Trypanosoma cruzi and Trypanosoma rangeli in Acre, Brazilian Amazonia: Coinfection and Notable Genetic Diversity in an Outbreak of Orally Acquired Acute Chagas Disease in a Forest Community, Wild Reservoirs, and Vectors

Abstract

Acute Chagas disease (ACD) caused by Trypanosoma cruzi has emerged as a major food-borne disease in Brazilian Amazonia. For the first time, we characterized an outbreak of orally acquired ACD in Acre, in the forest community of Seringal Miraflores, affecting 13 individuals who shared the pulp of açai palm berries: 11 adults and two children (one newborn), all diagnosed by thick-drop blood smears. The fluorescent fragment length barcoding method, which simultaneously identifies species/genotypes of trypanosomes in blood samples, uncovered an unprecedented genetic diversity in patients from a single outbreak of ACD: T. cruzi TcI in all patients, mostly concomitantly with the non-pathogenic Trypanosoma rangeli of genotypes TrA or TrB, and TcI, TcIV, and TrB in the child. The patients presented persistent fever, asthenia, myalgia, edema of the face and lower limbs, hepatosplenomegaly and, rarely, cardiac arrhythmia. The clinical symptoms were not correlated to gender, age, or to trypanosome species and genotypes. The inferred SSU rRNA phylogenetic analyses of trypanosomes from humans, triatomines and sylvatic hosts included the first sequences of T. cruzi and T. rangeli from humans in southwestern (Acre and Rondônia) Amazonia, and the first TcI/TcIV sequences from Rhodnius spp. from Acre. The sylvatic transmission cycles of genetically different trypanosomes in landscapes changed by deforestation for human settlements and increasing açai production is a novel scenario favoring trypanosome transmission to humans in Acre.

Assessment of Cross-Reactivity of Chimeric Trypanosoma cruzi Antigens with Crithidia sp. LVH-60A: Implications for Accurate Diagnostics

“…In the case of human T. cruzi infection, cross-reactivity has been reported with a range of pathogens, including toxoplasmosis, dengue, filariasis, schistosomiasis, measles, rubella, HIV-1/2, HTLV-1/2, HBV, HCV, syphilis, Zika virus, Hanseniasis, tuberculosis, autoimmune diseases, and leishmaniasis, as previously reported [25,32,40,42]. Few investigations have reported cross-reactivity for T. rangeli [25,40,41] and T. evansi [42], while no studies have explored cross-reactivity among Crithidia, Herpetomonas, Blastocrithidia, Leptomonas, or Crithidia sp. LVH-60A.…”

“…Cross-reactivity occurs when antibodies produced in response to one pathogen mistakenly recognize antigens from another, resulting in false-positive or inconclusive results. The challenges in diagnosing CD are further amplified when considering Trypanosoma rangeli [25,40,41], Trypanosoma evansi [42], and other members of the Trypanosomatidae family, including Crithidia, Herpetomonas, Blastocrithidia, and Leptomonas genera, as well as newly discovered species like Crithidia sp. LVH-60A [34].…”

First report of Rhodnius stali Lent, Jurberg & Galvão, 1993 (Hemiptera: Reduviidae: Triatominae), vector of Trypanosoma cruzi (TcI) and Trypanosoma rangeli (TrA), in Rondônia, Southwestern Brazilian Amazonia

“…For the identification of trypanosome species, the Fluorescent Fragment Length Barcoding (FFLB) method was used, which presents high sensitivity and precision in distinguishing species/genotypes of trypanosomes simultaneously (as in mixed infection) [ 20 ].…”

“…The DTUs TcI, TcIII, TcIV, and TcV genotypes of T. cruzi were related to oral outbreaks of acute Chagas disease (ACD) in Brazil, Colombia, Venezuela, Bolivia, and French Guiana [ 33 ]. In Brazil, there is a predominance of TcI and TcIV in oral transmission in the Amazon region [ 12 , 13 , 20 , 34 , 35 ]. T. rangeli is non-pathogenic to humans but is epidemiologically relevant as it can cause false-positive results in xenodiagnosis of triatomines, and microscopical and serological tests used to diagnose T. cruzi infection [ 36 , 37 ].…”

“…This species is widespread in Brazilian Amazonia, where three (TrA, TrB and TrE) of the five known genotypes are transmitted by Rhodnius spp. to a range of wild mammals, domestic dogs, and humans (Maia da Silva et al, 2007; Dario et al, 2021; [ 20 ].…”