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Human outbreaks of acute Chagas disease acquired by oral transmission

In humans, the possibility of oral transmission of T. cruzi has recently been considered a serious issue because microepidemic or epidemic episodes of acute Chagas disease have been increasingly reported in areas without domiciliated triatomines or with a low level of domestic infestation by triatomines. When various serious acute cases appear at the same time in a family or a community, or during a common meal (meetings, celebrations), systematic inquiry generally raises suspicion of an oral route of contamination and its origin. Several cases are reported below.

The first outbreak of acute Chagas disease due to oral transmission was reported in 1968124: 17 simultaneous cases with acute myocarditis occurred in March 1965, in a rural school from Teutonia, situated in Estrela, the Rio Grande do Sul state in Brazil. The inquiry showed that the first clinical signs appeared 13—19 days after the infection, and during this epidemic period, five people died before 40 days. The points suggesting oral transmission were (1) the occurrence of 17 serious cases at the same time; (2) the lack of cutaneous or mucosal injury in the patients; (3) the lack of triatomines in the school; and (4) the presence of a Didelphis spp. infected with T. cruzi in the school. Accordingly, the authors favored the hypothesis that food contaminated by the anal gland secretions of the opossum were ingested.

In the Amazon region, reports of acute cases due to oral transmission are more common. In October 1986, 7—22 days after a meeting at a farm in Catole do Rocha, in the Paraiba state in Brazil, 26 acute cases of Chagas disease were identified.125 The patients had a febrile illness associated with bilateral eyelid and lower limb edema, mild hepatosplenomegaly, lymphadenopathy, and occasionally a skin rash. One 74-year-old patient died. In this outbreak, it seemed that an infected opossum could have deposited infective anal gland secretions over the sugar cane crusher. Between 1988 and 2005, 233 cases including 183 (78.5%) during outbreaks (mean, four individuals), probably due to oral transmission, were reported in Para, Amapa, and Maranhao, Brazil.126 In these cases, the most frequent clinical signs were fever, headache, myalgia, pallor, dyspnea, swelling of the legs, facial edema, abdominal pain, myocarditis, and exanthema. These grouped cases appeared mostly in July (19 cases) and August (25 cases), with the highest numbers in October (40 cases) and November (43 cases). This seasonality raised the suspicion of the consumption of contaminated beverages as the source of oral transmission because at that time there was a very high production and consumption of different juices from palm tree fruits, sugar cane, and other sources. In 2005 in Santa Catarina, Brazil, sugar cane juice was implicated as the source of infection (24 cases and several deaths),127 while the consumption of agai, the fruit of a palm of the Aracaceae family, was reported to be the source of infection in several outbreaks in the Brazilian Amazon.128,129

Outside Brazil, where it is estimated that over 1500 patients in 6 states of the Amazon region have been infected through oral transmission,130 several outbreaks have been reported in Columbia and Venezuela,131-133 where the largest outbreak described occurred with 103 cases in the same school in Caracas city, 1 in French Guyana,134 and 1 in Bolivia.135 Through all these reports, the main sources of oral transmission were clearly the homemade fruit juices contaminated by infected tria- tomine feces or infected Didelphidae secretions.136 Note that the consumption of crude or undercooked meat of a T. cruzi-infected animal—even if very unusual and never evidenced—might also be a source of oral transmission.

The recent increase of oral transmission in the Amazon is related to the new scenarios of Chagas disease, which are related to the human impact on fauna and triatomines.7,131 Due to the deforestation associated with new human settlements, the forest balance of zoonotic cycles of T. cruzi is disturbed. The triatomines move in search of new hosts and new habitats to urban areas, most often attracted by lights. Accordingly, oral transmission should be considered in areas of humid tropical forest other than the Amazon, particularly those suffering from deforestation, because in this context, forest triatomine species may adapt to the anthropized medium. The approximation of the vectors to humans creates a situation of transmission risk, especially via the oral route.

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