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20 April 2023: Articles  Ecuador

Hymenolepiasis Caused by in Humans and Natural Infection in Rodents in a Marginal Urban Sector of Guayaquil, Ecuador

Unusual clinical course, Challenging differential diagnosis, Management of emergency care

Roberto Darwin Coello Peralta ORCID logo1ABCDEFG*, María de Lourdes Salazar Mazamba ORCID logo1BCDG, Betty Judith Pazmiño Gómez ORCID logo2DEF, Diego Martín Cushicóndor Collaguazo ORCID logo1BCD, Eduardo Alfredo Gómez Landires3EF, Geraldine Ramallo ORCID logo4ABCDE

DOI: 10.12659/AJCR.939476

Am J Case Rep 2023; 24:e939476

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Abstract

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BACKGROUND: Hymenolepiasis is a globally prevalent zoonosis of the monoxenic cycle. Humans acquire the disease through fecal-oral transmission by ingesting food or water with infective eggs from infected rodents. This report presents 3 cases of hymenolepiasis in children, due to zoonotic transmission from rodents and presumably associated with the consumption of powdered milk contaminated with infective eggs of Hymenolepis nana, and shows that awareness and early diagnosis contributed to timely treatment of the disease.

CASE REPORT: Three children, aged 9, 12, and 13 years, living in a marginal urban area of Guayaquil, Guayas province, Ecuador, presented symptoms of diarrhea, low body weight, abdominal discomfort, anorexia, paleness, and anal itching. Subsequently, their fecal samples were analyzed by direct coproparasitic methods, flotation and sedimentation with centrifugation using saline solution; the presence of H. nana eggs was determined. Blood biometry was performed. Further, 10 rodents were captured and necropsied to obtain intestinal contents. The powdered milk consumed by the children was analyzed, the same powder that contained rodent feces. Subsequently, these were studied with the above-mentioned coproparasitic methods. H. nana eggs were identified in the 6 trapped rodents, the powdered milk, and the feces of rodents found in the milk powder.

CONCLUSIONS: Hymenolepiasis can affect populations of endemic areas. In this case, the disease was identified in 3 children, who were diagnosed with eosinophilia and anemia. Additionally, the presence of H. nana eggs in captured rodents and in powdered milk was determined, indicating that the community was exposed to this zoonotic disease.

Keywords: Hymenolepis Nana, Hymenolepiasis, rodents, Zoonoses, children, Child, Animals, Humans, Hymenolepiasis, Rodentia, Ecuador, Powders, Prevalence, Zoonoses

Background

Hymenolepiasis is a neglected zoonotic disease that affects humans and is caused by the tapeworms Hymenolepis nana [1] (dwarf tapeworm) and Hymenolepis diminuta [2] (rat tapeworm), whose definitive hosts are rodents [3]. However, H. nana is the most common cause of all tapeworm infections in humans and is a major cause of morbidity in developing countries, mainly in areas with poor hygiene and sanitation. It has a high prevalence in children up to 15 years of age, and it is estimated that there are between 50 and 75 million carriers worldwide [4]. Likewise, it has a cosmopolitan distribution with socioeconomic and medical importance and is endemic in Asia, southern and eastern Europe, Central and South America, and Africa [5]. The prevalence ranges from 5% to 25% of the population; however, in poor communities, the prevalence can reach up to 50% [1].

The adult H. nana parasite measures between 1.5 and 4 cm and consists of a scolex with 4 hooks, a neck, and a strobile with 150 to 200 proglottids. The proglottids contain the genital organs, with a lateral pore from which the eggs emerge (they measure between 30 and 47 µm). The egg contains an oncosphere with 3 pairs of hooks and are the infectious forms that come out along with the rodent’s feces [6].

Among the clinical manifestations caused by H. nana infection are headache, weight loss, weakness, anorexia, reduced growth, hives, anal itching, abdominal pain, nausea, irritability, skin rash, flatulence, bloating, and diarrhea [4,5]. Additionally, the parasite can affect pregnancy and neonatal health. Newborns exposed to intrauterine maternal infections have an increased risk of developing allergies, inflammation, and metabolic disorders [7]. The treatment for this parasitosis is praziquantel, in a single dose of 25 mg/kg [8]; as an alternative, niclosamide is used, in doses of 2 g per day for 7 days [6].

Hymenolepiasis occurs most frequently in hot, dry, and temperate regions of the world. Infection by H. nana preferably occurs after ingestion of food contaminated with infective eggs (fecal-oral transmission) and accidentally in a few cases by arthropod insects (beetles, fleas, and weevils) infected with cysticercoid larvae [4,8]. In the present study, 3 cases of infection by H. nana were diagnosed in children 9, 12, and 13 years old. The infections were due to parasitized rodents in a marginal urban area called “La Ladrillera” in Guayaquil, Ecuador. Findings demonstrated how awareness and early diagnosis contributed to the timely treatment of hymenolepiasis.

Case Reports

CLINICAL PRESENTATION, DIAGNOSIS, AND TREATMENT:

Boys of 9 and 12 years of age from the same home and a 13-year-old girl from a neighboring house were residents of the marginal urban area called “La Ladrillera” in Guayaquil, Ecuador. All 3 children presented with a history of diarrhea, low body weight, abdominal discomfort, anorexia, paleness, and anal itching of 2 days of evolution. They were treated on October 24, 2022, by researchers from the FCI-029 Project of the University of Guayaquil, called “Ecoepidemiology of the neglected intestinal helminthiasis in urban-marginal and rural areas of the province of Guayas”, in clinical practice. The presence of nearby H. nana cases then prompted the laboratory analysis that confirmed the diagnoses.

The informed consent of the children’s parents was requested before researchers proceeded. A blood sample was taken from all patients to perform a blood biochemical analysis, and then a stool sample was requested. They were instructed to obtain the sample and were provided with a sterile container. The blood and fecal samples obtained were transported on the day of collection in refrigerated boxes at 4 to 8°C to the Pazmiño Clinical and Microbiological Laboratory in the city of Milagro [9].

With respect to the blood samples, hematic biometry was performed on the 3 patients, yielding the following indices: patient 1 (age 9 years, male): white blood cells 5000 U/L, red blood cells 3.6 million U/L, hemoglobin 11 g/dL, hematocrit 32%, neutrophils 60%, lymphocytes 32%, monocytes 1%, basophils 1%, eosinophils 6%, and platelets 240 000 mm3; patient 2 (age 12 years, male): white blood cells 5900 U/L, red blood cells 3.7 million U/L, hemoglobin 11.2 g/dL, hematocrit 32%, neutrophils 62%, lymphocytes 33%, monocytes 1%, basophils 1%, eosinophils 6% and platelets 240 000 mm3; and patient 3 (age 13 years, female): white blood cells 5500 U/L, red blood cells 3.5 million U/L, hemoglobin 11.1 g/dL, hematocrit 31%, neutrophils 55%, lymphocytes 30%, monocytes 1%, basophils 1%, eosinophils 7.5% and platelets 230 000 mm3.

According to the laboratory reference values, the red blood cells, hemoglobin, and hematocrit were below normal values, which meant that the patients had anemia [10]. In the leukocyte count, the eosinophils were above the normal value, which was associated with the parasitosis that the children presented.

The fecal samples were analyzed by direct coproparasitic methods, flotation with supersaturated saline solution and sedimentation with centrifugation using saline solution [9], and the presence of infective eggs of H. nana was detected (Figure 1).

The morphology of the H. nana eggs of the observed patients was compatible with parasitic identifications described by the Centers for Disease Control and Prevention (2022) [11]. In direct questioning about the risk factors for hymenolepiasis infection, the children and their parents reported that they consumed powdered milk from a store in front of a sewage ditch. In addition, they reported that there are many rodents and possums in the area.

The patients were treated with praziquantel, administered in a single dose of 25 mg/kg. Fifteen days after treatment, none had symptoms, nor were infective eggs observed in the stool. A week later, they had made a full recovery.

IDENTIFICATION OF THE POTENTIAL SOURCE OF HYMENOLEPIASIS:

Rodent captures were made using Tomahawk and Sherman traps, and nontoxic baits (oats with peanuts and vanilla, meat, mortadella, fish, or tuna) placed at 6: 00 p.m. and collected at 6: 00 a.m.

These traps were strategically placed in intradomiciliary and peridociliary sites of the 2 houses where children infected with H. nana lived, as well as in the vicinity of a large drainage ditch and a store (suspected of having infected food) belonging to the sector of “La Ladrillera”. Ten rodents were captured, 2 inside the house (Rattus rattus), 2 peridociliary (Rattus novergicus), 4 from a sewage ditch (2 R. novergicus and 2 Mus musculus) and 2 inside the store (R. novergicus and M. musculus). Rodents captured alive were killed with pure chloroform soaked in cotton, which is the method suggested by the Institutional Animal Care and Use Committee of the Faculty of Veterinary Medicine and Zootechnics of the University of Guayaquil. Likewise, as a biosecurity standard for the professionals who performed the procedure, the captured rodents were sprayed with 0.15% fipronil before proceeding with the necropsy [12]. The digestive system of the rodents was extracted to locate parasites following the qualitative technique of Travassos [13]. The mucous membranes of the previously washed organs were examined to detect the parasites attached to or below the mucosa.

All the rodents captured from a sewage ditch and inside the store (6 of 10) were positive for H. nana (eggs and adult parasites), and these areas were near to where the infected children lived. However, the 4 captured rodents from the 2 houses studied (1 intradomiciliary and 1 peridociliary per house) did not determine the presence of any parasitic form of H. nana. The presence of H. nana in the intestinal content of rodents and in the feces of rodents contained in powdered milk was determined by sedimentation with centrifugation using saline solution and staining with lugol, and was then observed under an optical microscope using 10× and 40× objectives (Figure 2). The eggs were of the embryonated type, with a thin membrane, sized between 42 and 45 microns, and there was the presence of hooks and polar filaments, as described by Brar et al (2021) [14].

Later, human fecal samples of family members of the infected children and from neighbors of the sector “La Ladrillera” were analyzed through of the coproparasitic methods: direct, flotation and sedimentation with centrifugation using saline solution; however, the presence of H. nana was determined in none of them.

It is important to mention that the owner of the store was informed about the infection to take sanitary measures, and these were accepted and applied. Among the sanitary measures applied were cleaning and disinfection of the place, elimination of rodents, elimination of contaminated powdered milk, and education on the prevention of the disease.

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After 1 month of the applied treatment, a direct coproparasitic examination, flotation and sedimentation with centrifugation using saline solution, was performed, and the absence of the parasite was confirmed in all 3 cases [9]. The disease was also controlled by deworming infected children and conducting health education campaigns in which the impact of this parasite was explained. In addition, cleaning and disinfection of locations was carried out.

Discussion

Three cases of hymenolepiasis were diagnosed in children aged 9, 12, and 13 years old with specific symptoms, and this was the fifth report of such an infection in Ecuador. In 2013, a 6-year-old girl from the Sigsig canton and resident of a rural parish of San Joaquín in the city of Cuenca-Ecuador was diagnosed. She reported epigastric pain and lack of appetite and had physical developmental deficits, and H. nana infection was determined through direct coproparasitological examination [15]. In 2016, in a study on the prevalence of helminths and protozoa in 3 regions of Ecuador, out of a total of 295 fecal samples, various types of parasites were identified by direct coproparasitic methods and the Ritchie method. In addition, 2 cases of H. nana (1.16%) infection were determined in the coastal region [16].

Likewise, in 2017, two cases of H. nana infection were reported in 2 men from Quito, who presented symptoms including headache, nausea, vomiting, generalized abdominal pain, epigastric pain, neck pain, and arthralgia [6,17]. In a study carried out in the Primero de Noviembre citadel of the city of Jipijapa, of 105 children, ranging in age from 1 to 14 years, 1 child (0.95%) was positive for H. nana eggs. However, 6 cases (60%) of H. nana infection were determined in rodents from the studied area; however, in a rodent sampling in 2018, out of 87 captured and processed rodents, 20 cases (22.99%) of H. nana infection were determined in a marginal urban area of the city of Milagro, according to Coello et al [2]. Solorzano et al [18], in urban and rural areas of 5 provinces of Ecuador, determined that out of 191 animals sampled, 10 were positive (5%) for H. nana. Over time, if not addressed, these high levels could lead to a public health problem, as the town of “La Ladrillera” has favorable conditions for the transmission cycle of this parasitic disease. Therefore, as shown by these case reports of hymenolepiasis in children and the study of the local prevalence of H. nana in rodents, this zoonosis is active in rodents, powdered milk, and humans.

The prevalence in children varies by region, including Europe (0.5–5%), Asia (0.2–28.4%), Africa (1.8–2.9%), and the Americas (0.9–23%) [19]. In North America (1%), Mexico 7.8% [20], Central America (2–25%) [21], and South America, the following prevalences were recorded: Brazil 2.3% [22], Peru 7.6–37.5% [19], Argentina 7.8% [23], Venezuela 14% [24], and Bolivia 29–78% [25].

The hematologic parameters determined in the 3 patients of the present report are related to cases of anemia reported by Almeida and Cedeño, who described the following hematologic indices in a parasitized 11-year-old boy: white blood cells 5900 U/L, red blood cells 3.6 million U/L, hemoglobin 10.6 g/dL, hematocrit 33%, neutrophils 62%, lymphocytes 30%, monocytes 1%, basophils 1%, eosinophils 6%, and platelets 240 000 mm3; according to the reference values of the laboratory, the red blood cells, hemoglobin, and hematocrit were below the normal value, which means that the patient had anemia. Likewise, Terán et al, in children aged between 6 and 12 years old, reported anemia with hematocrit values of 26% and hemoglobin of 13.9 g/dL. Further, Ikumapayi et al described a 29-month-old boy with mild anemia, with a hemoglobin value of 10.8 g/dL, and an iron deficiency, with ferritin of 12.9 µg/L [4,17,25].

H. nana has been recorded in brown rats (Rattus norvegicus) from many countries, including the Netherlands (3.3–4.1%), China (3.3–10.3%), Brazil (8.8%) [3], Ecuador (5–18%) [2,18], Taiwan (21.8%), and Italy (100%) [3].

The 25 mg/kg therapy in a single oral dose of praziquantel was effective in eliminating the infection in the 3 reported cases, similar to the reports of Loján et al in Quito, Ecuador, and Ikumapayi et al in Gambia, Africa [4,6].

Hymenolepiasis is a neglected tropical parasitic disease. Although preventive chemotherapy eliminates current infections, it does not necessarily prevent reinfections. This could be attributed to various factors, such as poor sanitation, overcrowding, poor hygiene, poor nutrition, and age. Overcrowded families in impoverished rural and urban areas could act as foci of intestinal helminth infections despite preventive chemotherapy. Overcrowding is a contributory factor in the transmission of the infection between humans and the maintenance of the parasite in the environment. Therefore, laboratory diagnosis and preventive chemotherapy are essential, especially among the susceptible population, to prevent infections or at least reduce the prevalence of the parasite [7].

The patients in this study had consumed powdered milk in which infective eggs of H. nana were identified, of which there are few reports worldwide; however, Aceituno and Quispe in 4 markets in Santa Cruz de la Sierra, Bolivia, identified H. nana eggs in 8% of flour with the same methods applied in the present study [26]. In addition, the infected children came from families of low socioeconomic status. It can be presumed that there is a risk of the disease appearing in neighboring sectors, since they have adequate conditions for the biological cycle of hymenolepiasis to take place.

Conclusions

Hymenolepidiasis is a zoonotic disease that can affect the population in endemic areas. In this case report, the pathology and the presence of H. nana eggs were identified in 3 children, in the intestinal content of necropsied rodents, in feces of rodents contained in powdered milk, and in powdered milk for consumption, indicating that the community was exposed to a significant environmental risk due to this zoonotic pathology. Therefore, the population must be educated about sanitary measures and must eliminate rodents to prevent the transmission of these diseases.

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American Journal of Case Reports eISSN: 1941-5923
American Journal of Case Reports eISSN: 1941-5923