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First reported case of clinical fascioliasis in Santa Catarina, Brazil

Abstract

Fascioliasis is a food-borne anthropozoonotic disease caused by Fasciola hepatica that affects multiple hosts, including humans. We herein report the first case of human fascioliasis in the state of Santa Catarina, Brazil. A 57-year-old female patient complaining of abdominal pain was admitted to the hospital for a clinical investigation. The diagnosis of F. hepatica was confirmed by ultrasound and indirect enzyme-linked immunosorbent assay. Authorities of the Northern coast of Santa Catarina were notified to investigate other cases and risk factors for contamination. The disease is also prevalent in cattle, which could pose as a potential route for infection.

Keywords:
Fasciola hepatica; Liver fluke; Neglected zoonosis

INTRODUCTION

Human fascioliasis generally occurs after the ingestion of metacercaria, the encysted form of the trematode parasite Fasciola spp. This infective form can be found attached to plants or in water11. Ashrafi K, Bargues MD, O’Neill S, Mas-Coma S. Fascioliasis: A worldwide parasitic disease of importance in travel medicine. Travel Med Infect Dis. 2014;12(6):636-49.. The incubation period starts after ingestion and is followed by acute and chronic clinical phases. The acute phase includes fluke migration to the bile ducts for about 2-4 months. During the chronic phase, adult worms attach themselves on the bile ducts, leading to months or years of persisting infection22. Mera Y Sierra R, Agramunt VH, Cuervo P, Mas-Coma S. Human fascioliasis in Argentina: Retrospective overview, critical analysis and baseline for future research. Parasit Vectors. 2011;4(1):1-18.,33. Mas-Coma S, Bargues MD, Valero MA. Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol. 2005;35(11-12):1255-78..

In Brazil, declaration of fascioliasis is not compulsory; therefore, only 48 cases of human infection have been reported in scientific papers between 1950 and 201644. Pritsch IC, Molento MB. Recount of reported cases of human fascioliasis in Brazil over the last 60 years. Rev Patol Trop. 2018;47(2):75-85.. Combined with the challenges of an accurate diagnosis, this results in only a small number of reported cases leading to a considerable underestimation of the actual, putatively much larger number of subjective cases44. Pritsch IC, Molento MB. Recount of reported cases of human fascioliasis in Brazil over the last 60 years. Rev Patol Trop. 2018;47(2):75-85.. To the best of the authors’ knowledge, the last case of fascioliasis in Brazil reported in the literature was from Amazonas state in 2018, where 36 (8.3%) human serum samples were reactive in enzyme-linked immunosorbent assays (ELISAs), 8 (1.8%) of which were also positive in Western Blot experiments, and only 1 fecal sample was positive in the F. hepatica coprological test55. Maciel MG, Lima WDS, Almeida FLM, Coelho LIARC, Araújo GAN, Lima MG, et al. Cross-Sectional Serological Survey of Human Fascioliasis in Canutama Municipality in Western Amazon, Brazil. J Parasitol Res. 2018;(2018):1-8..

The under-reporting of human fascioliasis cases stem from both the difficulty in performing a proper diagnosis and the lack of knowledge on fascioliasis by health care professionals33. Mas-Coma S, Bargues MD, Valero MA. Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol. 2005;35(11-12):1255-78.,66. Webb CM, Cabada MM. Recent developments in the epidemiology, diagnosis, and treatment of Fasciola infection. Curr Opin Infect Dis. 2018;31(00):1-6.. Considering these challenges, frequent reporting of fascioliasis cases such as the present case will aid local authorities by allowing them to take necessary preventive measures. Thus, the availability of case reports is of importance for local healthcare providers, particularly when it comes to such a neglected disease. This work is the first human fascioliasis case to be reported in the state of Santa Catarina in the South of Brazil, an area where the occurrence of bovine fascioliasis is well established77. Aleixo MA, Freitas DF, Dutra LH, Malone J, Martins IVF, Molento MB. Fasciola hepatica: Epidemiology, perspectives in the diagnostic and the use of geoprocessing systems for prevalence studies. Semin Cienc Agrar. 2015;36(3):1451-65..

CASE REPORT

A 57-year-old woman from Balneário Piçarras, Santa Catarina, Brazil (Figure 1), was admitted to the local health unit with persistent abdominal pain. The patient had been admitted 15 days earlier to a hospital and had received stationary treatment for acute abdominal pain followed by fever and acute jaundice (yellowing of the skin) for 5 days. An ultrasound examination revealed a hepatic cyst and a small hemangioma nodule. She was treated with non-specific antibiotics and showed signs of clinical improvement. Nevertheless, the patient had recurring pain episodes after a few days and therefore sought another consultation where she was submitted to another ultrasound examination. Although the liver showed a normal parenchyma, a hepatic cyst of 2.6 cm in size was detected. The absence of lithiasis was also observed.

FIGURE 1:
Map of the State of Santa Catarina, Brazil, indicating the location of the city of Balnéario Piçarras.

The liver function findings were as follows: 66 U/L aspartate transaminase [normal: <31 U/L], 150 U/L alanine transaminase [normal: <32 U/L], 159 U/L alkaline phosphatase [normal: 27-100 U/L], 106 U/L gamma-glutamyl transferase [normal: 5-32 U/L], a normal total bilirubin level, persistent eosinophilia, and elevated values in tests for inflammation.

She returned to the hospital after 4 months with a mild but recurrent abdominal pain. The possibility of F. hepatica infection was suspected after a hepatic capsule rupture was observed in magnetic resonance imaging (MRI) scans (Figure 2A and 2B). For this reason, a blood sample (serum) was collected for screening with anti-F. hepatica antibodies using an indirect ELISA. The ELISA method presents a sensitivity and specificity of 99.9%, and employs a F. hepatica cathepsin L1 recombinant protein as an antigen88. Santana BG, Dalton JP, Camargo FV, Parkinson M, Ndao M. The Diagnosis of Human Fascioliasis by Enzyme-Linked Immunosorbent Assay (ELISA) Using Recombinant Cathepsin L Protease. PLoS Negl Trop Dis. 2013;7(9):e2414.. The immunological test confirmed the presence of anti-F. hepatica IgG antibodies.

FIGURE 2:
Nuclear magnetic resonance images of (A) the main coronal contrast and (B) the axial contrast. The arrows point to the lesions formed by the presence of the adult Fasciola hepatica parasite.

Unfortunately, despite multiple attempts to contact the patient, she did not return to receive the required follow-ups and treatment. This study was approved by the ethics committee of the Federal University of Parana (CAAE number 50984215.0.0000.0102).

DISCUSSION

The life cycle of F. hepatica is heteroxenous where hosts of different species are required for its entire life cycle to be completed. The intermediary hosts are snails that belong to the lymnaeidae family, while the most common definitive hosts are livestock animals and humans33. Mas-Coma S, Bargues MD, Valero MA. Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol. 2005;35(11-12):1255-78.. These multiple F. hepatica hosts make it almost impossible to eradicate fascioliasis infection66. Webb CM, Cabada MM. Recent developments in the epidemiology, diagnosis, and treatment of Fasciola infection. Curr Opin Infect Dis. 2018;31(00):1-6..

The diagnosis of fascioliasis in humans is still a challenge, particularly in non-endemic regions, given that the disease is not recognized by health authorities and that there are numerous non-specific symptoms observed in infected people. In the acute phase of the disease, eosinophilia is the most common laboratory finding and was also observed in our case. Nonetheless, eosinophilia may not be detected in all human fascioliasis cases as it is only a general indication of parasitic infection33. Mas-Coma S, Bargues MD, Valero MA. Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol. 2005;35(11-12):1255-78.,66. Webb CM, Cabada MM. Recent developments in the epidemiology, diagnosis, and treatment of Fasciola infection. Curr Opin Infect Dis. 2018;31(00):1-6.. Although diagnostic methods based on coprological exams to search for parasite eggs are routinely used, they are time-consuming and have a low accuracy. Furthermore, the immunodiagnostic analysis based on ELISA is rarely used even for the validation of fascioliasis in Brazil (M. Molento, personal observation).

Triclabendazole (TCBZ) that effectively kills early immature and adult Fasciola liver flukes, is the drug of choice to treat fascioliasis in humans and animals. Although fascioliasis treatment with TCBZ is tolerated well and easily administered, the patient reported in the present case did not return to the healthcare unit to receive it. This episode should serve as a warning to demonstrate that educational health programs are required to inform the community about the risks of this parasitic disease.

Certain factors need to be considered regarding the risk of human infection, such as areas with a high incidence of fascioliasis in ruminants99. Perez-C JE, Giraldo-Pinzon EJ, Aguilar-Marín S. First Report of Human Fascioliasis in an Endemic Region of Bovine Fascioliasis in Caldas-Colombia. Vector Borne Zoonotic Dis. 2016;16(6):377-81.. Although there is no data confirming a correlation between human and animal fascioliasis in Brazil, there is a high prevalence of fascioliasis in cattle, in areas close to that of the present case (Joinville, Blumenau, Florianópolis, and Itajaí)77. Aleixo MA, Freitas DF, Dutra LH, Malone J, Martins IVF, Molento MB. Fasciola hepatica: Epidemiology, perspectives in the diagnostic and the use of geoprocessing systems for prevalence studies. Semin Cienc Agrar. 2015;36(3):1451-65..

This study reports the first case of human fascioliasis in Balneário Piçarras, an area with a high prevalence of animal fascioliasis77. Aleixo MA, Freitas DF, Dutra LH, Malone J, Martins IVF, Molento MB. Fasciola hepatica: Epidemiology, perspectives in the diagnostic and the use of geoprocessing systems for prevalence studies. Semin Cienc Agrar. 2015;36(3):1451-65.. The present case report highlights the need to alert the scientific and medical community, and local authorities to the occurrence of the disease in this region. As this hepatic infection is a food-borne disease, it is recommended that the community is provided with specific safety measures to ensure the proper sanitation of fresh vegetables (i.e., cress, arugula/rocket) and the consumption of clean potable water. These important preventive actions would considerably reduce the risk of disease transmission and improve the welfare of the population.

ACKNOWLEDGEMENTS

The authors wish to thank Coordenação de Aperfeiçoamento Pessoal de Nivel Superior (CAPES) and Prefeitura Municipal de Balneário Piçarras for their support. I. Pritsch was awarded a doctoral fellowship from CAPES.

REFERENCES

  • 1
    Ashrafi K, Bargues MD, O’Neill S, Mas-Coma S. Fascioliasis: A worldwide parasitic disease of importance in travel medicine. Travel Med Infect Dis. 2014;12(6):636-49.
  • 2
    Mera Y Sierra R, Agramunt VH, Cuervo P, Mas-Coma S. Human fascioliasis in Argentina: Retrospective overview, critical analysis and baseline for future research. Parasit Vectors. 2011;4(1):1-18.
  • 3
    Mas-Coma S, Bargues MD, Valero MA. Fascioliasis and other plant-borne trematode zoonoses. Int J Parasitol. 2005;35(11-12):1255-78.
  • 4
    Pritsch IC, Molento MB. Recount of reported cases of human fascioliasis in Brazil over the last 60 years. Rev Patol Trop. 2018;47(2):75-85.
  • 5
    Maciel MG, Lima WDS, Almeida FLM, Coelho LIARC, Araújo GAN, Lima MG, et al. Cross-Sectional Serological Survey of Human Fascioliasis in Canutama Municipality in Western Amazon, Brazil. J Parasitol Res. 2018;(2018):1-8.
  • 6
    Webb CM, Cabada MM. Recent developments in the epidemiology, diagnosis, and treatment of Fasciola infection. Curr Opin Infect Dis. 2018;31(00):1-6.
  • 7
    Aleixo MA, Freitas DF, Dutra LH, Malone J, Martins IVF, Molento MB. Fasciola hepatica: Epidemiology, perspectives in the diagnostic and the use of geoprocessing systems for prevalence studies. Semin Cienc Agrar. 2015;36(3):1451-65.
  • 8
    Santana BG, Dalton JP, Camargo FV, Parkinson M, Ndao M. The Diagnosis of Human Fascioliasis by Enzyme-Linked Immunosorbent Assay (ELISA) Using Recombinant Cathepsin L Protease. PLoS Negl Trop Dis. 2013;7(9):e2414.
  • 9
    Perez-C JE, Giraldo-Pinzon EJ, Aguilar-Marín S. First Report of Human Fascioliasis in an Endemic Region of Bovine Fascioliasis in Caldas-Colombia. Vector Borne Zoonotic Dis. 2016;16(6):377-81.
  • Financial support: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Publication Dates

  • Publication in this collection
    18 July 2019
  • Date of issue
    2019

History

  • Received
    09 Feb 2019
  • Accepted
    29 Apr 2019
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