Dengue in India with Special Reference to the ...

Vector Biology Eds. VP Sharma and Jagbir Singh Kirti The National Academy of Sciences, India, Allahabad

Dengue in India with Special Reference to the Interspecific Invasive and Virus Transmission Potential of the Asian Tiger Mosquito, Aedes albopictus (Skuse) in Kerala: An Update BK Tyagi and AP Dash Centre for Research in Medical Entomology (ICMR), 4-Sarojini Street, Chinna Chokkikulam, Madurai-625 002, Tamil Nadu

Introduction At the end of the last century, the world faced the resurgence of many infectious diseases, dengue - an African word meaning "bone breaking" and a mosquito-borne infection which has been referred in the Guinness Book of World Record as the most dangerous vector-borne disease in the current millennium - being one of the most important in terms of both morbidity and mortality'. The dengue virus is transmitted to man by the bite of several day biting mosquitoes, amongst which Aedes aegypti is the principal vector. Some other species have also derived enormous importance in recent years, particularly Ae. albopictus which has been found to transmit dengue even in the absence of the principal vector in certain ecological situations'. Both these mosquito species are also serious vectors for certain other diseases, mostly in Africa and the Americas. While Ae. aegypti, along with certain other species, is the principal carrier for the deadly yellow fever virus, Ae. albopictus - popularly known as Asian Tiger mosquito (understandably because the mosquito was first described from Bengal in 1894 by Skuse and the mosquito bears the characteristic tiger-like stripes on its body) - is currently involved in the transmission of as many as 23 different types of viral infections in the orth America alone3,4,5 • Yet, dengue overshadows all these maladies due to its sheer presence in all the continents as well as its ever growing strongholds in newer areas, on one hand, and an altogether non-availability of a specific drug to control the disease, on the other. A dengue-specific vaccine currently undergoing rigorous trials will possibly still take many years to be available commercially. Esmail: [email protected]

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Both these mosquitoes are also capable to regulate vertically dengue viruses in nature through trans-ovarial mode of transmissionv'. The first confirmed dengue epidemic is known to have occurred in 1779, but the dengue virus and its carrier mosquitoes could not be determined until early 201h century. The four viruses, dengue 1 to 4, classified in an antigenic complex of the flavivirus genus of the family flaviviridae are the aetiological agents for causing dengue'. These spherical agents of 40-50 mm in diameter have a lipid envelope and a positive single stranded RNA The viral genome of approximately 11 kb in length encodes three structural proteins (capsid, C, membrane protein, M, envelope glycoprotein, E) and seven non-structural proteins (NS1, S2, NS2b, S3, NS4a, NS4b and NS5). The 5' and 3' noncoding regions are important for regulating viral replication. The main biological properties of the viruses are located in the E protein, including receptor binding, haemagglutination of erythrocytes, neutralizing antibody induction and protective immune response. Dengue is a rather cryptic disease. illness due to dengue presents a spectrum of mild flu-like disease to a severe and occasionally fatal haemorrhagic clinical picture referred to as dengue haemorrhagic fever (DHF) and dengue shock syndrome (DSS) which are all increasingly important public health problems in the tropics and subtropics. Ironically, immunity developed against a given virus serotype is limited to this only and does not provide cross-protection against anyone of the other three serotypes, and upon contracting a second infection subsequently with a different serotype, a patient already with a strain-specific immunity may stand a greater risk of developing dengue haemorrhagic fever. About 2.5-3 billion people (40% of the global population) continue to live at constant risk of contracting infection, while 50 million cases and 24,000 deaths are estimated to regularly occur annually in just over 100 endemic countries worldwide, including hospitalization of nearly 500,000 cases of which 90% are children. More importantly, with the imposing disease burden as high as 465,000 DALYs across the globe, dengue in certain socio-ecological settings may exact disease burden that can only be paralleled with that of malaria among all the vector-borne diseases. The South-East Asia Region contributes 52% or 1.3 billion cases annually. India is one of the seven identified countries in the Region regularly reporting incidence of DF/DHF outbreaks and seems to be heading to transform into a major hyperendemic niche for dengue infection in near future, with more new areas being struck by the epidemic dengue on a cyclic basis. The first confirmed report of dengue infection in India was made in 1945 where after several states, including three of the four southern states, viz., Kamataka, Andhra Pradesh and Tami! Nadu, began to report the disease

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which mostly struck in epidemic proportion often claiming heavy morbidity and mortality, both in urban (e.g., Delhi metropolis in 1996) and rural environments (e.g., showTamil Nadu's Dharrnapuri district in 1997)8.9.Dengue haemorrhagic fever was first reported in India during the 1960s, although Kerala remained a terra cognito until mid-1990s. Before describing an arcane situation of dengue infection in Kerala characterized by (i) Cyclic annual outbreaks for past five years, (ii) Emergence of DHF and DSS since 2003, (iii) Hyperendemicity, i.e., all the four dengue viruses in circulation in nature, and (iv) Aedes albopictus, being the primary and only confirmed vector of dengue infection in Kerala, it is considered opportune to have a firsthand information on the bio-ecology of the main dengue vectors, Ae. aegypti and Ae. albopictus.

Bio-Ecology of Dengue Vectors Several species such as Aedes aegypti, Ae. albopictus, Ae. polynesiensis and several species of the Ae. scutellaris complex (incl. Ae. mediovittatus) are carriers of dengue viruses across the globe, although only Ae. aegypti is credited as the most dangerous vector worldwide while in recent years danger of dengue spread even in areas earlier unknown for the disease. In India only vector species Ae. aegypti and Ae. albopictus occur, with former having a ubiquitous distribution while latter is present in a more patchy style. Both these species complete their life cycles through egg, larval, pupal and adult stage which look alike if discerned cursorily. In Kerala State it is Ae. albopictus which is predominantly present and is the sole vector of dengue so far.

Ae. albopictus has also posed an unprecedented

1. Aedes aegypti (Linnaeus, 1758) (i)

Altitude

Altitude is an important factor in limiting the distribution of Ae. aegypti. In India, Ae. aegypti ranges from sea level to 1000 m above sea level. Lower elevations (less than 500 meters) have moderate to heavy mosquito populations while mountainous areas (greater than 500 meters) have low populations. An altitude of 1000 to 1500 m appears to be the limit for Ae. aegypti distribution, although elsewhere in the world, such as in Columbia, it could be found at even higher altitudes, i.e. up to 2200 m. (ii) Ecology and Bionomics (a) Eggs

Eggs are deposited singly on damp surfaces just above the water line. Most female Ae. aegypti will lay eggs in several oviposition sites during a single

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gonotrophic cycle. Embryonic development is usually completed in 48 hours in a warm and humid environment. Once embryo development is complete, the eggs can withstand long periods of desiccation (more than a year). Eggs hatch once the containers are flooded, but not all eggs hatch at the same time. The capacity of eggs to withstand desiccation facilitates the survival of the species during adverse climatic conditions. (b) Larvae and Pupae The larvae pass through development depends on in the receptacle. Under to adult emergence can the pupal stage. At low for adults to emerge.

four developmental stages. The duration of larval temperature, availability of food, and larval density optimal conditions, the time taken from hatching be as short as seven days, including two days in temperatures, however, it may take several weeks

Throughout most of South-East Asia,Ae. aegypti oviposits almost entirely in domestic, man-made water receptacles. These include a multitude of receptacles found in and around urban environments (households, construction sites and factories), such as water-storage jars, plates on which flower pots stand, flower vases, cement baths, foot baths, wooden and metal barrels, metal cisterns, tyres, bottles, tin cans, polystyrene containers, plastic cups, discarded wet-cell batteries, glass containers associated with "spirit houses" (shrines), drain pipes and ant-traps in which the legs of cupboards and tables often stand. Natural larval habitats are more rare, but include treeholes, leafaxils and coconut shells. In hot and dry regions, overhead tanks, groundwater storage tanks and septic tanks may be primary habitats. In areas where water supplies are irregular, inhabitants store water for household use, thereby increasing the number of available larval habitats. (c) Adults

Soon after emergence, the adult mosquitoes mate and the inseminated female may take a blood meal within 24-36 hours. Blood is the source of protein essential for the maturation of eggs.

Feeding Behaviour Ae. aegypti is highly anthropophilic, although it may feed on other available warm blooded animals. Being a diurnal species, females have two periods of biting activity, one in the morning for several hours after daybreak and the other in the afternoon for several hours before dark. The actual peaks of biting activity may vary with location and season. In the case of interrupted feeding, Ae. aegypti may feed on more than one person. This behaviour greatly increases the epidemic transmission efficiency. Thus, it is not

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uncommon to see several members of the same household with an onset of illness occurring within 24 hours, suggesting that they were infected by the same infective mosquito. Ae. aegypti generally does not bite at night, but it will feed at night in lighted rooms.

Resting Behaviour Aedes aegypti prefers to rest in dark, humid, secluded places inside houses or buildings, including bedrooms, closets, bathrooms and kitchens. Less often it can be found outdoors in vegetation or other protected sites. The preferred indoor resting surfaces are the undersides of furniture, hanging objects such as clothes and curtains, and on walls.

Flight Range The dispersal of adult female Aedes aegypti is influenced by a number of factors including availability of oviposition sites and blood meals, but appears to be often limited to within 100 meters of the site of emergence. However, recent studies in Puerto Rico indicate that they may disperse more than 400 meters primarily in search of oviposition sites. Passive transportation can occur via eggs and larvae in containers.

Longevity Aedes aegypti has an average adult survival of only eight days. During the rainy season, when survival is longer, the risk of virus transmission is greater. More research is required on the natural survival of Ae. aegypti under various environmental conditions.

2. Aedes Albopictus (Skuse, 1894) Aedes albopictus belongs to the same subgenus (Stegomyia) as Ae. aegypti. This species is widely distributed in Asia from tropical to temperate countries. During the past two decades, the species has extended its range to orth and South America, the Caribbean, Africa, Southern Europe and some Pacific island. It is primarily a forest species that has become adapted to rural, suburban and urban human environments. . It oviposits and develops in tree holes, bamboo stumps and leafaxils in forest habitats; and in these plus artificial containers in urban settings. It is an indiscriminate blood feeder and is generally considered more zoophagic than Ae. aegypti. Its flight range may be up to 500 metres. Unlike Ae. aegypti, some strains are cold adapted in Northern Asia and America, with eggs that spend the winter in diapause. Aedes albopictus is a very notorious creature, preferring to inseminate several females simultaneously.

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Virus Transmission A vector mosquito may become infected when it feeds on a viraemic human host. In the case of DF/DHF, viraemia in the human host may occur 12 days before the onset of fever and lasts for about five days after the onset of fever. After an intrinsic incubation period of 10-12 days, the virus grows through the midgut to infect other tissues in the mosquito, including the salivary glands. If it bites other susceptible persons after the salivary glands become infected, it transmits dengue virus to those persons by injecting the salivary fluid.

Dengue Fever!Dengue Heamorrhagic

Fever in Kerala

In some areas of Asia and in the Seychelles, Ae. albopictus has been occasionally incriminated as the vector of epidemic DF/DHF, though it is much less important than Ae. aegypti. In the laboratory, both species can transmit dengue virus vertically from a female through the eggs to her progeny, although Ae. albopictus does so more readily. As far as Kerala is concerned, it took almost five decades for dengue to surface where the first dengue cases associated with some deaths were reported in 1997 only, albeit detection of DEN-1, DEN-2 and DEN-4 viruses in the human sera in the 1970s from Calicut, Cannur, Palakkad, Thrissur, Kottayam and Thiruvananthapuram districts'"!', Interestingly, available records that of the two well known dengue vector species in India only Aedes aegypti (L.) occurred in these seropositive districts, though without an evidence of its role in the disease transmission in Kerala State. In recent times, however, DEN-2 and DEN-3 were isolated respectively from the vector mosquito and human blood seral2.l3. Development of hyperendemicity (i.e., multiple virus circulation in nature) in a short span of one decade, along with incrimination of Ae. albopictus, is an ample proof of the magnitude of severity of dengue infection in Kerala which warrants a firsthand review of the emerging disease under the changing climatic and anthropogenic impacts",

Physiography and Climate of Kerala Kerala, endowed with a unique physiography, is one of the smaller states (38,863 sq. km area; being 1% of the country's total land mass) harbouring nearly 4% of the country's population with a stupendous density of 819 persons per sq. km. that is nearly three times the national average. The whole state, organized in 14 districts, is well connected to those of neighbouring states by rail, road, air as well as waterways. With an average breadth of 50 km, it is blissfully endowed with diversified climatic richness, though

148


not without a pinch of hydrological concern as 41 of its 44 rivers originating in the Western Ghat empty into the Arabian sea in less than 48 hours after a rain. The state's lowland region, which accounts for 10% of the total area in Kerala, runs along the coastline and embodies beaches, swamps and lagoons, besides backwaters, paddy fields and coconut plantations. Kerala's midland (42% of the total landmass), with altitudes ranging from 7.5 m to 75 m above mean sea level (MSL), is primarily made up of valleys with undulating small hills and meandering passages. A variety of seasonal, annual and perennial crops are grown in its mainly lateritic soil. Of all these crops, cocoa and pineapple plantations are of tremendous significance as dengue vectors have been found to breed there15•16• The highland region (48% of the total state's area), with steep hills ranging from 75 m to 750 m above MSL is rife with forests and small streams. Plantation crops like rubber, tea, coffee and cardamom are grown in this region. The diversity of its geographical features has resulted in a corresponding diversity in climate, too. On one hand, while the high ranges along the eastern border, extend at times up to 2694 m above MSL, have a cool and bracing climate throughout the year, the plains, invariably merging coastally into Arabian sea along the western flank, are hot and humid, on the other. The average level of annual rainfall (3000 mm) is quite high when compared to other Indian states, almost three times higher than in Karnataka while twice than in Tamil adu. The state basically enjoys four types of climate such as Winter, Summer, South West Monsoon and North East Monsoon. The winter season sets in during the month of December and continues till end of February. During this season comparatively there is less rainfall especially in the northern parts of the state. Winter is followed by the summer season. It starts in February and continues till May. Temperature is very high during this period. Occasional showers with lightening is a characteristic of this season. Kottayam district tucked in the Western Ghat ranges receives the highest rainfall during this season. The South West Monsoon, accounting for 60-65% of the total rainfall, begins either in the end of Mayor in the beginning of June and fades out by September. Moving towards north this seems to gain intensity, hailing optimally on Peerumedu in Idukki and Vaithiri-Kuttiyadi range in Malabar districts. The rainfall is comparatively low in the Lakshadweep islands. In the southern areas the monsoon is around 40-50% and in the northern areas it is reaching up to 80%. The North East Monsoon, commencing in October, contributes but 25-30% of the total rainfall. The annual temperature is comparatively low in Kerala. The coastal areas record a maximum temperature of 32°C. The interiors record a maximum

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of 37°C during summer. In the coastal area it is hot and humid during April-May while cool during December-January. A careful analysis of epidemics in Kerala State will point out that not only dengue seemed to have an epicenter in Kottayam before spreading over to entire Kerala, but also most of the cases had erupted in the mountainous and sylvan environs of the Western Ghat ranges on the south-western edge of the peninsular India facing Arabian sea coast in Kerala State of which it covers nearly 90% of the total landmass. These lie between 8° 11' to 20° 02' north latitude and 73° 35' to 77° 27' east longitude, rising at times to a height of 2,600 m above mean sea level. The Western Ghat ranges receive variable amount of rainfall from both the southwest (May-July) and the northeast monsoon (September- ovember), and is characterized with the 'Shola' forest punctuated with man-grown extensive plantations of rubber (Hevea brasiliensis), cocoa (Theobroma cacao), coconut (Cocos nucifera) and pineapple (Ananas comosus).

Anthropocentric Activities versus Denguegenic Conditions Anthropogenic impacts have brought about a discernible vicissitude in Kerala 's forest cover, new agriculture practices, traditional water harvesting, demography, urbanization and human mobility. Thus, it would be hard to believe that in Kerala, land of 44 rivers, myriads of seasonal cascades and backwaters, and an annual rainfall of over 3000 mm, there came about a severe drought in 2003, the first ever in the last millennium, with the average annual rainfall dipping to an all-time low of 2000 mm! Ironically, Kerala enjoys high rainfall of 11,500 lit per capita per day, yet it still gets no more than 5060 lit. of water for domestic use per person daily. Water allowanee per capita has depleted miserably in past few years since the per capita availability of water in Kerala is presently lower than even that in a perpetually droughthit Rajasthan state. The Kerala state has an estimated 77.35 billion cubic meters (BCM) of fresh water, but nearly 40% of the resources are lost as run off, meaning only 42 BCM of water being available for the whole populace though the state requires a minimum of 49.70 BCM for various indispensably vital activities such as irrigation, domestic use, industries and others miscellaneous annually. This shortage has lead people to resort to exploiting groundwater so severely that the water table in several districts has gone below 200250 m. The water scarcity also induced people to store water in a melange of containers like pitchers, cement tanks etc. as long as possible. A cadence in both ambient temperature and relative humidity is considered highly supportive to a wide dissemination of the dengue vector in time


150

and space. There is thus an evidence to prove a decline in rainfall, on one hand, and a marginal yet perceptible rise in ambient temperature, on the other. The India Meteorological Department considers southwest monsoon to be deficient if rainfall is below 20% of the average annual rainfall. Since 1980 Kerala has suffered seven years of deficient rainfall and another five years below normal rainfall. Kerala State, founded in 1956, originally had a total cropped area spanning over 2 million hectares, with paddy as the major crop covering about 35% of this area, followed by coconut (21%). By 1975 the paddy growing area reduced to 30% of the total cropped area, with only 0.881 mill. ha growing paddy. In 2003 the area under paddy cultivation nosedived to a paltry 0.31 mill. ha, although the coconut plantation sustained a good growth rate of 3% per annum through 1990s of land coverage. It is noteworthy here that, along with coconut, rubber plantation has de novo supported breeding of dengue vector, Ae. albopictus". Presently while rubber plantation occupies the largest area in Kerala, paddy field have reduced and reclaimed largely for construction of human habitation. It is noteworthy thatAe. albopictus bred predominantly in the latex collecting cups.

Dengue Hyperendemicity

in Kerala

Cyclic dengue epidemics in Kerala State have been occurring since 2001, even though the first dengue cases were already brought on recorded from Kottayam district in 1997 reporting 14 cases and 4 deaths. This was followed by another more severer dengue outbreak implicating 67 cases (5-fold increase) and a toll of 13 human lives (3-fold increase) in 1998, again in the same district (fable 1). The years of 1999 and 2000 were virtually free from any dengue cases. However, soon in 2001, epidemic dengue resurged mainly in Kottayam, Idukki and Ernakulam reporting 70 cases, followed by 219 cases in 2002 with some deaths. The year 2003 experienced the severest epidemic till date yielding as many as 3546 confirmed cases (253-fold increase) and a toll of 68 human lives, spread for the first time all over the Kerala's fourteen districts. The occurrence of DHF and DSS was also clinically and serologically

documented.

In view of a rather recent emergence of dengue infection in Kerala, the data on disease epidemiology are very scanty and inconclusive. During 2003, however, the dengue cases, which initially kept a low ebb, suddenly began to appear in large numbers from invariably all the fourteen districts soon after the south-west monsoon, reaching a maximum of 1337 in the month of July.

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151

Table 1: Dengue cases in different districts in Kerala State between 1997 and 2003 Year 1997 998 1999 2000 2001 2002 2003

Cases

Proportionate increase (taking 1997 as base year)

14 67 1 0 70 219 3546

1: 4.8

1: 5 1:15.6 1: 253.3

Deaths 4 13 0 0 1 2 68

It is evident that 75.5% of the total dengue cases in Kerala State occurred during 2003 only during the southwest monsoon period whenAe. albopictus also prevailed in higher density. Since then nine of the fourteen districts continued to yield dengue cases till the end of the year, with Thiruvananthapuram reporting the highest incidence of 789/3546 (22.2%). It is further noteworthy that 9 of the 14 districts, of which four are landlocked in the high ranges of the Western Ghat mountains, had reported dengue cases for the first time. However, all those districts (e.g., Kottayam, Idukki, Ernakulam etc.) which had been reporting dengue earlier had also shown an increase in the incidence. Clinically dengue patients had been found to present a wide spectrum of signs and symptoms, often overlapping with flu and other infections including leptospirosis. However, during an investigation carried out in 2003, major symptoms elicited by DF cases included fever (100%), headache (85.9%), retero-orbital pain (47.4%), myalgia (77.2%) and joint pain or arthralgia (47.4%). The haemorrhagic patters of the DHF cases were manifested as rashes (86.3%), gum bleeding (21.1 %) and purpural/echymosses (5.3%) etc. Children below 15 yrs of age were quite severely affected (19.3%), although majority of infection occurred in the active adult age group of 16-60 yrs (77.2%) with the geriatric group (>60 yrs) people being also vulnerable (3.5%). While a total of30 patients (52.64%) exhibited haemorrhagic patterns of DHF (Fig. 6), only 27 patients (47.36) manifested signs and symptoms of the classical dengue fever. Five (16.7%) DHF cases showed multiple haemorrhagic manifestations with skin rashes being most common. Rarely though, Gullain-Barre syndrome and acute necrotising myelitis with unknown aetiology were also reported to be associated with the dengue infection".

Virus Detection and Isolation Serologically, even though clinical cases had not appeared until late 1990s, the DEN-1, DEN-2 and DEN-4 viruses had been detected in 1970s from

152


the human sera in a few districts like Calicut, Cannur, Palakkad, Thrissur, Kottayam and Thiruvananthapuram'v'v'v". It is interesting to note here that only Ae. aegypti without an instance of virus incrimination was recorded from all these districts covered under serological surveillance of local human population and Ae. albopictus was conspicuously absent. During the 2003 outbreak, a total of 112 finger-pricked blood samples were collected from dengue suspected and/or confirmed cases, of which 74 (66.0%) sera originating from Pattanamthitta (22.9%), Kottayam (22.2% ),Alleppy (24.3%), Ernakulam (6.7%) and Thiruvananthapuram (25.6%) were found positive in antigen capture MAC-ELISA Using dengue positive human sera, the biological TOXO-IFA system was employed and DEN-3 (67%) was isolated from Kerala cases (67%), implying introduction of a new dengue virus serotype in Kerala. Additionally, a total of 37 human sera were tested by indigenously developed MAC-ELISA test and 8 (48.6%) exhibited IgM type of antibodies against DEN-2 indicating recent dengue virus infection. These observations carry tremendous epidemiological significance from the viewpoint of evolving hyperendemicity, being one of the possible causes to bring about DHF. Virus detection from a dengue vector had been elusive until 2002. A long term investigation by the author and his team on both Ae. aegypti and Ae. albopictus in Kerala during 2002-2004 yielded a total of 240 pools (5173 adults) of Ae. albopictus comprising 112 pools (2456 adults) of males and 128 pools (2717 adults of which 413 were wild-caught females) were screened for the presence of dengue virus through ELISA Of these one pool consisting of 20 females of Ae. albopuictus, reared from the fieldcollected immatures collected from Mundakayam in Kottayam district, was found positive for dengue virus, indicating towards the trans-ovarial mode of transmission by this species. This phenomenon was further corroborated by a similar observation on Ae. albopictus in a nearby Nagercoil area (Kanyakumari district, Tamil Nadu) tucked in the lower reaches of the Western Ghat ranges (cf Fig. 1). Subsequently, during 2004, DEN-2 virus was finally isolated using the TOXO-IFA system and confirmed through ELISA from the two pools of wild caughtAe. albopictus female mosquitoes from Kottayam district, demonstrating with certainty the inevitable role of Ae. albopictus in the transmission of dengue in Kerala state. Ironically, so far Ae. aegypti has failed to be incriminated with a dengue virus in nature in Kerala.

Breeding of Dengue Vectors Of the 26 species belonging to eight genera sampled in Kerala Aedes albopictus- the Asian tiger mosquito, was most dominant (69.7%), followed by Armigeres subalbatus (20.7%), Aedes aegypti (4.4%) and Culex uniformis

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(1.5 %), with rest of the species accounting for less than 1% individually. Aedes aegypti was generally conspicuous by either a total absence or a very low density Mosquito species sampled exhibited a good degree of flexibility in breeding adaptability to various kinds of habitats. Aedes albopictus surpassed all species by exhibiting a wide spectrum of breeding preferences with a clear-cut predilection for coconut shells/plastic cups (79.7%) deployed in collecting latex from the rubber trees. Aedes albopictus breeding in cocoa pods (Theobroma cacao) has been widespread in Western Ghat forest fringe areas and its significance has been duly emphasized in preserving the vector density during high monsoon times when the main breeding habitats such as the latex-collecting cups tethered along the main trunk of the rubber tree are rendered unsuitable for breeding due to latter being turned upside down or covered with polythene sheets to avoid water collection in CUpS21.Ae. albopictus was found to maintain two peaks of high density correlating with the two monsoon seasons. This observation was considerably substantiated by both the container larval positivity and tbe adult landing index for Ae. albopictus. While the container larval positivity was as high as 64.1-73.8% in June and 80-84.3% in December, the adult landing index too was correspondingly high in June (7.2-11) and December (7.1-7.8), respectively. High density of Ae. albopictus (Breteau Index about 20) compared to relatively very low BI for Ae. aegypti seemed to bear a direct impact on dengue transmission and dissemination since the highest cases seemingly arose during these two periods only; the more conspicuous peak of both cases and deaths being during the south-west monsoon.

Interspecific Invasive and Virus Transmission Activities by Aedes Albopictus Dengue is an enigmatic disease largely because it does not have a specific antidote nor a vaccine is available for this infection. In spite of the fact that dengue in India was first reported in 1940s, yet the first case of confirmed dengue infection from Kerala State was brought on record in 1997 only. Since 2001 dengue's occurrence increased in Kerala State and outbreaks were reported repeatedly from most of the central and southern districts. DEN-1 and DEN-4 were detected in human sera from Calicut, Kannur, Palakkad, Thrissur and Thiruvanthapuram districts, whereas DEN-2 alone was reported from Kottayam and Thrissur districts". Later wide distribution of DEN-2 virus was empbasized in Kerala, without any evidence to vector incrirnination-", although Ae. aegypti was regularly sampled only along the sea coast. Characteristically no reference was made to the existence of another


154 Table 2' Breeding Type of breeding

habitats habitats

of Aedes

albopictus

No. positive' surveyed

in Kerala

state

Percent positivity (I'o habitats)

Percent positivity (To total)

Natural: Leaf axils (pineapple) Cocoa pods Tree holes Plant stumps (plantain)

14 12 5 2

36 18 7 2

38.9 66.7 71.4 100

0.8 0.3

Total

33 , 63

52.4

5.3

499 , 1093 45 , 89 8 , 21

45.7 50.6 38.1 80.0 50.0 14.3

19.7 1.2 1.3

560 , 1226

45.7

89.5

9 , 38 9,20 t t 10 5 , 8 3 , 3

23.7 45.0 10.0 62.5 100

1.4 1.4

33 , 19

41.8

5.3

Artificial: Latex coUecting cups Coconut shells Mud pots Grinding stones Flower pots Cement cisterns Total Discards: Plastic containers Tin containers Tyres Bottles Abandoned shoes

4' 2' 2'

, , , ,

5 4 14

2.2 1.9

0.6 0.3 0.3

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155

competing with, and attempting to displace, Ae. aegypti. A highly significant observation on the interspecific invasive behaviour between these two dengue vector species had been taken recently in the Ernakulam township in Kerala where Ae. albopictus was found to breed in the domains well defined for Ae. aegypti", In VeLLoredistrict of Tamil Nadu, during a 2-year study in three dengue endemic villages Ae. aegypti, Ae. albopictus and Ae. vittatus were considered as the prevalent vector species". From 271 pools (4016 specimens) of adult females, eight dengue virus isolates were obtained, of which seven were from Ae. aegypti and one from Ae. albopictus. This is the first report of dengue isolation from Ae. albopictus in rural India. Infection rates in the two species were comparable. However, due to higher and perennial prevalence. Ae. aegypti is considered as primary vector, with Ae. albopictus playing a secondary role. Despite circulation of all four dengue serotypes detected mainly during the transmission season, the high anthropophilic index ofthe vectors and their abundance, no human dengue case was reported, suggesting silent dengue transmission.

virus in several southeast Asian countries".

In a study carried out on the vertical transmission of DEN-2 by a strain of Ae. albopictus in India foLLowing intrathoracic inoculation of the virus; a total of 650 larvae and 1315 adults of the F1 generation obtained from Ae. albopictus were processed", One pool of larvae and two pools each of males and females showed the presence of DEN antigen. Pools of second and third gonotrophic (G2 and G3, respectively) cycles were found positive for DEN virus. Six pools of 12 and seven pools of 11 showed the presence of DEN antigen in the batches of one and 2 months, respectively. This study indicates the capacity of the mosquito strains studied to effect vertical transmission and is comparable to similar studies elsewhere in Asia.

Both Stegomyia species are widely distributed throu~hout India. The yearly report of the National Institute for VIruses (NIV) m Pune .for 1988 observes that Ae. albopictus is an important vector of dengue m southeast Asia and that DEN-4 virus has been isolated from it in Asanol, We~t Bengal by the Nnf24. It has also been reported tha.t, in ~dia, dengue IS transmitted by Ae. aegypti in cities and Ae. albopzctus .m su?urban and rural areas. This amply changed the epidemiology of dengue m India,. probably due to the invasion of suburban and urban areas by Ae. aegypti and Ae. albopictus, respectively. In Kolkata, results of a .study in the early 199.0s implied that Ae. albopictus had gained a foothold m the suburban township. A larval and adult survey of Aedes species conducted from October 19~5 to September 1996 in crowded areas of the city and an urb~ garden m the centre of the city found both Ae. aegypti and Ae. albopzctus prese~t in the surveyed areas as larvae and adults. Aedes albopictus, however, IS

In India, the transmission of dengue by both the vector species has been well documented, yet it was never known if Ae. albopictus could also transmit the dengue virus in the total absence of Ae. aegypti, as was noticed in certain other southeast Asian countries. Author's Kerala investigation on dengue between 2001 and 2004, has offered the answer. It has been demonstrated that dengue virus in Kerala State is transmitted by Ae. albopictus in the absenceAe. aegypti, alluding towards its primary rather than secondary role in disease transmission as an epidemic vector, which is reported for the first time in India". Their investigations have additionally suggested thatAe. albopictus is prodigiously present particularly in the Kerala's sylvan and mountainous Western Ghat ranges rife with rubber and cocoa plantations't-". It is interesting to note, therefore, that there is a direct correlation between the preponderance of Ae. albopictus and the conflagration of dengue cases in Kerala State. While circulation of multiple strains (hyperendemicity) in

Total

1.1 0.8 0.5

important vector of dengue, Ae. albopictus in Kerala till 1980s. Aedes albopictus is a competent vector for dengue viruses, an~ the presence of this species in association with Ae. aegypti increas.es t~e .nsk for ~mergence of dengue epidemics. Aedes albopictus has been incriminated WIth dengue

156


nature seems to be a comprehensible factor in conflagrating dengue outbreaks, discovery of DEN-3 virus in human sera in early 2003 and DEN-2 virus in the vector mosquito Ae. albopictus soon after in 2004 lend a good support to the hypothesis that the dengue viruses are still in the process of dissemination and establishment across the length and width of the state. A constant occurrence of dengue cases from Kottayam district, adequately supported by first the detection of virus fromAe. alabopictus in 2002 and subsequently its isolation from the same vector and site in 2004, allude towards a likely pathway of origin of dengue emergence in other neigbouring districts arising from Kottayam. In view of these observations a clear parallelism can be viewed between the occurrence of dengue epidemic foci and the Ae. albopictus strongholds in Kerala State (Tyagi et al., 2003), and the human-factor has obviously played an important role in dispersing the vector species in the hitherto uninvaded areas in the State and cause conducive environment for manAe. albopictus contact27•28• Human behavior is often associated with the spatial and temporal distribution of Ae. albopictus in Kerala which has a tendency to displace Ae. aegypti from its habitats29•JO,JI. At least three human activity-related reasons can be attributed to the spread ofAe. albopictus far from its original sylvatic abode in the Western Ghat in yore to the coastal plains harbouring congested human settlements at present: (i) massive deforestation during past three decades that forced Ae. albopictus to come out of its natural abode, (ii) development of human settlements along forest fringe areas where mosquito frequently fed on human blood peridomestically, and (iii) its potential and likeness for transportation through different modes. Although, nothing is known at present about zoonosis in Kerala, it has been demonstrated shown clearly that dengue is a zoonotic disease of monkeys in Malaysia maintained by Ae. psedoniveuslsubniveus at canopy level", Therefore, it would be interesting to know if monkey-based zoonotic reservoir would be occurring in the Western Ghat region abounding both in Ae. albopictus and different types of monkeys.

Acknowledgements The authors express their gratitude to the Director General, Indian Council of Medical Research, New Delhi for encouragement, guidance and facilities.

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