Oral Transmission of Chagas Disease: New Epidemiology for an Old Disease

By Brian G. Blackburn, MD and Michele Barry, MD FACP

Dr. Blackburn is a Clinical Assistant Professor in the Division of Infectious Diseases and Geographic Medicine at Stanford University School of Medicine

Dr. Barry is the Senior Associate Dean for Global Health at Stanford University School of Medicine

Drs. Blackburn and Barry report no financial relationships to this field of study.

Synopsis: Several recent outbreaks of Chagas disease have been due to oral transmission. Although this protozoal infection is classically transmitted by triatomine insects, an emerging recognition of oral transmission could expand our understanding of the distribution for this parasitic infection.

Source: Shikanai-Yasuda MA, Carvalho NB. Oral transmission of Chagas disease. Clin Infect Dis. 2012;54:845-52.

Chagas disease is caused by the protozoan parasite Trypanosoma cruzi, endemic only to the Americas. Most cases occur in tropical Central and South America, typically in impoverished communities that impinge upon the rural transmission cycle of this organism. About 8 million people are infected, and transmission classically occurs through the bite of infected triatomines, a subfamily of large bloodsucking insects. Triatomines transmit the parasites through deposition of infected feces following their bites,; parasites are subsequently scratched into the bite wound or a mucous membrane. T. cruzi is perpetuated in the wild by a sylvatic transmission cycle between forest-dwelling mammals and triatomines. Human infection usually occurs when settlements impinge upon this sylvatic cycle, leading to disease predominance in rural areas. In addition, human infections occur commonly only in areas with substandard housing, given the preference of these insects to dwell in the nooks and cracks of mud-thatched houses.

In part due to urban migration in many Latin American countries, transmission has been recognized increasingly in urban and peri-urban areas. Although these insects are endemic to the United States, where a few autochthonously transmitted cases have been documented, vector-borne transmission in the U.S. is rare, in part because of high housing standards. Infection can also occur through blood transfusion, congenitally from mother to child, and rarely through laboratory accidents or organ transplantation. Overall, the incidence of Chagas disease has been on the decline in recent years due to better vector control and blood screening programs in endemic areas.

Most patients infected with T. cruzi remain asymptomatic; a minority develop acute Chagas disease, with symptoms such as fever, lymphadenopathy, hepatosplenomegaly, an erythematous, indurated chagoma at the entry site (or unilateral bipalpebral edema if the innoculation site is the conjunctiva – Romaña's sign), and detectable parasitemia. Acute and severe manifestations rarely occur (e.g., meningoencephalitis, myocarditis), which are fatal in 5-10% of symptomatic patients. Subsequently, most patients enter an asymptomatic indeterminate phase during which they are usually seropositive and sub-patently parasitemic. After years — decades, 10-30% progress to chronic Chagas disease; cardiac Chagas in most of those who develop chronic cardiac disease (e.g., arrhythmias, congestive heart failure, thromboembolism), and gastrointestinal (e.g., megaesophagus, megacolon) or mixed Chagas in others.

The clinical syndrome of orally-acquired Chagas disease is similar to that of vector-borne Chagas, which causes acute symptoms in <5% of infected patients, although the incubation period is longer for orally-acquired disease, and no chagoma nor Romana's sign are seen. The severity of the disease depends in part on the number of parasites ingested and the host's immune response. Treatment of acute Chagas disease is recommended in all recognized cases, preferably with benznidazole, or alternatively nifurtimox.

Commentary

Although oral transmission of T. cruzi has been described since at least the 1960s, the past decade has seen a dramatic increase in the number of described cases from oral transmission, often in the context of outbreaks. In areas where vector control programs are strong, oral transmission may be a particularly important means of spread to humans. From 2000-2010, over 1,000 acute Chagas disease cases were reported in Brazil, with 71% of these due to oral transmission; most were in areas with good vector control programs.

Although there were just three reported outbreaks of acute Chagas disease from 1968-2000, there have at least been ten since 2001. The largest two outbreaks each involved over 100 people. Overall nearly a dozen deaths occurred in these outbreaks, mostly due to myocarditis / heart failure. The outbreak sources included fruit juices (e.g., acai, guava, orange/ tangerine), sugarcane juice, water, food, and soup. In most cases, crushed triatomines probably contaminated the food/drink, but other sources were possible as well. In many outbreaks, it is likely that unsanitary preparation of food/drink allowed triatomine contamination; in addition, these insects are attracted to light, which may result in high triatomine densities where there is ongoing food preparation. Although sensitive to desiccation, T. cruzi appears able to survive in sugar cane juice for 24 hours, based on experimental inoculation studies. T. cruzi can also survive in acai juice for many hours, including at extremes of pH and temperature.

Although the vectors of T. cruzi are largely under control in some countries, eradication of Chagas disease is not feasible because of the zoonotic cycle of T. cruzi. In the Amazon, household colonization with triatomines generally does not occur, but the role of acai as a food source and the presence of humans impinging upon the sylvatic transmission cycle have been associated with T. cruzi propagation, and may explain why in such a high proportion of acute Chagas cases it appears to be orally-acquired. In other regions of Brazil, the opossum is a source of blood for triatomines, and can contribute to Chagas transmission. Infection can also occur in domestic animals which could perpetuate the transmission cycle in some areas where humans impinge upon T. cruzi transmission in forest border zones. Although the Amazon region has seen the most Chagas outbreaks to date, they have occurred both north and south of this region, including in urban areas.1,2

Oral transmission of Chagas represents an emerging means of transmission for this disease, and may continue to grow in importance as vector control programs render transmission due to triatomines less important in many areas. A need exists for health education in at-risk areas to diminish the risk of orally acquired Chagas disease.1 Implementation of measures such as crop cleaning to exclude insects, covering of presses and avoiding operations adjacent to artificial light, pasteurization of commercial acai juice, and keeping vulnerable juice preparations covered are some examples of preventative measures that could help prevent oral transmission of T. cruzi.

Several researchers have studied the importance of oral transmission of Chagas disease; however recent outbreaks associated with acai juice have garnered attention to foodborne contamination and transmission. Acute morbidity in orally transmitted infections appears to be more severe than among patients with vector-borne infections.3 In theory, undercooked meat from infected host reservoir animals could also pose risk for transmission, but laboratory data suggest the infectivity is lower than that for trypomastigotes in crushed triatomines or their feces.4

References

  1. Miles MA. Orally acquired Chagas disease: lessons from an urban school outbreak. J Infect Dis 2010;201:1282-4.
  2. Alarcón de Noya B, et. al. Large urban outbreak of orally acquired acute Chagas disease at a school in Caracas, Venezuela. J Infect Dis 2010;201:1308-15.
  3. Pereira KS, et. al. Chagas' disease as a foodborne illness. J Food Prot 2009;72:441-6
  4. Roellig DM, et, al. Oral transmission of Trypanosoma cruzi with opposing evidence for the theory of carnivory. J Parasitol 2009;95:360-4.