EPIDEMIOLOGY OF CHAGAS DISEASE

By: João Carlos Pinto Dias (in: Chagas Disease - American Trypanosomiasis: its impact on transfusion and clinical medicine. S. Wendel, Z. Brener, M.E. Camargo, A. Rassi (Edt.). ISBT BRAZIL'92, SAO PAULO, BRAZIL).

INTRODUCTION

American trypanosomiasis (Chagas disease) is a protozoan infection caused by the flagellate Trypanosoma (Schizotrypanum) cruzi, widespread in the American Continent chiefly among small wild mammals (enzootic sylvatic cycle). Human Chagas disease constitutes a more recent situation, in which bio-ecological and socioeconomic factors leave rural poor populations of South and Central America in contact with the sylvatic cycle, where the parasite is transmitted by natural vectors of the infection. From the Public Health standpoint, the importance of Chagas disease remains correlated to this so-called "domestic" cycle, not only because millions of human beings are involved but also because all the available control measures are directed against it.

T. cruzi can be detected over a wide area of America, from latitude 42 N to latitude 46 S. Although the distribution of wild vectors and reservoirs is much greater than that of the human disease. The "domiciliation" of the triatomines exposes at least 90 million persons at risk of the infection, from south of the Unites States of America to the province of Chubut, Argentina. Nevertheless, the better living standard of the population and the conditions of the local species of triatomines make the human infection by the vector extremely rare in the United States. In endemic countries, it is estimated that 16-18 million people are infected by the parasite, excluding Mexico and Nicaragua, from which adequate data are not available. Chagas disease is not an isolated problem among Latin American populations. In endemic areas it is closely associated with typical "social" diseases such as malnutrition, diarrhoea, tuberculosis and other parasitic disease that both limit, and more limited by, the general context in which they occur. Classically considered as a typical rural disease of Latin America, a new trend is modifying the spectrum of human American Trypanosomiasis in all the Continent: that of urbanization.

Profound economic and social changes in the last four decades are stimulating rural- urban migration in most of endemic areas, with more than 60% of the population presently settled in urban centers. It is estimated that, because of migration, about 300.000 infected individuals are living today in the city of São Paulo and more than 200.000 in Rio de Janeiro and in Buenos Aires. In addition, chagasic patients are migrating northward to the USA and even eastward to Europe: nowadays, around 100.000 infected individuals are living in the USA, most of them immigrated from Mexico and Central America.

The medical and social impact of Chagas disease is high. For instance, it is estimated that about 752.000 of working years per year are lost due premature deaths caused by disease in the seven southernmost American countries, corresponding to 1208.5 US$ million/year. On the other hand, and only for Brazil, considering that at least 10% of infected people develop severe cardiac or digestive chronic involvement, the medical costs for their obligatory treatment could reach US$ 250.000 million. Similarly, the minimum absenteeism of 75.000 Brazilian chagasic workers with serious cardiac damage could represent minimum losses of US$ 5.625,00 per year.

Chagas disease in blood transfusion is also an increasing problem in Latin America. Since the 1950's, many scientific papers have shown that the transmission of T. cruzi by blood transfusion from infected donors is extremely frequent in some endemic areas. Natural non- vector transmission of the parasite involving congenital and oral routes can also occur in both sylvatic and domestic cycles, while transfusional transmission is an artificial mechanism depending on socio-epidemiological situations and directly linked with the quality of the health system in endemic countries. The comprehension of the epidemiology of American Trypanosomiasis is fundamental to understand and to control "transfusional" Chagas disease. The present chapter intends to summarize the main epidemiological aspects of the parasitosis, chiefly those which concern to the basic subject of this book.

SOCIO-ECOLOGICAL ASPECTS AND MODES OF TRANSMISSION

Basic framework: parasite, its cycle & reservoirs.

Trypanosoma (Schizotypanum) cruzi belongs to the Mastigophora subphylum of the phylum Sarcomastigophora, which comprises flagellar protozoans with an organelle that contains a mass of fibrous DNA, the kinetoplast. T. cruzi is included in the stercorarian group of trypanosomes which contaminate the vertebrate hosts throughout the vectors' feces. In the vector, the parasite is found in the digestive tract, also invading the Malpighian tubes, while in the vertebrate hosts it has two different phases, hematic and cellular.

The ancient sylvatic cycle of Chagas disease involves the interaction between wild vectors and hosts in different natural ecotopes of American Continent. In a general way, there is an ecological balance between the parasite and its vectors or hosts, since the parasitism seems not to harm triatomines or wild reservoirs. The domestic cycle results from human-vector contact, involving the colonization of artificial ecotypes by the invertebrate vector (triatomines) and a series of social and ecological modifications in the environment. In this latter cycle, parasitism can cause important damage in the vertebrate hosts, with high degrees of morbidity and mortality frequently detected among infected people. The interaction between domestic and sylvatic cycles occurs as a product of different factors, the majority of them dependent on human behavior. Two good examples that demonstrate the influence of ecological and social factors in human Chagas disease are:

The reservoirs of T. cruzi play a fundamental role in both sylvatic and domestic cycles of American Trypanosomiasis, as well as in the very dynamic interaction between them. Humans are the main reservoirs at the domestic side, followed by dogs, cats and domestic rodents, while numerous species of arboreal and terrestrial wild mammals have been found naturally infected by the parasite in all endemic areas. Infected synanthropic mammals like opossums and wild rodents frequently invade domestic and peridomestic areas where they are likely to increase the risk of human Chagas disease. Among domestic reservoirs, according to the ecology of the region and the habits of the people (Bolivia, Peru), some animals such as guinea-pigs can play a very particular role in the cycle, since they are very close to human beings. As a general rule, the parasite easily infects small mammals, chiefly the younger ones. Large mammals such as cows, horses and tapirs normally are not suspectible to infection. Pigs, sheep and goats (very frequent in all Latin America) may be found naturally infected, but their parasitemia usually is scarce and very transient. Birds are not susceptible to T. cruzi infection and their role in the ecology of Chagas disease is essential since they are the main source of blood meals for the majority of triatomine species. (The same occurs, in minor intensity, for poikilothermic vertebrates like frogs and lizards). Tables I and I-A summarize the main sylvatic and domestic natural reservoirs of T. cruzi in America.

The original landscape of human Chagas disease in all Latin America is composed of rural areas with huts covered by grass or palm leaves and constructed with mud, stones or wood cracked walls, sheltering a very poor human population living side by side with rats, mosquitoes, cockroaches and triatomines. Rural production is very primitive and devaluated in such areas, because of the absence of political priority, the lack of industries, the almost nonexistent transportation and the extreme difficulties of crop storage. The population is marked by illiteracy, poverty and weak social organization. In such situations, the failure of the productive system is the general rule and emigration to urban centers is the common survival strategy.

Current observation and mathematical models show that the social and political development of endemic regions is sufficient to achieve control of Chagas disease. But unlike other parasitic diseases, American Trypanosomiasis can also be controlled by three different and complementary strategies: a) the systematic elimination of domestic vector populations (chiefly by using insecticides of long residual action; b) housing improvement, and c) the control of transfusional Chagas disease. Among the 18 Latin America countries where the disease in endemic, regular national control programmes exist only in 4, even so frequently presenting enormous difficulties to keep the necessary continuity and the minimum coverage level. On the other hand, important ecological changes are occurring in most endemic regions, most of them resulting from anthropic action, with direct impact on the scenario of the disease. Human migration, extensive and intensive agricultural projects (involving mechanization, eletricity, pesticides and new patterns of labor relations), the reforestation of the areas with foreign species (Pinus, Eucalyptus), the construction of big dams, etc, are producing enormous impact over the sylvatic cycle, while the conquest of new agricultural frontiers (i.e. Amazon,) open new possibilities for expanding the domestic cycle of the disease.

Modes of transmission of American Trypanosomiasis

Considering the natural history of human Chagas disease the different routes or mechanisms of T. cruzi transmission are the following:

Vectorial transmission and the vectors of Chagas disease

The most important mechanism of transmission of T. cruzi to humans and other mammals is throughout the feces of infected triatomines. The vectors of Chagas disease are insects of the order Hemiptera, family Reduviidae and subfamily Triatominae. Of the 118 species of triatomines, a relatively small number are epidemiologically significant as vector of T. cruzi. These are species that colonize poorer quality rural houses, where colonies of hundreds of individuals (or even thousands) can be found. Other species are strictly inhabitants of different wild ecotopes and never invade houses, thus not representing any problem for the man. Between the two polar categories there is yet an important number of sylvatic species which leave their natural habitat and invade the domestic space and eventually transmit the parasite to man and/or domestic mammals.

The main domiciliated species are responsible for certainly more than 80% of the cases of human Chagas disease in endemic areas. These species (Triatoma infestans, T. brasiliensis, T. dimidiata, T. sordida, Panstrongylus megistus & Rhodnius prolixus) are characteristic of the so called "open"spaces of South and Central America, chiefly those poorer ones that were submitted to anthrop action. The vectorial transmission of T. cruzi to man and other mammals is basically due to the contact of these vertebrates with the feces of the infected vector, generally therewith the insect blood meal ("posterior" transmission). Nevertheless, in the sylvatic cycle, it is common that some insectivorous mammals such as monkeys and marsupials become infected through the ingestion of infected triatomines. The rate of vectorial transmission will be dependent on several factors, including the density of vectors, preferred food source, longevity, susceptibility to different parasite strains, capacity to defecate immediately after the blood meal, ability to yield and eliminate large numbers of T. cruzi. Other factors are the facility or difficulty for the parasite to penetrate the skin of mammalian hosts, age and immunological conditions of the vertebrate, irritability during the vector bite, etc. Generally, children and younger mammals are much more susceptible to vectorial contamination. On the other hand, there are also important environmental conditions: the majority of acute cases of human Chagas disease are detected during the summer time; triatomines generally are not detected over 3.000 meters; concentration of infected individuals, etc. Figure 3, shows the geographical distribution of the main vectors of human Chagas disease. From Mexico to Venezuela and Colombia, R. prolixus and T. dimidiata are the principal vectors, while T. infestants is undoubtedly the main source of human Chagas disease below the Equator line. The Amazon region appears as a real closed barrier between southern and northern endemic regions, in spite on the existence of wild vectors and reservoirs throughout the forest.

Most persons acquire Chagas disease when feces and urine of infected triatomines (in which numerous metacyclic forms of the parasite exist) enter in contact with either mucosa or skin. In different species of triatomines, the susceptibility to different T. cruzi strains seems to vary, and the capability of the parasite to induce differentiation metacyclic forms. Penetration of T. cruzi is easy in oral or eye mucosae. In normal skin the penetration does not seem to occur, unless in the exceptional case of very young children. In most of the cases the parasite penetrates throughout the puncture produced by the insect bite, or even by scratched skin (generally the bugs bite causes itching). In human Chagas disease, after the penetration, a short period of 7 to 9 days elapses until the beginning of the classical symptomatic acute phase (incubation period), in which the parasite undergoes an intensive process of tissue multiplication and invades the bloodstream and several organs. For practical purposes (in laboratorial accidents, for instance), a short treatment with the available drugs at this period will be sufficient to prevent the setting of the infection.

Infection acquired through blood transfusion

In human Chagas disease, this is the second most important mechanism of transmission of T. cruzi. In some endemic regions, such as the state of São Paulo, Brazil, where the vectorial transmission was controlled through an intensive and continuous Public Health Programme, blood transfusion is now the main route of transmission. Furthermore, human migration from endemic areas to urban centers is providing a rising risk of transfusional Chagas disease in all Latin America and even in non-endemic countries. Considering the high number of infected blood donors in all the Continent, it is estimated that thousands of new cases of transfusional Chagas disease may occur yearly.