Eco-epidemiological analysis of dengue infection during an outbreak of dengue fever, India

Dengue infection (DI) is amongst the most important emerging viral diseases transmitted by mosquitoes to humans, in terms of both illness and death [1]. The worldwide large-scale reappearance of dengue for the past few decades has turned this disease into a serious public health problem, especially in the tropical and subtropical countries [2–4]. It is estimated that 52% of the global population are at the risk of contracting Dengue fever (DF) or dengue hemorrhagic fever (DHF) lives in the South East Asian Region. Although all the four serotypes have been circulating in this region, ecological and climatic factors are reported to influence the seasonal prevalence of the dengue vector, Aedes aegypti, on the basis of which countries in this region are divided in to four zones with different DF/DHF transmission potential [5]. In most of the countries, dengue epidemics are reported to occur, during the warm, humid and rainy seasons, which favor abundant mosquito growth and shorten the extrinsic incubation period as well [6–9].

DF has been known to be endemic in India for over two centuries as a benign and self-limited disease. In recent years, the disease has changed its course manifesting in the severe form as DHF, with increasing frequencies [10] Delhi City (India) is home to more than 13 million people and is endemic for DI [11]. Overpopulation has consequently led to poor sanitary conditions and water logging at various places. A major epidemic of DHF from Delhi was last reported in the year 1996 after which DI became a notifiable disease and a number of policies were formulated to bring the DI as well as its vector under control. The retrospective studies, one conducted by us during the period, 1997–2001 and another by National Institute of Communicable Diseases (NICD), New Delhi during the year 1997, have observed a decline in the number of cases having either DF or DHF in the following years [12, 13]. Although, the vector mainly responsible for the spread of DI is present all the year around in Delhi, studies on the relative prevalence and distribution have shown the highest A. aegypti larval indices during the monsoon and post monsoon period [13–15].

In the year 2003, India had experienced one of the wettest monsoons in 25 years, which led to a spate of mosquito growth creating an alarming situation of mosquito borne diseases in many states. Delhi experienced an outbreak of DF this year, after 6 years of silence. Studies conducted in the countries like Brazil, Indonesia and Venezuela, where DI is present either in epidemic or endemic form have suggested a correlation between weather and pattern of DI. Rain, temperature and relative humidity are suggested as important factors attributing towards the growth and dispersion of this vector and potential of dengue outbreaks [2–4]. Since limited data is available on the association of climatic conditions and the pattern of DI from this geographical region, this study was conducted to find out the relationship of dengue infection with climatic factors such as the rainfall, temperature and relative humidity during the dengue outbreak in the year 2003.

In the year 2003, India had experienced one of the wettest monsoons in 25 years, which led to a spate of mosquito growth creating an alarming situation of mosquito borne diseases in Delhi and many other states [16]. As a consequence to this unusually heavy rain, an outbreak of dengue fever was once again reported from Delhi after a silence of six long years. Most of vector borne diseases exhibit a distinctive seasonal pattern and climatic factors such as rainfall, temperature and other weather variables affect in many ways both the vector and the pathogen they transmit [17]. Worldwide studies have proposed that ecological and climatic factors influence the seasonal prevalence of both the A. aegypti and dengue virus [2–4]. The vector mainly responsible for the spread of DI is present at the basal level all the year around in Delhi, however, studies on the relative prevalence and distribution have shown the highest A. aegypti larval indices during the monsoon and post monsoon period [13–15]. Since limited data is available on the affect of climatic factors on the pattern of DI, this study was planned to carry out the month wise detailed analysis of three important climatic factors such as rainfall, temperature and relative humidity on the pattern of DI.

Observations on the seasonality were based on a single year's data as the intensity of sampling was at its maximum during this outbreak period. The outbreak coincided mainly with the post monsoon period of subnormal rainfall, which was followed, by relatively heavy rainfall during the monsoon period; from June to September 2003. The difference in the total rainfall and temperature during three seasonal periods was found to be statistically significant (p < 0.05). Monthly weather data showed that temperature variations were more amongst different months during the pre monsoon and post monsoon period as compared to the monsoon period. Even though, the monsoon season began in mid- June, there was no respite from the heat as there was not much difference in the temperature during the last month of pre monsoon; May and beginning of monsoon in the June. Unusual heavy rainfall subsequently led to decrease in temperature during the later part of monsoon period. The temperature showed a decline and remained almost constant during the months of July and August (30.2°C), continuous heavy rainfall subsequently led to further decrease in the temperature during the month of September to 29°C. Relative humidity increased during the rainy season and remained high for several weeks. An in-depth analysis of these three factors thus led to a proposal that optimum temperature with high relative humidity and abundant stocks of fresh water reservoirs generated due to rain, developed optimum conditions conducive for mass breeding and propagation of vector and transmission of the virus.

Our study was in tune with a previous study by NICD of seasonal variations and breeding pattern of A. aegypti in Delhi, which showed that there are two types of breeding foci, namely; primary and secondary breeding foci. Primary breeding foci served as mother foci during the pre monsoon period. A. aegypti larvae spread to secondary foci like discarded tyres, desert coolers etc., which collect fresh water during the monsoon period [14]. This study supported the proposal that all the three climatic factors studied could be playing an important role in creating the conducive condition required for breeding and propagation of this vector, the basal level of which is present all round the year. This prospective study therefore highlighted the major important factors, which could alone or collectively be responsible for an outbreak.

In our study, the largest proportion of serologically positive cases was recorded in the post monsoon period, which is in agreement with our previous study [12]. Our findings were in coordination with study by other groups from this geographical region [13–15]. The seasonal occurrence of positive cases has shown that post monsoon period is the most affected period in Bangladesh as well [18]. However, a retrospective study from Myanmar during 1996–2001 reported the maximum cases of dengue during the monsoon period [19]. Study by group of Rebelo from Brazil has also emphasized the importance of season. They have observed that dengue cases were higher during rainy season showing the importance of rain in forming prime breeding sites for A. aegypti thus spread of DI [20]. Study of eco-epidemiological factors by Barrera et al [21] showed that DF has a positive correlation with the relative humidity and negative relation with evaporation rate. Peaks of dengue cases were observed to be near concurrent with rain peaks in this study from Venezuela showing a significant correlation of intensity of DI with the amount of rain [21]. In this study we have observed that temperature tends to decrease towards the end of monsoon period, specially remains moreover constant during the later months of rainy season. India and Bangladesh fall in the deciduous, dry and wet climatic zone. The temperature remains high during the pre monsoon period. It is continuous rain pour for a couple of days that brings down the temperature during the monsoon period, which may also be responsible for an increase in the relative humidity and decrease in the evaporation rate thus maintaining secondary reservoirs containing rain water. More studies are needed to establish the relationship between the climatic changes and dengue outbreaks, which would help in formulating the strategies and plans to forecast any outbreak in future, well in advance.

Very little dengue is found in adults in Thailand, presumably because people acquire complete protective immunity after multiple DI as children [1], as DI is highly endemic in Thailand [22]. On the other hand, DI especially DHF is an emerging disease in India; probably this may be the reason that people of all the age are found to be sensitive to infection in our study. Even though more adults were reported of having anti dengue antibodies, the difference in the number of positive cases was not significant as compared to pediatric age group.

The severity of this outbreak was lesser as compared to the DHF epidemic that occurred in year 1996 caused by the serotype Den-2 [23]. Serotype Den-2 is reported to be the one mainly associated with DHF, the more severe form of the disease [24, 25]. More studies in this regard can further elucidate correlation of serotypes with severity of disease from this geographical region.

This prospective study highlighted rain, temperature and relative humidity as the major and important climatic factors, which could alone or collectively be responsible for an outbreak. More studies in this regard could further reveal the correlation between the climatic changes and dengue outbreaks, which would help in making the strategies and plans to forecast any outbreak in future well in advance.