Natural history

There are four dengue virus serotypes: DENV-1, DENV-2, DENV-3 and DENV-4. They belong to the genus Flavivirus, family Flaviviridae (of which yellow fever is the type species), which contains approximately 56 viruses (ICTV 2005).

Humans are infected with dengue viruses by the bite of an infective Ae. aegypti mosquito (Gubler 1988). Ae. aegypti is a small, black-and-white, highly domesticated urban mosquito that prefers to lay its eggs in artificial containers commonly found in and around homes in the tropics, for example, flower vases, old automobile tires, buckets that collect rainwater, and trash in general. Containers used for water storage, especially 55-gallon drums and cement cisterns, are especially important in producing large numbers of adult mosquitoes in close proximity to dwellings where people live and work. The adult mosquitoes prefer to rest indoors, are unobtrusive, and prefer to feed on humans during daylight hours. The female mosquitoes are very nervous feeders, disrupting the feeding process at the slightest movement, only to return to the same or a different person to continue feeding moments later. Because of this behaviour, Ae. aegypti females will often feed on several persons during a single blood meal and, if infective, may transmit dengue virus to multiple persons in a short period of time even if they only probe without taking blood (Gubler & Rosen 1976). It is not uncommon to see several members of the same household become ill with dengue fever within a 24 to 36 h time frame, suggesting transmission by a single infective mosquito (D. J. Gubler, unpublished data). It is this behaviour that makes Ae. aegypti such an efficient epidemic vector. Inhabitants of dwellings in the tropics are rarely aware of the presence of this mosquito, making its control difficult.

After a person is bitten by an infective mosquito, the virus undergoes an incubation period of 3—14 days (average, 4—7 days), after which the person may experience acute onset of fever accompanied by a variety of non-specific signs and symptoms. During this acute febrile period, which may be as short as 2 days and as long as 10, dengue viruses may circulate in the peripheral blood. If other Ae. aegypti mosquitoes bite the ill person during this febrile viraemic stage, those mosquitoes may become infected and subsequently transmit the virus to other uninfected persons, after an extrinsic incubation period of 8 to 12 days (Gubler 1988).

The disease pattern associated with dengue, which was characterized by relatively infrequent epidemics until the 1940s, changed with the ecological disruption in Southeast Asia during and after World War II. The economic development and urbanization in the post-war years created ideal conditions for increased transmission of mosquito-borne diseases, and in this setting a global pandemic of dengue began. With increased epidemic transmission and movement of people within and between countries, hyperendemicity (the cocirculation of multiple dengue virus serotypes) developed in Southeast Asian cities, and epidemic DHF, a newly described disease, emerged (World Health Organization 1997, Halstead 1980). The first known epidemic of DHF occurred in Manila in 1953-1954, but within 20 years the disease had spread throughout Southeast Asia. By the mid-1970s, DHF had become a leading cause of hospitalization and death among children in the region (World Health Organization 1997). In the 1980s and 1990s, dengue transmission in Asia further intensified; epidemic DHF increased in incidence and expanded geographically west into India, Pakistan, Sri Lanka, and the Maldives, and east into China (Gubler 1997, Halstead 1980, 1992, World Health Organization 1997). At the same time, the geographic distribution of epidemic DHF was expanding into new regions—the Pacific islands in the 1970s and 1980s and the American tropics in the 1980s and 1990s (Gubler 1993, 1997, Halstead 1992, 1980, Gubler & Trent 1994, Gubler & Clark 1995, Rosen 1982, Barnes & Rosen 1974, Guzman et al 1984, Pinheiro 1989).

Epidemiological changes in the Americas have been the most dramatic. In the 1960s and most of the 1970s, epidemic dengue was rare in the American region because the principal mosquito vector, Ae. aegypti, had been eradicated from most of Central and South America (Gubler 1987, 1989, 1997, 1993, Pinheiro 1989). The eradication program was discontinued in the early 1970s, and this species then began to reinvade those countries from which it had been eradicated. By the 1990s, Ae. aegypti had regained the geographic distribution it had before eradication was initiated (Fig. 1).

Epidemic dengue invariably followed after reinfestation of a country by Ae. aegypti. By the 1980s, the American region was experiencing major epidemics of dengue fever in countries that had been free of the disease for 35-130 years (Gubler & Trent 1994, Gubler 1993, Pinheiro 1989, Gubler 1987, 1989). With increased epidemic activity came the development of hyperendemicity in American countries and the emergence of epidemic DHF, much as had occurred in Southeast Asia 25 years earlier (Pinheiro 1989, Gubler 1987, 1989, 1993). From 1981 to 2005, 28 American countries reported laboratory-confirmed DHF (Gubler & Trent 1994, Gubler & Clark 1995, Rosen 1982, Barnes & Rosen 1974, Guzman et al 1984, Gubler 1989, 1993, 2002, Pinheiro 1989) (Fig. 2).

While Africa has not yet had a major epidemic of DHF, sporadic cases of severe disease have occurred as epidemic DF has increased markedly in the past 25 years. Before the 1980s, little was known of the distribution of dengue viruses in Africa. Since then, however, major epidemics caused by all four serotypes have occurred in both East and West Africa (Gubler 1997, 2002). In 2006, dengue viruses and

1930's

1970

2006

1930's

1970

2006

Thomas Tolfvenstam
FIG. 1. Distribution of Aedes aegypti mosquitoes in the Americas in 1930, 1970 and 2006.

Prior to 1981

1981-2006

FIG. 2. Expanding geographic distribution in the Americas from 1981 to 2006.

Ae. aegypti mosquitoes have a worldwide distribution in the tropics with over 2.5 billion people living in dengue-endemic areas (Fig. 3) (Gubler 1997, 2002).

Currently, DF causes more illness and death than any other arboviral disease of humans. The number of cases of DEN/DHF reported to WHO has increased dramatically in the past two decades (Fig. 4).

I I Areas infested with Aedes aegypti ■ Areas with Aedes aegypti and dengue epidemic activity

FIG. 3. Global distribution of Aedes aegypti mosquitoes and recent epidemic dengue.

1000000 900000 800000 ! 700000

<3 600000

° 500000 | 400000 H 300000 200000 100000 0

FIG. 3. Global distribution of Aedes aegypti mosquitoes and recent epidemic dengue.

FIG. 4. Global average dengue fever/dengue haemorrhagic fever cases reported to WHO annually, by decade.

Each year, an estimated 50—100 million dengue infections and several hundred thousand cases of DHF occur, depending on epidemic activity (Gubler & Clark 1995, Gubler 2002, Monath 1994, World Health Organization 2000). DHF is a leading cause of hospitalization and death among children in many Southeast Asian countries (World Health Organization 1997).

Factors responsible for increased incidence

The emergence of epidemic dengue and DHF as a global public health problem in the past 25 years is closely associated with demographic and societal changes that have occurred over the past 50 years (Gubler & Trent 1994, Gubler & Clark 1995, Gubler 2002). A major factor has been the unprecedented population growth which has been the primary driving force for unplanned and uncontrolled urbanization, especially in tropical developing countries. The substandard housing and the deterioration in water, sewer and waste management systems associated with unplanned urbanization have created ideal conditions for increased transmission of mosquito-borne diseases in tropical urban centres.

A second major factor has been the lack of effective mosquito control in dengue-endemic areas (Gubler & Trent 1994, Gubler & Clark 1995, Gubler 1989, 2002). Emphasis during the past 25 years has been on space spraying with insecticides to kill adult mosquitoes; this has not been effective (Gubler 1989, Newton & Rieter 1992) and, in fact, has been detrimental to prevention and control efforts by giving citizens of the community and government officials a false sense of security (Gubler 1989). Additionally, the geographic distribution and population densities of Ae. aegypti have increased, especially in urban areas of the tropics, because of increased numbers of mosquito larval habitats in the domestic environment. The latter include non-biodegradable plastics and used automobile tires, both of which have increased dramatically during this same period of time.

Another major factor in the global emergence of dengue and DHF is globalization and increased movement of humans, animals and commodities via aeroplane, which provides the ideal mechanism for the transport of dengue and other urban pathogens between population centres of the world (Gubler & Trent 1994, Gubler & Clark 1995, Gubler 1989, 2002). For instance in 2004, an estimated 1 billion persons travelled somewhere via aeroplane. Many travellers become infected while visiting tropical dengue endemic areas, but become ill after returning home, resulting in a constant movement of dengue viruses in infected humans to all areas of the world, and ensuring repeated introductions of new dengue virus strains and serotypes into areas where the mosquito vectors occur. The result is increased epidemic activity, the development of hyperendemicity, and the emergence of epidemic DHF (Fig. 5).

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