting as yellow-green exudates in the peritoneum. The authors suggest larvae accessing the female genital tract may enter the peritoneal cavity via the fallopian tubes leading to peritonitis.
In this retrospective series, E. vermicularis was identified macroscopically in 31 of 180 colonoscopies (17.2%). We suggest that in patients with symptoms suggestive of inflammatory bowel disease E. vermicularis must be excluded as a nonspecific cause of colitis. There is an increasing need to dispense with vague terminology such as “nonspecific colitis,” and when we identify inflammatory changes in association with the presence of E. vermicularis we classify this as “Enterobious colitis.”
Identification of E. vermicularis by saline swab and Sellotape test in our cohort was unsuccessful. Although 20 of 26 patients had saline swabs, 0 detected E. vermicularis. The Sellotape test was underused, performed in only 4 of a possible 26 patients, and it was negative in all of them. This reflected the notion that the test has a low sensitivity because of the variable emergence of worms at the anal verge, and the intermittent nature of egg laying with respect to their life cycle. Although we acknowledge that repeating the test 3 times raises the level of sensitivity, this can be difficult to achieve when samples require collection in the early morning by family members. A more sensitive and specific noninvasive test is required to exclude the condition.
Of 31 cases of E. vermicularis identified macroscopically at colonoscopy, 81% of the histology was reported as nonspecific colitis. This should prompt the clinician and histopathologist to consider E. vermicularis as a cause of nonspecific colitis.
The good clinical response to treatment with mebendazole (19 of 23) indicates that E. vermicularis colitis can be treated simply and effectively. It is now our practice to initially offer this treatment empirically to a select group of patients who present with intermittent rectal bleeding, but who have no significant change of bowel habit or weight loss.
In conclusion, E. vermicularis must be excluded as a common cause of nonspecific colitis in patients with symptoms suggestive of inflammatory bowel disease. Identification of E. vermicularis infestation by noninvasive tests may be lacking in sensitivity, but if identified at colonoscopy, the condition is readily treated with mebendazole, leading to resolution of symptoms in the majority of patients.
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