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Table of Contents
Year : 2020  |  Volume : 57  |  Issue : 1  |  Page : 63-70

Seasonal variations of dengue vector mosquitoes in rural settings of Thiruvarur district in Tamil Nadu, India

1 Department of Life Sciences, Central University of Tamil Nadu, Thiruvarur, Tamil Nadu, India
2 Department of Ecology and Environmental Sciences, School of Life Sciences, Pondicherry University, Puducherry, Tamil Nadu, India
3 Department of Zoology, Bharathiar University, Tamil Nadu, India
4 Visiting Faculty, Department of Epidemiology and Public Health, Central University of Tamil Nadu, Thiruvarur; Division of Entomology & Vector Control, National Vector Borne Disease Control Programme, Delhi; Director, Absolute Human Care Foundation, New Delhi, India
5 ICMR–National Institute of Malaria Research Field Unit, Chennai, India

Date of Submission09-Jul-2019
Date of Acceptance14-Oct-2019
Date of Web Publication05-Feb-2021

Correspondence Address:
Dr Jayalakshmi Krishnan
Department of Life Sciences, Central University of Tamil Nadu, Thiruvarur–610 101, Tamil Nadu
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/0972-9062.308803

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Background & objectives: Mosquitoes are vectors of several important vector-borne diseases (VBDs) like malaria, dengue, chikungunya, Japanese encephalitis (JE) and lymphatic filariasis (LF). Globally, these VBDs are of major public health concern including India. The information on vector mosquitoes from Thiruvarur district in Tamil Nadu state remains largely either unknown or undocumented. The present study was, therefore, undertaken to find out the seasonal variation in mosquitoes with special reference to dengue vectors in rural areas of Thiruvarur district, Tamil Nadu, India.
Methods: Surveillance of immature vector mosquitoes was undertaken from March 2018 to February 2019. The emerged adults were identified to find out the composition of mosquito species prevalent in the district. The seasonal variations of the mosquitoes especially dengue vectors were analysed for summer (March–July) spring (August–November) and winter (December–February) seasons in all the blocks of Thiruvarur district.
Results: A total of 4879 mosquitoes emerged from the immature collection and the species identification revealed the prevalence of both vector and non-vector species. Five important mosquito vectors collected were —Aedes albopictus, Ae. aegypti, Culex tritaeniorhynchus, Cx. gelidus, and Cx. quinquefasciatus. Other mosquito species collected were Lutzia fuscana, Anopheles barbirostris, An. subpictus, and Armigeres (Armigeres) subalbatus. During the spring season, the dengue vectors showed high indices of breateau index (BI), ranging from 16 to 120; besides, container index (CI) ranging from14.29 to 68.57 and pupal index (PI) from 53.33 to 295 among the study blocks. The major breeding sites were discarded plastic containers, discarded tyres, open sintex tanks (water storage tanks), cement tanks, discarded fibre box, pleated plastic sheets, tree holes, bamboo cut stumps, coconut spathe, and coconut shells.
Interpretation & conclusion: The immature vector surveillance revealed seasonal variations in the entomological indices of Aedes breeding potential. The high indices observed indicate high Aedes breeding density and, therefore, a higher risk for dengue/chikungunya outbreaks in rural areas of Thiruvarur district. The present finding warrants intensive surveillance and follow up vector control measures to avert outbreaks and prevent vector-borne diseases. Health education and the community participation in awareness camps prior to monsoon and societal commitment will help in strengthening source reduction, anti-larval operations and anti-adult measures to tackle vector-borne diseases especially dengue.

Keywords: Breeding sites; seasonal variation; Thiruvarur district; vector surveillance; vector-borne diseases

How to cite this article:
Shukla A, Rajalakshmi A, Subash K, Jayakumar S, Arul N, Srivastava PK, Eapen A, Krishnan J. Seasonal variations of dengue vector mosquitoes in rural settings of Thiruvarur district in Tamil Nadu, India. J Vector Borne Dis 2020;57:63-70

How to cite this URL:
Shukla A, Rajalakshmi A, Subash K, Jayakumar S, Arul N, Srivastava PK, Eapen A, Krishnan J. Seasonal variations of dengue vector mosquitoes in rural settings of Thiruvarur district in Tamil Nadu, India. J Vector Borne Dis [serial online] 2020 [cited 2021 Apr 18];57:63-70. Available from: https://www.jvbd.org/text.asp?2020/57/1/63/308803

  Introduction Top

Vector-borne diseases (VBDs) such as malaria, lymphatic filariasis (LF), dengue, and chikungunya are highly prevalent in India[1]. The VBDs are transmitted by haematophagous arthropods such as ticks, fleas, mites, and mosquitoes. Aedes aegypti and Ae. albopictus (Diptera: Culicidae) are the vector mosquitoes which spread various arboviral diseases like dengue fever (DENV)[2], chikungunya (CHIKV)[3], zika, and yellow fever[4]. Outbreaks of dengue have been reported from various states of India such as Delhi, Haryana, Punjab, West Bengal, Odisha, Maharashtra, Rajasthan, Gujarat, Assam, Arunachal Pradesh, Madhya Pradesh, Tamil Nadu, Kerala, Karnataka, and Andhra Pradesh over a period of time[5]. In South India, dengue was endemic during the 1960s and 1970s[6] and since then cases have been recorded in rural and in urban settings.

In Tamil Nadu, the first evidence of dengue fever was reported during 1956 in Vellore district[7]. In recent years, studies undertaken in Kanyakumari, Villupuram, Thanjavur, Thoothukudi, Namakkal, Perambalur, Dharmapuri, and Virudhunagar districts of Tamil Nadu have reported a high abundance of the Ae. aegypti immatures with high entomological indices[8]. Further, re-emergence of Ae. aegypti and Ae. albopictus were also recorded from the Nilgiri hills and Ramanathapuram districts of Tamil Nadu[9],[10]. Many studies from various districts in Tamil Nadu except Thiruvarur shed light on the faunistic studies of mosquitoes and seasonal variation of dengue vectors. Besides, various studies have shown that climatic changes are the key factors for the expansion of Ae. albopictus and Ae. aegypti[11],[12],[13]. Temperature, rainfall, relative humidity (RH) and the environment plays an important role in the transmission of dengue vectors and disease burden[14]. Climatic factors have shown their impact on dengue fever transmission in other parts of the world.

Vector control is a very important tool for control of dengue as there is no specific drug and treatment; only management practices are available to reduce morbidity. Entomological surveillance of dengue vectors immensely helps the programme managers to chalk out effective plans against vector control during outbreaks. Thiruvarur district is well known as the ‘rice bowl of Tamil Nadu’ with paddy fields although the area has water storage practices due to inadequate water supply. The district also experiences both dry and wet seasons with sporadic reports of malaria and Japanese encephalitis (JE). The district reported a spurt in dengue cases from 2012–2014 although relatively less compared to other endemic areas of Tamil Nadu. In view of the lack of sufficient data on Aedes breeding potential in the district, the present study was aimed to examine the prevalence and distribution of dengue vector mosquitoes across different seasons, which would be beneficial for public health programme and the general public at large.

  Material & Methods Top

Study sites

Thiruvarur region extends from latitude 10° 46′ 17.76″ N to longitude 79° 38′ 12.48″ E of south Indian coastal region in Tamil Nadu. Thiruvarur district was formed in January 1997 which is one of the important districts in deltaic region with an area of 2274 km2. According to 2011 census, the region has a population of 1,264,277. The climate of Thiruvarur is generally hot and humid with seasonal and daily variations in temperature. The average daily temperature, rainfall and RH area is about 28.85°C, 1178 mm and 80.8%, respectively.

The study was carried out in 10 different blocks of the district from March 2018 to February 2019 covering all the seasons, summer (March to July 2018), spring (August to November 2018) and winter (December 2018 to February 2019). The blocks of the survey area include Koradacheri, Kottur, Kudavasal, Mannargudi, Muthupet, Nannilam, Needamangalam, Thiruthiraipoondi, Thiruvarur and Valangaiman [Figure 1]. The GPS co-ordinates of the study sites were plotted using Garmin Etrex 10x software.
Figure 1: Study areas of Thiruvarur district, Tamil Nadu, India.

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Immature sample collection and rearing

Immature collections of mosquitoes were carried out from all the 10 blocks using standard sampling methods described by WHO[15]. While performing the immature monitoring, other related parameters like pH, temperature, vegetation, and nature of the water in the breeding habitats were also recorded. Sampling equipments such as ladle, pipette, plastic containers, flashlight, and enamel trays were used for immature surveillance. Immature collection methods were based on the nature and type of the breeding sites, e.g. dipper and plastic trays were used for the large water bodies such as cement tank, discarded container, etc. and a pipette was used for small water bodies such as tree holes, discarded tyres, etc. The number of dips taken for each sampling site was according to the surface water area[15]. Immature collections from all the blocks were collected habitat-wise in separate plastic containers, with the same water that was in the larval habitat, and were then transported to the laboratory. The containers were marked with permanent marker pen indicating the date, nature, and type of the habitat. The collected larvae were seggregated to different enamel trays based on the mosquito genera following larval identification key[16]. They were then reared in the laboratory by providing larval food (dog biscuit and yeast powder mixed in the ratio 3:1). The emerged pupae in a bowl were separated and transferred to cloth cages (W29.5×D29.5×H29.5) for emergence into adults.

The emerged mosquitoes were maintained at 25 ± 2°C, 75 ± 5% RH and 10 : 14 h light/dark photoperiod along with 10% glucose solution soaked in the cotton pad at Vector Biology Research Laboratory of Department of Life Sciences, Central University of Tamil Nadu, Thiruvarur for further observation to reconfirm mosquito species. The emerged mosquitoes were identified to the species level following identification keys and nomen-clature[17],[18]. The entomological indices like house index (HI), container index (CI), breteau index (BI), and pupal index (PI) were also calculated[19]. The different Aedes breeding habitats observed in the study area are illustrated in [Figure 2].
Figure 2: Common mosquito breeding habitats in Thiruvarur district, Tamil Nadu.

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Figure 3: Mean temperature, rainfall, relative humidity and seasonal fluctuation of dengue vectors in Thiruvarur district, Tamil Nadu.

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Figure 4: Mosquito species composition observed during different seasons: (a) summer; (b) spring; and (c) winter, in Thiruvarur district, Tamil Nadu

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Data analysis

The immature surveillance data for Aedes species were analysed to find out the entomological indices. The calculation of indices was based on standard formulae, i.e. HI—Percentage of houses infested with larvae and/or pupae; CI—Percentage of water-holding containers infested with larvae and/or pupae; BI—Number of positive containers per 100 houses inspected; and PI—Number of pupae per 100 houses inspected. The seasonal variations of the density of dengue vectors observed in all the 10 blocks of the district were analysed using one-way ANOVA in statistical package for the social sciences (SPSS) version 21. All the levels of significance were determined at p = 0.05.

  Results Top

A total of 4879 mosquitoes could be reared from the immature collections undertaken in the study areas during three different seasons, namely summer, spring, and winter. The breeding sites encountered in the blocks are documented in [Table 1]. Dengue vector breeding was observed in the discarded habitats such as broken buckets, tyres, coconut shells, bamboo cut stumps, cement tanks, and open sintex tanks. Five important mosquito vectors could be collected altogether including the dengue vectors, Ae. aegypti and Ae. albopictus. Other vector mosquitoes collected were Culex tritaeniorhynchus and Cx. gelidus that transmits JE and Cx. quinquefasciatus, responsible for the transmission of LF. The collection also included Lutzia fuscana, Anopheles barbirostris, An. subpictus and Armigeres (Armigeres) subalbatus.
Table 1: Breeding habitats of vector mosquitoes in Thiruvarur district

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During the summer season, the mean temperature observed was high (30.6°C) with low mean RH (63.8%). Aedes aegypti and Ae. albopictus population encountered was, therefore, low in density. However, during the spring season, the mean temperature was relatively low (28.75°C), with relative humidity of (71%) [precipitation (191.9 mm)], and hence, Ae. aegypti and Ae. albopictus population was very high during this period. On the other hand, in winter season when the mean temperature was 26.33°C and mean RH was 78%, density of dengue vectors observed was moderate (less when compared to the spring season).

In the summer season, dengue vector contributed to only 7% of the mosquito species composition, whereas Cx. tritaeniorhynchus and Cx. quinquefasciatus were the predominant species collected (79%). However, during the spring season, Ae. albopictus contributed to 60% of the collection, although Ae. aegypti collection was only 6%. In contrast, during winter, Ae. albopictus contributed to 34% of the species composition followed by Cx. quinquefasciatus (28%) and Cx. tritaeniorhynchus (23%).

The entomological indices observed during various seasons are summarised in [Table 2]. In the summer season, out of the 10 blocks, only four blocks showed high indices of HI, CI, BI and PI. In overall, the blocks of Thiruvarur (HI: 20.0, CI: 38.46, BI: 33.33 and PI: 80.0), Needamangalam (HI: 26.32, CI: 33.33, BI: 36.84 and PI: 26.32), Kottur (HI: 43.75, CI: 27.78, BI; 31.25 and PI: 37.5) and Mannargudi (HI: 40.0, CI: 50.0, BI: 40.0 and PI: 60.0) observed the presence of Ae. albopictus. During the spring season, all the blocks showed the presence of Ae. albopictus. The HI (72) was high in Kottur block but BI (120) and CI (68.57) were higher in Thiruvarur district. The PI (195.0) was high in Kudavasal compared to all other blocks. The common breeding sites in these blocks were discarded tyres, bamboo spathe, discarded beer bottles, open sintex tanks, fallen coconut spathe, mud pots, etc.
Table 2: Entomological indices in study blocks of Thiruvarur district

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In winter seasons, all the blocks indicated the presence of Ae. albopictus and Ae. aegypti. Koradacheri block showed higher HI (72.0) compared to other blocks. The percentage of CI, BI and PI were also higher for Needamangalam (76.19) and Valangaiman (114.29). The breeding sites in these blocks were predominantly discarded plastic buckets, open sintex tanks and mud pots.

A one-way analysis of variance (ANOVA) was used to analyze the significant differences in dengue vector, Ae. albopictus; entomological indices (HI, BI, CI, PI), and meteorological factors such as rainfall, temperature and RH (p <0.05 at 95% level of confidence). The analysis revealed no significant difference in Ae. aegypti population in terms of seasonal variation (p >0.05).

  Discussion Top

The entomological survey of mosquito immatures in Thiruvarur district, Tamil Nadu indicated the presence of various vector species such as Ae. albopictus, Ae. aegypti, Cx. tritaeniorhynchus, Cx. quinquefasciatus, and Cx. gelidus, besides the secondary vectors (An. subpictus), and non-vectors such as Lt. fuscana and Ar. subalbatus. Various published reports suggest that the density of dengue vectors are correlated to the seasonal variability[20],[21] and similar variations were also observed in the present study and elsewhere in the world. The observed vector density indicated the probable prevalence of dengue infections in Thiruvarur district, which is in concurrence with the data of the local health department proving the occurrence although in decreasing trend since 2017.

The study revealed higher presence of Aedes mosquitoes in spring compared to summer and winter seasons. The climatological factors during spring and early winter seasons enhance the density and abundance of Aedes mosquitoes[22]. In spring season, due to the rainfall followed by the creation of mosquito breeding habitats, the emergence of Ae. albopictus was aplenty. On the other hand, in the summer season, due to high temperature and negligible rainfall, very low density and abundance were observed. Temperature, relative humidity and precipitation or rainfall are the major environmental variables which influence the Ae. albopictus population. Temperature can influence the adult and immature survival of Ae. albopictus population[23],[24]. It has been reported that temperature between 25 and 30°C[25] is optimal for Ae. albopictus survival and mortality is observed below15°C and above 35°C. The RH also has a specific effect on Aedes survival, for example, if humidity is high, mainly due to rainfall, the conducive environmental conditions facilitate the mosquito development, survival and its viral capacity[26]. It may be noted that rainfall is responsible for the creation of various secondary foci, less examined and not covered under the routine intervention measures. These habitats include discarded tyres, bottles, containers and any water-holding surface which provide conducive oviposition habitat for Ae. aegypti and Ae. albopictus[27]. In summer season, density of dengue vector is low due to high temperature and low rainfall; however, in the present study, high density of dengue vectors was observed in some blocks which may be due to the water storage practices facilitating immature breeding. Various studies have reported that low socioeconomic neighbourhoods result in increased Ae. albopictus invasion which correlates with the availability of discarded habitats and unused containers with water[29].

The proportion of Ae. albopictus was very low in all the 10 blocks during the summer season, whereas in the spring season, an increase in the density and proportion of Ae. albopictus was observed. This indicates that Ae. albopictus is the predominant species of Aedine mosquitoes in Thiruvarur district, due to their preferential habitat selection to breed in artificial containers such as plastic containers, mud pots, discarded tyres, etc. Apart from this, householders used to store water in containers, which facilitates the breeding of Aedes larvae. Aedes albopictus prefers natural containers or man-made breeding sites with a great amount of organic debris. Although Ae. albopictus was predominant during spring and winter, the proportion was less during the summer season due to extreme hot climatic conditions encountered in the district.

The present study has shown the high abundance of Ae. albopictus in spring season which may be attributed to intermittent rainfall, creating many temporary breeding sites which are also suitable for the Culex, Anopheles and other vector species. The high entomological indices of Aedes breeding and abundance of immature forms from October to December 2018 in the district may be attributed to the post ‘Cyclone Gaja’ effect. Cyclonic impact results in abundant rainfall thereby creating innumerable breeding habitats, both natural and artificial habitats which are secondary foci and less examined but builds up adult density. Various studies have reported increase of mosquito density after the natural disaster globally[29],[30]. Although the whole district was severely affected, innumerable mosquitogenic conditions favourable for mosquito vectors were created during the receding monsoon period, especially Ae. albopictus. The winter season also showed moderate distribution of Ae. albopictus in Thiruvarur, Nannilam, Valangaiman, Thiruthiraipoondi, Mannargudi, Koradacherri and Muthupet blocks with high density on the analysis of immature surveillance data.

Apart from Ae. aegypti and Ae. albopictus, other mosquito vectors were also observed, such as Cx. quinquefasciatus, Cx. tritaeniorhynchus, and Cx. gelidus. All the blocks during summer showed a higher prevalence of Cx. tritaeniorhynchus and Cx. quinque-fasciatus because of the presence of rice fields (paddy fields) and poor drainage system. Culex quinquefasciatus is generally found in rural as well as in the urban areas, and this pattern was observed in our study as well. Culex tritaeniorhynchus, the JE vector is mainly present due to the agricultural practices, which is quite common in the district. However, Cx. gelidus was distributed in all the blocks in moderate numbers. The present study revealed innumerable breeding habitats contributing to the density of the mosquito vectors in Thiruvarur district. These habitats mainly in rural pockets can flare up the incidence and lead to outbreaks if adequate vector control measures are not taken up. Although the district may be reporting low burden of VBDs, this should not be taken lightly as dengue vectors can play a havoc in the morbidity and mortality if all other confounding variables like climatic conditions, environmental determinants are conducive for transmission. Furthermore, the presence of JE and LF vectors also add to the morbidity burden of the district. Hence, a comprehensive vector control plan which is situation-specific may be rolled out by the programme managers to tackle the dreaded dengue infection besides other VBDs, by mobilizing the community and school children for source reduction, promoting mosquito control and disease prevention awareness programmes. Health camps may also be organized periodically so that the message to prevent mosquito breeding would go to the desired grass-root level. This would definitely benefit the society as there will be a joint commitment from the community level and the local vector control programme to address mosquito control measures.

The present study may be taken into account within the context of a few limitations and constraints. The vector surveillance was mainly dependent on immature surveys, and adult vector surveillance could not be carried out due to the limited manpower and prevailing time constraints. The present study could not find out the correlation between disease and entomological surveillance. Nevertheless, the local health department may investigate and find out, if cases are being recorded at private diagnostic centres which are not notified to the government health systems.

  Conclusion Top

This study was undertaken to explore the seasonal prevalence of various mosquito vector species particularly the dengue vectors that might implicate local transmission of infection. In the present investigation, five important vector species were recorded from the study area, of which Ae. albopictus was found to be the predominant vector followed by Ae. aegypti. Observation on the seasonal variation indicated high breeding during rainy season. These findings will enable the local vector control department to undertake intensive actions to strengthen entomological and disease surveillance further. Micro-level evaluation of the areas with high breeding density would be beneficial to curtail morbidity of the infections and transmission potential. A detailed eco-epidemiological study in the future would help in mapping risk areas depending on the availability of potential key containers contributing to the Aedes breeding density and abundance from natural, man-made and discarded artificial containers for targeted intervention operations.

Conflict of interest

The authors declare that they have no conflict of interest.

  Acknowledgements Top

The authors thank the State Health Department of Tamil Nadu and health authorities of the Thiruvarur district for providing data on the vector-borne diseases of the district during the study. The authors are grateful to the Central University of Tamil Nadu for providing necessary infrastructure facility at Vector Biology Research Laboratotory of Department of Life Sciences. The authors are also thankful to the NIMR, Field Unit, Chennai for helping in data analysis, and Bharathiar University and Pondicherry University for mapping of GPS coordinates.

  References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2]


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