Zoonotic Transmission of Hepatic Hydatid Cyst from Domestic Dogs: A Case Report from an Urban-Marginal Area in Ecuador

Background

Cystic hydatidosis, or echinococcosis, is a zoonotic disease of worldwide prevalence with great economic impact. It poses a serious health problem for domestic and wild animals, and can spread to humans, creating a public health problem. It is caused by the larval stages (hydatid cysts) of the dog tape-worm Echinococcus granulosus, which affects animals and humans [1]. According to the World Health Organization (WHO), this pathology is one of the 20 neglected zoonotic diseases prioritized worldwide [2]. It has annual infection rates of 2 to 3 million cases worldwide [3], with an annual mortality rate of 2.2%, and it is estimated that 3.6 million years of life are lost per year due to disability. Likewise, it is responsible for more than $3 billion in medical expenses each year [2].

Domestic dogs play a key role in the transmission in acquiring the infection by ingesting the viscera of animals that contain hydatid cysts. However, humans can become infected by ingesting parasite eggs in contaminated food, water, or other sources [3,4].

The cysts are slow growing and contain clear fluid and many protoscolices. Each year, they grow approximately 1 cm and can reach a diameter of up to 20 cm [5]. They develop mainly in the liver (70%) and lungs (20%), and 10% can occur in any part of the body (brain, body muscles, kidneys, bones, heart wall, and eye socket) [6]. In the development stage of E. granulosus, the eggs hatch into larvae or oncospheres, which later transform into a hydatid cyst in the intermediate host and, if consumed by the definitive host, become an adult parasite [1].

According to the WHO (2021), the incidence rates of human hydatidosis in endemic regions can reach more than 50 per 100 000 inhabitants per year, and the prevalence can reach between 5% and 10% in some areas of Peru, Argentina, China, Central Asia, and East Africa [7]. The worldwide prevalence of echinococcosis is between 9% and 66% [8].

As the disease does not cause a manifest pathology in animals, deworming of dogs with praziquantel is used as a treatment for E. granulosus in the home environment [9].

The aim of this paper was to describe a zoonotic association in a home between a patient with a hydatid cyst and her parasitized dogs from the urban-marginal area “Balerio Estacio” in the city of Guayaquil, Ecuador. Likewise, we demonstrated how awareness and early diagnosis contributed to the timely treatment of hydatidosis.

Case Report

CLINICAL PRESENTATION, DIAGNOSIS, AND TREATMENT:

On October 1, 2022, in a routine visit to the urban area-marginal sector of the “Balerio Estacio” cooperative in the city of Guayaquil, Ecuador, a 40-year-old woman presented with a history of discomfort, pain in the upper-right hypochondrium, palpable mass, jaundice, and fever of several days of evolution. Clinical verification was made considering the epidemiological criterion (presence of cases at the site), laboratory analysis, and computed tomography (CT) scan, contrasted with optiray.

Consent was obtained before fecal and blood samples were collected from the patient. The patient was instructed about how to obtain the fecal sample and was provided with a sterile container. The blood and fecal samples were transported on the day of collection in refrigerated boxes at 4–8°C to the Pazmiño Clinical and Microbiological Laboratory in the city of Milagro, where they were analyzed by direct coproparasitic methods, flotation, and sedimentation, with centrifugation using saline solution. The sample was examined under a light microscope, using 10× and 40× objectives [10], and Entamoeba histolytica was found. However, it is important to mention that, in the anamnesis, the patient stated that she slept with and kissed her animals, and she had not dewormed her animals in many months. In addition, the patient reported not knowing of cases of hydatidosis in the sector. Regarding the blood samples, a complete blood count and liver function test were performed on the patient, yielding the following blood results: white blood cells 9200 U/L, red blood cells 4 900 000 U/L, hemoglobin 13 g/dL, hematocrit 40%, neutrophils 60%, lymphocytes 30%, monocytes 5%, basophils 1%, eosinophils 15%, platelets 280 000 mm3, aspartate transaminase (AST) 56 U/L, alanine transaminase (ALT) 70 U/L, and alkaline phosphatase (ALP) 180 U/L. According to the leukocyte count laboratory reference values described by Béavogui et al and Lala et al, the eosinophils were above the normal value and liver transaminases (AST, ALT, and ALP) were elevated, which is associated with parasitosis and liver disease [11,12].

Next, an abdominal computed tomography (CT) scan contrasted with optiray was performed in a private clinic, where the presence of hydatid cysts was determined in the liver without bile duct (intra- and extrahepatic) involvement (Figure 1). Subsequently, the patient underwent drainage (before and during surgery) and transabdominal laparoscopic excision in another private clinic to remove the cysts. A percutaneous puncture was performed prior to the surgery to determine the presence of a parasitic form. By microscopy and cytology, protoscolic and proligerous vesicles of E. granulosus were located. In addition, other tests such as Gram stain, acid-fast bacteria stain, and fungal stain were performed, but all were negative.

It is important to mention that, in the radiological findings, the following was determined: hypodense focal cystic lesion in the right hepatic lobe, with a single septum toward segment VI, VII, and VIII of 15 mm. The cyst had a transverse diameter of 110 mm. Furthermore, no pus was identified, but there was low-grade fatty infiltration.

Finally, treatment was indicated before and after surgery with albendazole at a dose of 15 mg/kg/day, twice a day for three 30-day cycles, with 2-week rest periods. One month after the treatments, she did not present symptoms, and a week later, no hydatid cysts were observed in the liver through abdominal ultrasound.

IDENTIFICATION OF THE SOURCE OF ECHINOCOCCOSIS:

Stool samples were collected from the 2 dogs, with the consent of their owner. The samples were collected on October 2, 2022, and transported the same day in refrigerated boxes at 4–8 °C to the laboratory of the Besito Vet Pet veterinary clinic to be analyzed by coproparasitic methods: direct, flotation, and sedimentation, with centrifugation using saline solution. The sample was observed by optical microscopy using 10× and 40× objectives, and Lugol’s solution was used to improve the visualization [13,14]. Finally, both samples were positive for E. granulosus (Figure 2). The eggs were spherical in shape and contained a hexacanth embryo with 3 pairs of hooks, with a size of 33 microns, as described by Bowman [14].

Subsequently, the stool samples of the dogs were analyzed using the coproantigen ELISA technique, following the procedures described by Merino et al and Flores et al. All samples were positive for E. granulosus [15,16].

:

The dogs infected with E. granulosus were dewormed with a dose of antiparasitic medication (praziquantel 5 mg/kg and pyrantel 15 mg/kg) [15]. After 1 month, 3 coproparasitic examinations were performed: direct, flotation, and sedimentation, with centrifugation using saline solution to confirm the absence of the parasite. The disease was also controlled by deworming all family members and by conducting health education campaigns in the sector, where the impact of this parasite on the environment was explained. In addition, the house and surroundings were cleaned and disinfected, as were the water and objects used by pets.

Discussion

In this investigation, the fourth case of a hydatid cyst was registered in Ecuador. The host was a 40-year-old woman who presented characteristic symptoms [17–19]. The first case in the country was reported in 1988 in an indigenous 20-year-old male patient of Shuar ethnicity from the Taisha municipality, Morona Santiago province [17]. In 2000, the second case was reported in an 84-year-old female patient, who was a resident in the city of Guayaquil [18]. Finally, Guanuchi and González reported the case of an 81-year-old woman from the city of Ambato [19].

Among the clinical manifestations of cystic echinococcosis in the liver are fever, pruritus, urticarial rash, anaphylactic reaction, cystic tumor, eosinophilia [5], hepatomegaly, right upper quadrant abdominal pain, jaundice, and digestive symptoms [4]. Some nonspecific signs are anorexia, weight loss, and weakness [7]. All these symptoms are similar to the present reported case.

In this study, E. histolytica was found in the patient as a coinfection. It should be noted that its evidence is scarce in cases of hydatidosis. In addition, the presence of hydatid cysts in the liver was identified and confirmed by CT with contrast, as described by Aguilar et al [20] and Rinaldi et al [21]. The cysts were removed surgically, and parasitic forms of E. granulosus were found inside, findings also reported by Rinaldi et al [21] and Botero and Restrepo [4]. Eosinophils and elevated liver transaminases, determined in the present patient, coincide with cases described by Ramírez et al, Elshazly et al, and Kim et al [18,22,23], but they differ from the results of González et al [5], Orea et al [24], and Bonfrate et al [25].

The 2 cases of E. granulosus identified in the dogs of the infected person showed zoonotic activity between them; throughout China, there is a prevalence of E. granulosus in domestic dogs between 0.5% and 2% [26–28]. Various prevalence rates of E. granulosus have been reported in domestic dogs, including in African subregions (1.7%) [29], China (7.3%) [30], Mediterranean and Balkan European countries (0%–31.9%) [31], Peru (5.1–13.8%) [15], Ecuador (0.5–2%) [27,28], Brazil (7.7%), Bolivia (3.4%) [16], Chile (7.2%) [32], and Argentina (9.3%) [16]. In addition, the cases identified in the dogs in the present report were confirmed by coproantigen ELISA, following the procedures described by Merino et al and Flores et al [15,16].

It is important to note that over time, liver hydatid cysts can cause severe liver disease, and they have a high risk of mortality if left untreated. In addition, cysts occasionally rupture and cause severe allergic reactions in humans [26]. Therefore, the ideal method for hepatic cystic echinococcosis is surgery, which allows the infection to be completely eliminated. In the present clinical case, the hydatid cysts were removed by surgery, as in the studies by Orea et al [24], Guanuchi and González [19], and Kim et al [23].

In our study, we used the same procedures described by Botezatu et al [33], who mention that eosinophilia is a worrisome sign of echicococcosis, and Singh et al [34], who performed various tests such as Gram staining, acid-fast staining, and fungal staining to rule out E. granulosus. The pathology determined in the present study (liver hydatid cyst) was similar to that described by Orea et al [24]; however, it differs from the reports by Galvis et al [35], Guanuchi and González [19], and Aguilar et al [20].

Treatment is almost always surgical for large, calcified cysts. However, the administration of albendazole or mebendazole is also recommended as a pre- and postoperative treatment [24]; in the present case, the procedures described by González et al [5] were followed. In patients in whom surgery is not indicated, albendazole is used at a dose of 10 to 15 mg/kg/day in 3 or more cycles of 4 weeks, with rest periods of 2 weeks; mebendazole can also be used at a dosage of 200 mg every 12 h for 6 days [5].

The patient in this study had a middle-income level and lived in a concrete house but reported that she did not deworm her dogs, kissed them on the mouth, and slept with them. Supposedly, the parasite was latent for a long time in the studied location until it found susceptible hosts. This was demonstrated by the large number of parasite eggs in the feces of the dogs and the presence of their cysts in their owner. A similar situation was described by González et al [5].

Conclusions

This is the case report of a liver cyst identified in a 40-year-old woman. In turn, E. granulosus eggs were identified in the patient’s dogs. Therefore, there was zoonotic transmission in 1 household, and the community was exposed to significant environmental risk from this pathogen. In addition, it is important to educate the population about sanitary measures and the obligation to deworm animals periodically to avoid the transmission of this and other parasites.