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Industry: Email Alert RSS FeedDengue emergence and adaptation to peridomestic mosquitoes
Emerging Infectious Diseases, Oct, 2004 by Abelardo C. Moncayo, Zoraida Fernandez, Diana Ortiz, Mawlouth Diallo, Amadou Sall, Sammie Hartman, C. Todd Davis, Lark Coffey, Christian C. Mathiot, Robert B. Tesh, Scott C. Weaver
Phylogenetic evidence suggests that endemic and epidemic dengue viruses (DENV), transmitted among humans by the anthropophilic mosquitoes Aedes aegypfi and Ae. albopictus, emerged when ancestral, sylvatic DENV transmitted among nonhuman primates by sylvatic Aedes mosquitoes adapted to these peridomestic vectors. We tested this hypothesis by retrospectively examining evidence for adaptation of epidemic and endemic versus sylvatic strains of DENV-2 to Ae. albopictus and Ae. aegypti. First and second-generation offspring of mosquitoes from different geographic regions in the Americas and Southeast Asia were tested for their susceptibility to epidemic/endemic and sylvatic DENV-2 isolates from West Africa, Southeast Asia, and Oceania. Both Aedes species were highly susceptible (up to 100% infected) to endemic/epidemic DENV-2 strains after ingesting artificial blood meals but significantly less susceptible (as low as 0%) to sylvatic DENV-2 strains. Our findings support the hypothesis that adaptation to peridomestic mosquito vectors mediated dengue emergence from sylvatic progenitor viruses.
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Dengue is caused by any of four antigenically distinct serotypes of dengue virus (DENV), family Flaviviridae. An estimated 100 million annual dengue cases occur each year in tropical cities, in which more than 2.5 billion people (almost half of the global population) are at risk (1). Infection with one DENV serotype confers lifelong protection against homologous reinfection, while a subsequent heterologous infection increases the likelihood of a more severe form of the disease (2-4).
Dengue has four clinical manifestations: 1) undifferentiated illness, 2) classic dengue fever, 3) dengue hemorrhagic fever, and 4) dengue shock syndrome. Undifferentiated dengue, the most common syndrome, occurs when a DENV infection is asymptomatic or mildly symptomatic. Dengue fever involves an abrupt febrile illness lasting 2-7 days, accompanied by malaise, headache, retroorbital pain, myalgia, and arthralgia of such great intensity that it has earned the lexicon "break-bone" fever (5,6). Dengue hemorrhagic fever progresses to hemorrhagic manifestations and plasma leakage caused by increased vascular permeability. Dengue shock syndrome is characterized by circulatory failure and is the most lethal dengue syndrome (7).
Within forest habitats of West Africa, Malaysia, and probably Vietnam, zoonotic, sylvatic dengue cycles have been described involving Aedes spp. mosquitoes and monkeys (8-10). Sylvatic DENV vectors in Africa include Aedes (Stegomyia) africanus, Ae. (S.) luteocephalus, Ae. (S.) opok, Ae. (Diceromyia) taylori, and Ae. (D.) furcifer (10); in Malaysia, Ae. niveus has been implicated in transmission (8,9). These sylvatic cycles, probably involving only DENV-2 in West Africa but all four serotypes in Malaysia, are believed to represent the ancestral DENV cycles from which epidemic/endemic (henceforth referred to as endemic) strains of DENV-1-4 evolved independently hundreds to thousands of years ago (11). Although humans occasionally become infected with sylvatic DENV in West Africa and perhaps in Asia, they are tangential to the maintenance cycle, which involves sylvatic Aedes spp. mosquito vectors and nonhuman primates as reservoir hosts. In contrast to the sylvatic cycles, epidemic DENV cycles involving transmission among humans by Ae. (Stegomyia) aegypti, Ae. (S.) albopictus, and other anthropophilic Aedes species have emerged in large tropical urban cities (12). These urban cycles are ecologically and evolutionarily independent of the ancestral sylvatic cycles, with humans serving as reservoir hosts.
Dengue is a reemerging disease in the neotropics and is transmitted primarily by Ae. aegypti. The abundance in Africa of closely related Aedes species within the Stegomyia subgenus, the lack of closely related Stegomyia species in the Americas, and the existence of sylvatic Ae. aegypti (Ae. aegypti formosus) in Africa suggest an African origin for this species (13-17). Movement of people and their requisite water storage containers during the 17th to 19th centuries probably spread Ae. aegypti throughout the tropics and subtropics. After World War II, Ae. aegypti prevalence and distribution increased in Asia and the Pacific Islands. Ae. aegypti was partially eradicated from tropical America in the 1940s and 1950s, but peridomestic Ae. aegypti aegypti has now reinfested most of the neotropics (12).
The Asian tiger mosquito, Ae. albopictus, originally of sylvatic origin as well, has spread widely in the world since the 1970s, including to the United States, Latin America, tropical Africa, the Pacific Islands, and Europe (7). Although less anthropophagic than Ae. aegypti, it is a secondary vector of DENV and possibly of greater importance in the early historical stages of urban dengue emergence.
We hypothesized that all four endemic dengue viruses evolved independently from sylvatic progenitors by adaptating to peridomestic mosquito vectors and human reservoir hosts (11). The rise of urban civilizations and the associated peridomestication of Ae. aegypti and Ae. albopictus mosquitoes provided this opportunity for adaptation and resulted in the emergence of dengue in urban areas of the tropics. This hypothesis predicts that endemic DENV strains are more efficient at infecting urban mosquitoes such as Ae. aegypti and Ae. albopictus than are the ancestral, sylvatic DENV strains. We tested this hypothesis by using experimental infections of Ae. aegypti and Ae. albopictus with sylvatic versus urban strains of DENV-2. Our results support the hypothesis that adaptation to peridomestic mosquito vectors mediated dengue emergence from sylvatic progenitor viruses.