Oral Outbreak of Chagas Disease in Santa Catarina, Brazil: Experimental Evaluation of a Patient’s Strain

Abstract

Chagas disease is a worldwide public health problem. Although the vectorial transmission of Chagas disease has been controlled in Brazil there are other ways of transmission, such as the ingestion of T. cruzi contaminated food, which ensures the continuation of this zoonosis. Here, we demonstrate the influence of the inoculation route on the establishment and development of the SC2005 T. cruzi strain infection in mice. Groups of Swiss mice were infected intragastrically (IG) or intraperitoneally (IP) with the T. cruzi SC2005 strain derived from an outbreak of oral Chagas disease. The results revealed that 100% of IP infected mice showed parasitemia, while just 36% of IG infected showed the presence of the parasite in blood. The parasitemia peaks were later and less intense in the IG infected mice. Mortality of the IP infected animals was more intense and earlier when compared to the IG infected mice. In the IP infected mice leucopenia occurred in the early infection followed by leucocytosis, correlating positively with the increase of the parasites. However, in the IG infected mice only an increase in monocytes was observed, which was positively correlated with the increase of the parasites. Histopathological analyses revealed a myotropic pattern of the SC2005 strain with the presence of inflammatory infiltrates and parasites in different organs of the animals infected by both routes as well as fibrosis foci and collagen redistribution. The flow cytometric analysis demonstrated a fluctuation of the T lymphocyte population in the blood, spleen and mesenteric lymph nodes of the infected animals. T. cruzi DNA associated with the presence of inflammatory infiltrates was detected by PCR in the esophagus, stomach and intestine of all infected mice. These findings are important for the understanding of the pathogenesis of T. cruzi infection by both inoculation routes.

Oral Versus Intragastric Inoculation: Similar Pathways of Trypanosoma cruzi Experimental Infection? From Target Tissues, Parasite Evasion, and Immune Response

“…As demonstrated in Domingues and colleagues study, the peak of parasitemia in GI at 18 dpi is correlated with an increase in monocytes in the blood. The spleen also increases in GI, mainly CD8 + cells and double-positive CD8 + CD4 + , but at a later time and the thymus is slightly increased instead of the atrophy observed after IP ( 70 ). High levels of IL-12, IL-10, and GM-CSF are expressed in the spleen during the acute phase of CL strain-infected mice, while IFN-γ, TNF-α, IL-6, IL-4, IL-9, CCL3/4, CXCL9, CXCL10, GM-CSF, IL-2, and IL-7 are elevated during chronic infection ( 79 ).…”

“…More importantly, especially in Brazil and other endemic countries, the most frequent transmission route has been reported to be by ingestion of contaminated food and beverages ( 7 , 17 , 66 , 67 ). Several approaches to address oral infection in mice have been described in the literature, such as intrapharyngeal, intragastric, and in the oral cavity inoculation ( 37 , 44 , 45 , 51 , 68 – 70 ).…”

“…Still, OI leads to parasitemia and mortality levels higher than in GI models. Infection through gavage (intragastrically) presents less percentage of mice with patent parasitemia, parasitemia, and mortality than IP injection ( 51 , 70 ). Despite intermediate parasitemia and mortality levels between GI and IP, OI infection leads to a percentage of mice with patent parasitemia similar to IP (49.3% for GI and 97.5% for OI) ( 51 ).…”

“…High levels of IL-12, IL-10, and GM-CSF are expressed in the spleen during the acute phase of CL strain-infected mice, while IFN-γ, TNF-α, IL-6, IL-4, IL-9, CCL3/4, CXCL9, CXCL10, GM-CSF, IL-2, and IL-7 are elevated during chronic infection ( 79 ). The mesenteric lymph nodes decrease in GI with reduction of CD4 + cells ( 70 ). Of note, the only study addressing lymphoid organ alteration after oral infection (oral cavity inoculation) reports an increase of gastric lymph nodes ( 37 ).…”

The Role of Co-Stimulatory Molecules in Chagas Disease

“…In addition to vector transmission, the parasite can be transmitted to humans through blood transfusion, organ transplantation, laboratory accidents, congenitally, and through ingestion of food contaminated with trypomastigote forms of T. cruzi [ 11 , 12 , 13 ]. These forms of transmission are responsible for the introduction and maintenance of Chagas disease in non-endemic regions and contribute to the persistence and re-emergence of the disease in endemic countries [ 14 , 15 ]. Oral infection currently represents the most prevalent transmission route in Brazil [ 11 , 16 ].…”