Acute Cholecystitis Due to Taeniasis: A Case Report of an Unusual Site of or Infection

Introduction

Taeniasis is a pathological condition resulting from human infestation with several species of parasitic tapeworm of the Taenia genus, including Taenia solium, Taenia saginata, and Taenia asiatica [1]. These infections usually occur when individuals consume inadequately cooked pork (in the case of T. solium and T. asiatica) or beef (in the case of T. saginata), containing cysticerci that mature into adult tapeworms within the intestinal tract [2]. Taeniasis is particularly prevalent in rural areas with insufficient sewage treatment and close cohabitation of humans with cattle or pigs, and with consumption of raw or undercooked parasitized meat [3].

Many individuals infected with Taenia spp. remain asymptomatic and are often unaware of the infection until proglottids or segments appear in their fecal matter or are isolated on underwear or bedding [4]. In cases in which symptoms manifest, taeniasis can present with gastrointestinal disturbances, including, but not limited to, nausea, abdominal pain, weight loss, and diarrhea [5]. Although it primarily affects the small intestines, this parasitic infection can occasionally extend beyond these organs into extraintestinal sites, such as the appendix, pancreas, liver, and biliary system [6].

This report describes a unique case of acute cholecystitis in a 47-year-old woman that was caused by a T. saginata or T. asiatica infection. Considering the remarkable infrequency of this disease, we report this case along with a thorough review of the relevant literature.

Case Report

A 47-year-old Thai woman presented to Nan Hospital, located in northern Thailand, with severe abdominal pain in the epigastric region that had started 6 h prior. She also reported experiencing 2 episodes of nausea and vomiting but no fever or diarrhea. She denied a history of strange eating habits or traveling outside the country. The patient was fully conscious during the physical examination, without pale conjunctivae or icteric sclerae. An examination of her heart and lungs revealed no abnormalities. However, abdominal palpation revealed marked tenderness in the epigastric and right upper quadrant regions. No involuntary guarding or muscle rigidity was observed. Examinations of the neurological, musculoskeletal, and genitourinary systems revealed no noticeable abnormalities or signs of distress. Preoperative laboratory findings revealed no anemia or leukocytosis. Differential white blood cell and platelet counts were within the normal ranges. No electrolyte imbalances were observed. Nevertheless, the patient exhibited mild direct hyperbilirubinemia and transaminitis.

Abdominal ultrasonography revealed findings suggestive of multiple gallstones. An increased thickness of the gallbladder wall was also observed. The patient’s liver size appeared normal. These findings were consistent with a diagnosis of acute cholecystitis. The patient was prescribed intravenous omeprazole and buscopan for symptom relief and intravenous ceftriaxone as a preoperative antibiotic. Elective cholecystectomy was scheduled 1 day after admission, to remove the gallbladder surgically.

The resected gallbladder (Figure 1) measured 9×3.5×2.5 cm in size and had a smooth serosal surface. Its mucosa appeared irregular and brown and was covered with tan fibrin. The thickness of the gallbladder wall was measured at 0.5 cm, and no gallstones were identified. A tapeworm measuring 70 cm in length and 0.8 to 1.0 cm in width was found in the lumen of the gallbladder. Histopathology of the gallbladder tissue stained via hematoxylin and eosin (H&E) (Figure 2) revealed that the wall was edematous, and the mucosa exhibited signs of necrosis and acute inflammation. Further examination of sections taken from the parasite (Figure 3) with H&E stain revealed a thick tegument layer, smooth muscle layers, and calcareous corpuscles. The parasite was preserved in 10% formalin solution from the first hospital before being sent to the Department of Parasitology, Chiang Mai University, Chiang Mai, Thailand. Owing to the use of a preservative agent, the specimen hardened and shrank, molecular identification could not be performed, and standard staining procedures could not identify the parasite species. The gravid proglottids were transferred into a microcentrifuge tube of 10% potassium hydroxide to prepare the specimen. These tubes were submerged in a beaker containing distilled water and boiled at 80°C for 3 min. The specimens were submerged in a normal saline solution for 10 min to remove the 10% potassium hydroxide. Next, they were compressed using glass slides wrapped with a rubber band, then submerged in 10% formalin for 12 h to undergo re-fixation and create hard tissue. For staining, the flattened samples were rinsed with tap water for 12 h to remove formalin and then submerged in distilled water for 1 h. Samples were stained with Semichon’s acetic carmine solution and allowed to sit for another 12 h. Excess stain was removed using a hydrochloric acid solution in 70% ethanol for approximately 1 to 2 h. Following this, specimens were dehydrated by immersion in 50% ethanol twice, for 3 to 4 h each time. The process was repeated with 70%, 95%, and absolute ethanol. After dehydration, the specimens were immersed in a xylene solution for approximately 20 min. Finally, the samples were mounted using a resin mounting medium (Entellan new, Sigma-Aldrich: Merck KGaA, Darmstadt, Germany) and allowed to dry at room temperature, creating permanent slides of the Taenia spp. Microscopic examination (Figure 4) revealed 20 to 22 uterine branches in each of the 5 gravid proglottids, with 42 to 55 uterine twigs and an average uterine twigs to branches ratio of 2.41. Furthermore, the morphology of the specimen (number of uterine branches, number of uterine twigs, and ratio of uterine twigs to branches) provided evidence confirming that the worm in question could possibly be T. saginata or T. asiatica [7,8].

The patient experienced relief from her abdominal pain following the cholecystectomy procedure. The attending physician prescribed 4 tabs of niclosamide (500 mg) as an anti-helminthic drug. The patient was discharged on the seventh day following the completion of postoperative care.

Discussion

Gallbladder taeniasis, also known as gallbladder tapeworm infection, is a rare condition caused by tapeworms in the gall-bladder. It is typically caused by T. saginata or T. solium tapeworms [6]. We reviewed the literature on cases of gallbladder taeniasis in Table 1. Benedict et al described the first biliary migration of T. saginata and concluded that biliary taeniasis should be used to describe the presence of Taenia worms in the biliary channels [9]. The adult forms of Taenia worms travel through the ampulla and infect the gallbladder or biliary tracts [9,10]. After activation of the cysticerci, these adult worms may have migrated into biliary channels before being affixed to the small intestine wall, as is typical for these parasites [11].

Patients with gallbladder taeniasis can experience a range of symptoms or none. The most common symptoms are abdominal pain, nausea, vomiting, and fever. Less commonly, tapeworm infection can cause complications such as cholecystitis, choledocholithiasis, and pancreatitis [11,12].

Abdominal ultrasonography is a noninvasive technique for detecting helminths in the biliary system and pancreas [13]. Al Absi et al [14] studied the value of ultrasound for diagnosing and managing biliary ascariasis. They concluded that ultrasound is highly effective for diagnosing biliary ascariasis, owing to its high sensitivity and specificity. In our case, abdominal ultrasonography revealed a thickened gallbladder and multiple gallstones. The ultrasound report showed that the observed gallstones may have actually been the merging of whole helminths, which ultimately resemble gallstones.

Pathological findings associated with Taenia spp. in the gallbladder can vary. A case reported by Yu et al [6] described gallbladder taeniasis characterized by multifocal ulceration of the gallbladder mucosa, covered with a fibrinoid crust, and accompanied by infiltration of lymphoplasmacytic cells and eosinophils. However, in our case, examination of the cholecystectomy specimen showed mucosal necrosis, an edematous gallbladder wall, and infiltration of acute inflammatory cells – all of which were consistent with a diagnosis of acute cholecystitis. Regarding the size of the parasite, there is plausible evidence that it may have settled unnoticed inside the gallbladder for a prolonged duration before the patient finally experienced symptoms of acute cholecystitis.

Several methods are used to identify Taenia species, such as amplifying the 440bp fragment of the cox1 gene by polymerase chain reaction [15]. According to findings reported from Tibet, an amplified tapeworm cox1 gene showed 100% homology with the Iranian isolate T. saginata, and 99.5% to 99.8% homology with T. saginata samples taken from other areas of China [15]. Unfortunately, genetic material-associated methodologies were not used in our species identification process. The morphological approach used in this study was Semichon’s acetic carmine staining [16]. Our case results suggest that identifying helminth species can be challenging when relying on suboptimal specimens. This is because of the frequent loss of crucial morphological characteristics, such as the number, shape, and size of certain anatomical structures, caused by the fixative substances (eg, formalin) used to construct slides from tissue samples of the parasites. According to our protocol, the material was first fixed in a formalin solution. Consequently, the excised and fully-developed proglottids were slightly toughened before they were flattened and stained. Hence, the resultant slides may have been of suboptimal quality. However, some distinguishing features, such as the presence of 20 to 22 uterine branches and an average ratio of uterine twigs to branches of 2.41 (ie, 42 to 55 uterine twigs) [8,17,18], may be helpful in identification between T. saginata and T. asiatica in the future. Therefore, our work suggests preserving specimens using 70% to 100% ethanol for morphological and molecular study.

Northern Thailand has a high prevalence of taeniasis, with T. saginata being the most prevalent species, followed by T. solium [19–21]. In 2011, Maipanich et al reported 68 taeniasis cases using a stool examination and found tapeworm strobila in the stool from Ban Luang and Ban Pang Kae villages in Nan province. Of the 22 cases of discharged tapeworm strobila, 18 had tapeworm strobila that were positive for T. saginata, and 4 were not identified using molecular identification [19]. In 2021, Kusolsuk et al reported 22 cases of taeniasis (20 cases of T. solium and 2 cases of T. saginata) among the Karen people of Tha Song Yang District, Tak province [21]. Only one region of Thailand currently reports 10 cases of T. asiatica infection: Thong Pha Phum district, northwest of Kanchanaburi province, western Thailand [20,22,23]. This region’s high incidence of taeniasis was associated with consuming raw meat, specifically beef, buffalo, and pork. The popular local dishes contain raw or undercooked meat, such as Larb (spicy minced beef, buffalo, or pork meat with herbs), Lu (raw beef or buffalo meat mix with blood and herbs), and Sa (undercooked beef or buffalo salad meat with herbs) [19,21]. However, limited reports and information are available on the prevalence of taeniasis and the distribution of Taenia spp. in Thailand. Thus, the molecular species identification of Taenia spp. will provide useful information for species identification and disease control.

Conclusions

We present the case of a Thai female patient with acute cholecystitis caused by T. saginata or T. asiatica. Our findings regarding symptomatic infections caused by adult Taenia parasites are significant. While such cases are rare, and there is a potential for misdiagnosis on imaging investigations, clinicians should consider the possibility of Taenia spp. infection in the biliary system, particularly in regions where these infections are prevalent.