Abstract
Taeniasis is an intestinal helminth infection due to adult tapeworms belonging to the genus Taenia. Taeniasis remains a major burden in low-income countries in Asia. We present a case of intestinal perforation caused by adult tapeworm of Taenia in a 50-year-old Nepali male. The patients presented to the hospital with severe abdominal pain and intermittent vomiting. Following clinical presentations and imaging features, gastrointestinal perforation was suspected. Surgical removal of adult tapeworm of Taenia, suspected to be T. saginata or T. asiatica, was carried out during exploratory laparotomy, which was followed by an uneventful postoperative period. In addition to case presentation, we systematically review published case reports on taeniasis-related intestinal perforation. A learning point from this case is clinician should maintain a clinical suspicion of taeniasis as a possible cause of intestinal perforation in endemic areas.
Introduction
Taeniasis is an intestinal infection caused by adult tapeworms. Three parasite species cause taeniasis in humans: Taenia solium (pork tapeworm), Taenia saginata (beef tapeworm), and Taenia asiatica (a species phylogenetically closely related to T. saginata). 1 The human definitive host gets infected with T. saginata and T. solium by eating undercooked meat of the parasites’ respective intermediate host (T. saginata: cattle; T. solium: pigs) harboring the infective larval stage of the parasite (cysticerci).2,3 The life cycle of T. asiatica differs from that of T. saginata in its intermediate host (pigs vs cattle) as well as in the infected organs (liver vs muscle). 1
Most human taeniasis infections are asymptomatic and the only noticeable sign of infection is the passing of proglottids in the stool. 4 Nevertheless, unspecific gastrointestinal symptoms like nausea, vomiting, vague abdominal discomfort or pain, increased appetite, weight loss, or pruritus ani may be present.4,5
The diagnosis of taeniasis is made through the patient’s history (passing of proglottids), macroscopic identification of proglottids, or the microscopic detection of eggs in stool samples. Confirmation of Taenia species is conducted by morphological examination of tapeworm (adult tapeworm length, scolex [presence of rostellum], neck, and proglottid). 3 While Taenia eggs are microscopically indiscriminable, proglottids allow morphological species determination by assessing the number of primary uterine branches. Fewer than 13 primary uterine branches correspond to T. solium, more than 13 uterine branches correspond to either T. saginata or T. asiatica. 3 The proglottids morphology of T. saginata and T. asiatica is practically the same and, although the 2 species may be differentiable based on morphological features by experts, 1 the differentiation of the 2 species is mostly done by molecular diagnostic methods like polymerase chain reaction (PCR). 6 Taeniasis is easily treated by application of a single oral dose of praziquantel (10-20 mg/kg body weight) or niclosamide (adults: 2 g; children: 50 mg/kg body weight). 7
We report and discuss the case of ileal perforation due to adult tapeworm of Taenia in an academic hospital in low-resource setting and systematically review published case reports on taeniasis. The SCARE 2020 Guideline was used to guide the writing of this case report. 8
Case Description
A 50-year-old male from Gorkha district of Gandaki Province, Nepal presented to the emergency room of the Tribhuvan University Teaching Hospital (Kathmandu, Nepal) with increasingly severe abdominal pain for a day and a history of generalized abdominal pain, intermittent vomiting, and fever for 15 days. The patient denied history of traveling to any foreign countries. At admission, he was afebrile, hypotonic, and tachycardic with a blood pressure of 80/60 mmHg and a pulse rate of 100/min. The physical examination revealed generalized abdominal tenderness, guarding, and rebound tenderness but was otherwise unremarkable. Abdominal ultrasonography showed free intraperitoneal fluid in the left upper quadrant and a thickened small bowel wall and the chest X-ray revealed free air under the diaphragm on both sides establishing the diagnosis of pneumoperitoneum (Figure 1A). The full blood count showed leukocytosis (WBC 17 400/mm3; 78% neutrophils, 20% lymphocytes).
(A) Chest X-ray at hospital admission showing free air under the diaphragm. (B) Removed Taenia saginata tapeworms (two worms measuring approx. 2 and 3 m [laid out on surgical drape] and strobila parts [in metal kidney dish]).
With the provisional diagnosis of gastrointestinal perforation, the patient was taken to the operation theater and an exploratory laparotomy was performed. The exploratory laparotomy showed approximately 200 ml of pus in the peritoneal cavity, dilated small bowel loops, a single ileal perforation measuring ~2 × 2 cm at the antimesenteric border ~20 cm proximal of the ileocaecal junction. Through the perforation site 2 large Taenia tapeworms, measuring approximately 2 and 3 m, as well as several smaller Taenia worms protruded through the perforation site (Figure 1B). After cleaning of the peritoneal cavity, removal of the Taenia worms, and closure of the perforation site, a loop ileostomy was performed. The rationale behind the loop ileostomy was that it was impossible to rule out the presence of additional Taenia tapeworms possibly leading to obstruction in the postoperative period. To eradicate any possibly remaining Taenia tapeworms, the patient received a single oral dose of praziquantel (400 mg).
The patient denied any history of passing proglottids, however, based on microscopic analysis of the morphology of scolex and proglottids (number of uterus branches observed), it may be concluded that this parasite is suspected to be T. saginata or T. asiatica. Due to resource limitations in our hospital, we are not able to conduct PCR test to further differentiate the parasite. The histopathological examination of the excised margin of the perforation site showed granulation tissue with signs of acute and chronic inflammation involving the full thickness of the bowel wall. No atypical cells or granulomas were seen. When the culture of the peritoneal fluid revealed the presence of extended-spectrum beta-lactamase-producing Klebsiella pneumonia and Escherichia coli, the patient was treated, according to the susceptibility testing results, with meropenem (1 g i.v. 3 times per day) for 7 days. The remainder of the post-operative period was uneventful, and the patient was discharged on the eighth post-operative day. After 1 year of follow-up, no additional complaint or recurrence was reported.
Discussion
Although Taenia has a worldwide distribution, its occurrence is more common in low-income countries. Substantial prevalence of T. saginata, considered the most common zoonotic tapeworm, has been reported throughout East, Southeast, and South Asia due to lack of adequate sanitation, food safety measures, and health education standards. 9 As the consumption of beef is extremely uncommon in Nepal due to socio-cultural context (cow is considered sacred and existing ban for cow slaughter), it is more likely that the patient’s infection is due to T. asiatica. We speculate consumption of pig liver would be the most likely source of infection in this case.
Although rare, several intestinal as well as extra-intestinal complications due to taeniasis have been reported. A systematic literature review conducted in 2017 on surgical abdominal pathologies caused by helminths identified following numbers of case reports on T. saginata related complications: appendicitis (n = 11), gastrointestinal perforation (n = 5), migration of biliary tract (n = 3), intestinal obstruction (n = 2), acute cholecystitis (n = 2), and duodenal stump leakage (n = 2). 10 Other complications (n = 1) reported include acute abdomen, gallbladder perforation, colonic anastomosis leakage, esophageal leak, acute cholangitis, acute pancreatitis, Meckel’s diverticulitis, and acute intestinal bleeding. 10 Of note, no case reports on surgical abdominal complications due to T. solium were identified in this review.
We systematically conducted a review of published case reports on taeniasis-related intestinal perforation. A search was conducted on 14 April 2021 of Medline, ProQuest, and Google Scholar (first 50 results only) using the following broad search string: “(taenia*) AND (case report* OR case series) AND (gastrointestinal perforation OR intestinal perforation OR peritonitis).” Initial 306 records were screened by title and narrowed down to 10 case reports (as detailed in Figure 2). Details of the included case reports are displayed in Table 1.
Flow diagram of literature review.
Case reports on intestinal perforations related to taeniasis.
Abbreviations: F, female; M, male; n.d., no data.
The underlying pathophysiology of taeniasis-related intestinal perforation is not entirely clear. The most often quoted theory is that the impaction/mechanical obstruction of the gut lumen, by a bulk formed by the parasite’s strobila, enhances the parasite’s mucosal contact. 19 This parasite-mucosa contact is considered to cause a local irritative inflammatory reaction that predisposes to perforation. As seen in Table 1, the observation that the most frequent perforation site is the small bowel indirectly supports this theory, since there the intestine’s luminal diameter is narrowest which provides favorable conditions. 21
In line with this mechanical theory, the absence of reports on T. solium taeniasis related intestinal perforation (Table 1) may be explained by the overall smaller average size/length of the adult parasite (T. solium: 2–7 m vs T. saginata: 4–12 m), 7 which lowers the likelihood of the worm’s impaction. Based on mechanical theory, a high number of worms would also predispose to perforation. While the finding of two large and several smaller tapeworms in our case would support this assumption, the majority of case reports report only a single worm (Table 1). However, since it is impossible to inspect the entire length of the intestinal lumen, the presence of multiple worms can never be excluded.
Regarding extraintestinal complications, T. solium shows also considerably less potential for complications. Yu et al 22 reported a case of cholecystitis caused by T. solium and reviewed the published literature in 2019. They found that previously only 16 case reports of hepato-pancreatico-biliary taeniasis have been published (reporting Taenia tapeworms in the gallbladder [n = 10], the pancreatic duct [n = 3], the bile duct [n = 2], and as a cause of a liver abscess [n = 1]) and that all 16 cases were related to T. saginata or T. asiatica. 22 This disproportionate finding may be explained by the fact that the proglottids of T. saginata and T. asiatica show active motility, thus allowing for extraintestinal migration of the parasite, while T. solium proglottids lack active motility. 23 The active motility of T. saginata tapeworms may also explain their reported emergence from an anastomotic leakage site and a post-appendectomy fecal fistula.24,25
Interestingly, when reviewing the literature on complications related to Diphyllobothrium latum (fish tapeworm), which is the largest tapeworm that can infect humans (up to 25 m in length), 26 massive infections have been reported to cause intestinal obstruction and aberrant migrating proglottids may cause cholangitis or cholecystitis. 26 However, we were only able to identify 3 case reports, which reported occlusion, 27 intermittent obstructive symptoms, 28 and subacute appendicitis, 29 and we could not find any case report on intestinal perforation or biliary complications related to human diphyllobothriasis.
Conclusion
Taeniasis remains prevalent in low-income countries with T. saginata as the most common zoonotic tapeworm. T. saginata and T. asiatica tapeworms are more likely to cause intestinal and extraintestinal complications compared to T. solium tapeworms. Due to similarity in a morphological feature, a PCR test is needed to provide definitive specimen confirmation for Taenia spp. In an endemic region, clinician should maintain a clinical suspicion of taeniasis as a possible cause of intestinal perforation.
Footnotes
Acknowledgements
We thanked Dr. Dhruba Narayan Sah and Dr. Ranjut Sah for their support in this study.
Author Contribution
R.B: conceptualization, methodology, formal analysis, investigation, writing—original draft, visualization. R.C: writing—original draft. E.S: formal analysis, writing—review and editing, visualization. H.A: investigation, writing—review and editing. A.D: writing—review and editing. A.A.A: writing—review and editing. B.P: writing—review and editing. A.U: writing—review and editing. A.N: formal analysis, writing—review and editing, visualization, supervision. All authors approved the final version of the manuscript.
Declaration of conflicting interests:
The author(s) declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.
Funding:
The author(s) received no financial support for the research, authorship, and/or publication of this article.
Ethical Approval
This study is exempted from ethnical approval from Tribhuvan University Teaching Hospital.
Informed Consent
Written informed consent was obtained from the patient for publication of this case report and accompanying images.
