Distantiae transmission of Trypanosoma cruzi: a new epidemiological feature of acute Chagas disease in Brazil

Abstract

Background: The new epidemiological scenario of orally transmitted Chagas disease that has emerged in Brazil, and mainly in the Amazon region, needs to be addressed with a new and systematic focus. Belém, the capital of Pará state, reports the highest number of acute Chagas disease (ACD) cases associated with the consumption of açaí juice.

Methodology/principal findings: The wild and domestic enzootic transmission cycles of Trypanosoma cruzi were evaluated in the two locations (Jurunas and Val-de Cães) that report the majority of the autochthonous cases of ACD in Belém city. Moreover, we evaluated the enzootic cycle on the three islands that provide most of the açaí fruit that is consumed in these localities. We employed parasitological and serological tests throughout to evaluate infectivity competence and exposure to T. cruzi. In Val-de-Cães, no wild mammal presented positive parasitological tests, and 56% seroprevalence was observed, with low serological titers. Three of 14 triatomines were found to be infected (TcI). This unexpected epidemiological picture does not explain the high number of autochthonous ACD cases. In Jurunas, the cases of ACD could not be autochthonous because of the absence of any enzootic cycle of T. cruzi. In contrast, in the 3 island areas from which the açaí fruit originates, 66.7% of wild mammals and two dogs displayed positive hemocultures, and 15.6% of triatomines were found to be infected by T. cruzi. Genotyping by mini-exon gene and PCR-RFLP (1f8/Akw21I) targeting revealed that the mammals and triatomines from the islands harbored TcI and Trypanosoma rangeli in single and mixed infections.

Conclusion/significance: These findings show that cases of Chagas disease in the urban area of Belém may be derived from infected triatomines coming together with the açaí fruits from distant islands. We term this new epidemiological feature of Chagas disease as "Distantiae transmission".

Figure 1. Map of the spatial distribution of the Trypanosoma cruzi infections.

Mammals and triatomines collected in the Belém municipality, in the urban portion (Jurunas and Val-de-Cães) and on the islands (Combu, Murutucu and Pato). The pictures framed in red represent infections animals (positive cultures) among the triatomines, dogs and small mammals examined, and the pictures framed in yellow represent positive serology. On the left of the figure is the study site in Brazil, highlighting Pará state and the Brazilian and South American borders.

Figure 2. Trypanosoma cruzi genotyping of triatomine and mammalian isolates from the Belém/Pará, Brazil.

(A) PCR products of the mini-exon gene analyzed by electrophoresis on na agarose gel stained with ethidium bromide. Lanes: M. molecular-weight markers (100 bp DNA ladder); control samples: TcI (200 bp), TcII/TcV/TcVI (250 bp), TcIII/TcIV (150 bp), and T. rangeli (100 bp). (B) PCR-RFLP products of 1f8 gene/Alw21I. Control samples: PCR-RFLP 1f8/Alw21I digestion patterns of TcI to TcVI: 445, 450 and 068: triatomine isolates (Rhodinius pictipes from Combu, Murutucu and Val-de-Cães, respectively) characterized as TcI; 464: dog isolate characterized as T. rangeli; 465: dog isolate characterized as TcI; 473: Philander opossum isolates characterized as TcI; 451: P. opossum isolate characterized as a mixed infection of TcI/T. rangeli; and 463: P. opossum isolate characterized as T. rangeli.