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Table of Contents
RESEARCH ARTICLE
Year : 2017  |  Volume : 54  |  Issue : 3  |  Page : 270-276

Seasonal occurrence of Japanese encephalitis vectors in Bareilly district, Uttar Pradesh, India


1 Division of Veterinary Public Health, Indian Veterinary Research Institute, Bareilly, India
2 Division of Livestock Economics, Statistics and Information Technology, Indian Veterinary Research Institute, Bareilly, India
3 Division of Physiology and Climatology, Indian Veterinary Research Institute, Bareilly, India
4 Training and Education Centre, ICAR-Indian Veterinary Research Institute, Pune, India

Date of Submission31-Mar-2016
Date of Acceptance24-Aug-2017
Date of Web Publication7-Nov-2017

Correspondence Address:
H Dhanze
Division of Veterinary Public Health, ICAR-Indian Veterinary Research Institute, Izatnagar, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.217619

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  Abstract 

Background & objectives: Japanese encephalitis (JE) is one of the most common causes of acute encephalitis syndrome in many states of India. Uttar Pradesh state is well known for JE endemicity, contributing 75% of total cases during recent past. Several sporadic cases have been reported from Bareilly region of the state. The disease spread by bite of Culex mosquito. Survey of literature revealed no data on mosquito fauna with reference to JE in this region. Therefore, this study was planned to survey seasonal mosquito population and occurrence of JE vectors in Bareilly region.
Methods: Mosquitoes were sampled on monthly basis from organized pig farm from February 2016 to January 2017 and identified using mosquito identification keys. The meteorological parameters of the area were obtained monthly and standard statistical methods were used to assess the relationship between different weather variables and mosquito population.
Results: A total of 4337 mosquitoes belonging to five genera were collected. Mosquitoes of genus Culex were predominant and contributed 84.41% to the total catch. The most dominant species was Cx. tritaeniorhynchus (30.81%), followed by Cx. quinquefasciatus (28.50%), Cx. gelidus (17.24%), Cx. pseudovishnui (11.85%), Cx. vishnui (8.11%), Cx. fuscocephala (2.70%), Cx. infula (0.76%) and Cx. bitaeniorhynchus (0.03%). Pronounced seasonal variation was observed with majority of mosquitoes showing high density in monsoon and post-monsoon period.
Interpretation & conclusion: The present study provides knowledge on distribution of JE vector in Bareilly which indicates that the area is at risk of JE outbreak. Abundance of Culex vector clearly demarcates possible threat of JE incidence in the study area. A long-term entomological study is needed to further evaluate the significant role of different weather variables in shaping mosquito densities.

Keywords: Japanese encephalitis; mosquito; Uttar Pradesh; weather variable


How to cite this article:
Pantawane P B, Dhanze H, Verma M R, Singh G, Kapdi A, Chauhan J, Bhilegaonkar K N. Seasonal occurrence of Japanese encephalitis vectors in Bareilly district, Uttar Pradesh, India. J Vector Borne Dis 2017;54:270-6

How to cite this URL:
Pantawane P B, Dhanze H, Verma M R, Singh G, Kapdi A, Chauhan J, Bhilegaonkar K N. Seasonal occurrence of Japanese encephalitis vectors in Bareilly district, Uttar Pradesh, India. J Vector Borne Dis [serial online] 2017 [cited 2019 Nov 19];54:270-6. Available from: http://www.jvbd.org/text.asp?2017/54/3/270/217619




  Introduction Top


Japanese encephalitis (JE) is one of the leading causes of mosquito mediated childhood encephalitis globally[1],[2], causing neurological infection and disability[3]. The epidemiology of JE is complex, involving Culex mosquitoes as vectors and ardeid water birds as primary reservoirs, while pig acts as an amplifier host[4],[5],[6]. The disease is most commonly associated with rice growing fields in rural areas where irrigation system, precipitation and water logging favours environment for mosquito breeding, and presence of swine population in peri-domestic areas influences propagation of virus to human population[7],[8]. Bareilly is a major paddy producing district of Uttar Pradesh (UP), having ≥ 96% of land under irrigation coverage in the form of irrigated canal, tank and well, which supports mosquito breeding. In addition, ardeid birds are found as dominating bird fauna around paddy fields. Sporadic cases of JE have been reported from Bareilly district, with estimates of 0.5–1 per 10 0,000 population[8]. The knowledge of mosquito fauna and continuous monitoring of vector population is an important tool for surveillance of mosquito mediated disease and formulating effective control strategies for vector species[9]. Several entomological studies have been carried out on JE vectors in country[10],[11],[12],[13], but most of them are limited to southern India. The information on mosquito species distribution in western UP is scant[14],[15]. To the best of our knowledge, so far there is no published record of mosquito species, particularly JE vectors prevailing in Bareilly region (Western UP). Therefore, this study was planned to determine the mosquito species distribution and seasonal prevalence of JE vectors in the Bareilly region of UP.

The present paper reports the result of mosquito fauna study of one year carried out from February 2016 to January 2017.


  Material & Methods Top


Study area

Bareilly district lies between 28° 20” to 28° 54” N and 78° 58” to 79° 47” E in western region of Uttar Pradesh. The total geographical area is about 4120 km2 with a population density of about 550/km2 . The net irrigated area is 294,507 ha, and paddy is the main crop grown yearly in the district, followed by wheat and sugarcane. The year comprises three seasons, i.e. winter (October–February), summer (March–June) and monsoon lasting roughly from July to September[16]. The area receives 1032 mm annual rainfall. Water logging and formation of shallow pools are annual features in the region. The agriculture is the main source of economy in rural areas. Moreover, an urban agriculture and pig husbandry is becoming more common and majority of pig population is held by small and marginal farmers in the area[17].

Mosquito collections and identification

Organized pig farm in Bareilly was selected for monthly mosquito collection (twice in one month) for the period of one year, i.e. February 2016 to January 2017. The adult mosquitoes were sampled by battery operated and UV-lamp aided mosquito trap (Wantrn, Coimbatore, India) placed in and around pigsties and operated from dusk-to-dawn (1800–0600 hrs). After collection, the mosquitoes were transported to the laboratory of Division of Veterinary Public Health, ICAR-IVRI and given shock by placing at 0° C for 30 min. The specimens were counted, identified and pooled species wise with the use of mosquito identification keys[18],[19],[20],[21] and stored at –20° C for further use. Damaged specimens were not included in the study. The consent from farm authorities was obtained for mosquito collection.

Meteorological data collection

The meteorological parameters like maximum and minimum temperature, maximum and minimum relative humidity and rainfall during the study period were obtained monthly from Accu Weather website (https:// www.accuweather.com) and the Division of Veterinary Physiology and Climatology, Indian Veterinary Research Institute, Izatnagar, UP, respectively.

Statistical analysis

Statistical analysis was carried out to know the relationship between different weather variables and mosquito population density by Pearson’s correlation coefficient and multiple linear regressions using SAS 9.3 software. Further, chi-square test was applied to know the statistical significant difference between mosquito populations of different seasons.


  Results Top


A total of 4337 mosquitoes belonging to 14 species and five genera were collected during the study period. Culex was the most dominant genus accounting for 84.41% of total catch followed by Anopheles (5.74%), Aedes (4.54%), Mansonia (2.93%) and Armigeres (2.38%). Total eight species of genus Culex were caught and their order of predominance was Cx. tritaeniorhynchus (30.81%), Cx. quinquefasciatus (28.50%), Cx. gelidus (17.24%), Cx. pseudovishnui (11.85%), Cx. vishnui (8.11%), Cx. fuscocephala (2.70%), Cx. infula (0.76%) and Cx. bitaeniorhynchus (0.03%) [Table 1].
Table 1: Distribution of Japanese encephalitis vectors in Bareilly region, Uttar Pradesh, India

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Seasonal mosquito fluctuation of JE vectors

In the present study, seasonal mosquito population of JE vectors showed two peaks [Figure 1]. The pre-summer peak in February to March was due to Cx. quinquefasciatus followed by Cx. tritaeniorhynchus. The second peak was seen in August to October (monsoon and post-monsoon) where Cx. gelidus and Cx. tritaeniorhynchus contributed maximum out of the entire population [Figure 2]. The combined mosquito population was found higher in summer and during monsoon period, while it gradually declines to lower level in colder months of year. Culex tritaeniorhynchus, a principal JE vector in India was found throughout the year [Figure 2]. Each individual species showed seasonal pronounced variation in its population during entire study. The majority of JE vectors showed maximum population density in post-monsoon and monsoon season. Population size was substantially reduced during peak winter season (November–January). The statistically, high significant difference (p < 0.001) was observed in mosquito populations during summer, monsoon and winter seasons.
Figure 1: Monthly mosquito population during Feb 2016-Jan 2017 in the Bareilly region of Uttar Pradesh.

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Figure 2: Seasonal occurrence of JE vectors in Bareilly region of Uttar Pradesh.

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Relationship of different weather variables with mosquito population

To determine the role of temperature, humidity and rainfall in shaping the seasonal profile of mosquitoes a Pearson’s correlation coefficient and multiple linear regressions were applied by using PROC REG procedure of SAS 9.3. The following multiple regression model was formulated:

y=a + b1X1 + b2X2 + b3X3 + b4X4 + b5X5 + e

Where, y=Mosquito population; X1=Maximum temperature; X2=Minimum temperature; X3= Rainfall; X4=Minimum relative humidity; X5=Maximum relative humidity; e=Error term; a=Intercept; and b1, b2, b3, b4 and b5 are the regression coefficients.

Association of mosquito population with weather variables is presented in [Table 2] and explained in [Figure 3]. From the [Table 2], it is evident that mosquito population is positively associated with all the weather parameters. However, none of the correlations coefficients are statistically significant.
Table 2: Association of mosquito population with weather variables according to Pearson's correlation coefficient multiple regression model

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Figure 3:

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{Figure 4}{Figure 5}

The relationship of the weather variables and mosquito population was obtained using multiple regression equation which is given below:

y = −320.801 + 22.966X1 −7.283X2 + 0.064X3 + 8.792X4 −3.926X5

From the fitted regression equation, it was evident that mosquito population increased with increase in the maximum temperature (21–39°C), rainfall and minimum relative humidity (40–60%). While, with the change in minimum temperature from 12° to 8°C (increase in value of minimum temperature) mosquito population decreased. The maximum relative humidity was recorded 99% throughout the year. However, it was found that out of the five variables tested, none of them were significantly associated with mosquito abundance.

The goodness of the fit of the regression model is determined by coefficient of determination (R2). The value of R2 was found to be 0.32 which explained only 32% variation in weather variables along with the time (month), with mosquito population.


  Discussion Top


Japanese encephalitis is a re-emerging zoonotic disease which is endemic in several parts of India including Uttar Pradesh. Mosquitoes play an important role in transmission of JE virus to human beings and thus their monitoring is important to initiate effective control measures. So far, no study has been undertaken on the prevalence of JE vector in Bareilly region of Uttar Pradesh. Therefore, a prospective entomological study to record the seasonal abundance of different JE vectors in Bareilly district was carried out in order to design appropriate vector control strategies to reduce the probability of future outbreaks.

In the present study, a total of 4337 mosquitoes were collected, amongst which Culex mosquitoes were most abundant (3661). Similarly, species of Culex mosquitoes were found to be dominant in other entomological studies, carried out in different endemic areas of Uttar Pradesh[22],[23]. One of the reasons, would be the presence of stagnant polluted water containing decayed organic matter, which provides suitable breeding habitat for these mosquitoes[24]. From the study area, mosquito species of five genera were found. The Indian mosquito fauna include 255 species grouped under 16 genera; 58 species belong to genus Anopheles, 57 species to Culex, 111 species to Aedes and seven species to Mansonia[25]. There is an evidence of 67 species of mosquitoes belonging to 11 genera, reported in a long-term ecological study conducted in Gorakhpur region of Uttar Pradesh[15]. In the present study, eight Culex mosquito species were found, which includes Cx. tritaeniorhynchus, Cx. quinquefasciatus, Cx. gelidus, Cx. vishnui, Cx. pseudovishnui, Cx. bitaeniorhynchus, Cx. infula and Cx. fuscocephala. In India JE virus has been isolated from 16 mosquito species[26]. Out of 16 species, 10 belongs to Culex, viz. Cx. tritaeniorhynchus, Cx. vishnui, Cx. psedovishnui, Cx. gelidus, Cx. quinquefasciatus, Cx. fuscocephala, Cx. infula, Cx. bitaeniorhynchus, Cx. whitmorei and Cx. epidesmus. Mosquito species of Cx. vishnui subgroup and Cx. gelidus are the major common vectors of JE in different parts of the country[27], however, Cx. quinquefasciatus, Cx. whitmorei, Cx. bitaeniorhynchus, Cx. infula and Cx. fuscocephala are also incriminated as vectors of JE[26]. All the above mentioned species except Cx. epidesmus and Cx. whitmorei were found around pigsties during the study period indicating vulnerability of study area for JE.

Results of this study also represented the seasonal variation in mosquito population. The total mosquito population showed two density peaks, one short peak in the month of February to March due to abundance of Cx. quinquefasciatus followed by Cx. tritaeniorhynchus. The population of Cx. quinquefasciatus increased during these months due to sudden rise in mean air temperature to the range from 12–29 °C[28]. The second high peak was observed in the months of September and October, due to high prevalence of Cx. tritaeniorhynchus and Cx. gelidus. The population dynamics of Cx. tritaeniorhynchus is closely associated with paddy cultivation as nursery paddy beds, puddles and paddy fields are preferred breeding habitats for this species[29]. In Uttar Pradesh, single rice crop is grown per year[30] (from May–July to September–December), which might be responsible for single JE vector peak (mostly in September) in the area[8]. Hence, period from May to October is considered as JE transmission period and most of the cases were reported during this period[31]. The results of present study were found in accordance with other researchers[9], who reported a single short early summer peak of Cx. quinquefasciatus in the month of March–April and a high late monsoon peak of Cx. tritaeniorhynchus in the month of September in Gorakhpur, Uttar Pradesh[32]. Similarly, Kanojia and Geevarghesh[15] also found a single peak of Cx. quinquefasciatus in the month of March–April and the species was least prevalent in the month of September to October. While in southern India, two high peaks of JE vectors has been recorded as paddy crop is grown twice per year[11],[33],[34]. In this study Cx. tritaeniorhynchus was found throughout the year around pigsties, the number of pigs in farm could be the factor associated with this prevalence, as earlier studies have indicated that pigs are preferred feeding hosts for Cx. tritaeniorhynchus[35],[36].

The Cx. gelidus was found abundant in the post monsoon period from September to October, which might be due to the availability of marshy water pools[13], as these species breeds profusely in rice fields and ground pools[37],[38] as well as in fresh and dirty water with high concentration of organic matter, i.e. marshes and waste water canal[39],[40].

Other three JE species, Cx. fuscocephala, Cx. infula and Cx. bitaeniorhynchus altogether contributed only 3.49% of total catch. The JEV has been isolated from Cx. fuscocephala once in Mandya district, Karnataka[12] and six times in Cuddalore district, Tamil Nadu[33]. Atleast two JEV isolations were made from Cx. bitaeniorhynchus, one in Bankura, West Bengal[10] and the other in Kolar, Karnataka[12]; whereas single isolation of JEV was done from Cx. infula in Madurai[26] indicating its role in JEV transmission.

Temperature and humidity are known as primary drivers for mosquito occurrence[41]. In the present study, the tested weather variables including rainfall, minimum temperature, maximum temperature; minimum and maximum relative humidity were found to have least effect on shaping mosquito dynamics. Pearson’s regression coefficient explained only 32% effect of weather variables on mosquito population revealing that other environmental factors are also playing major role in shaping mosquito densities. Further, statistically highly significant difference was found in mosquito populations in different seasons. It is evident that global average air temperature has increased by around 0.85°C since 1880, and each decade has been warmer than its predecessor[42]; and it is well established that climate change influences vector distribution and habitat suitability of vector[43].

During the study period mosquito abundance was recorded throughout the year with only decline in colder months (November–January). The rise in mosquito population was observed with increase in maximum temperature range from 21–39°C, at 90% maximum relative humidity and, 40–60% range of minimum relative humidity throughout the year. Regis et al[44] explained that the temperature ranging from 22–32°C and relative air humidity between 70 and 90% throughout the year is a factor favouring mosquito breeding all year round. The higher temperature during early spring hastens the breeding season and increases the density[45]. Further, at lower temperatures (8–10°C), the mosquito population decrease, as only few eggs are capable of hatching at this temperature[46]; and the temperature-dependencies will not be same among the stages, leading to non-linearities in population responses to temperature[47],[48]. The average rainfall during the study period was 47 mm and minimum relative humidity was between 40 and 60%. Even, with this low rainfall and low minimum relative humidity, mosquito abundance was noticed, which might be due to the availability of sufficient breeding sites in the form of irrigated agricultural lands, stagnant water pools and nearby localization of swine farm which provided adequate blood meal to the mosquitoes.


  Conclusion Top


Abundance of several species of JE vectors was determined through this prospective entomological study in the Bareilly region of Uttar Pradesh, which indicates the vulnerability and possible threat of future JE outbreaks in the study area. The vectors were found throughout the year with highest peak in monsoon and post-monsoon period. Implementation of continuous vector control and surveillance programme in western Uttar Pradesh is the need of the hour. Further, a long-term entomological study is required to better understand the population dynamics of existing vector populations and to evaluate how it depends on different environmental factors including weather variables.

Conflict of interest

Authors don’t have any conflict of interest.


  Acknowledgements Top


The authors are highly thankful to Dr Ashwani Kumar, Scientist ‘G’, National Institute of Malaria Research, Goa and the laboratory staff for providing training on mosquito identification. The authors are also grateful to Dr S. Ghosh, Division of Parasitology, IVRI, for providing laboratory facilities and ICAR-outreach programme on zoonotic diseases for financial grant to conduct the present study.



 
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    Figures

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  [Table 1], [Table 2]


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