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| RESEARCH ARTICLE |
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| Year : 2021 | Volume
: 58
| Issue : 3 | Page : 265-272 |
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Seasonal abundance and infection of Japanese encephalitis vectors from Gorakhpur district, Uttar Pradesh, India
Philip Samuel Paulraj, Velayutham Thenmozhi, Sunil Kumar Mishra, Jaganathasamy Nagaraj, Rajaiah Paramasivan
ICMR-Vector Control Research Centre, Field Station, Department of Health Research, No.4, Sarojini Street, Chinnachokkikulam, Madurai 625002, Tamil Nadu, India
| Date of Submission | 26-Mar-2020 |
| Date of Acceptance | 15-Aug-2020 |
| Date of Web Publication | 15-Feb-2022 |
Correspondence Address:
Philip Samuel Paulraj
ICMR-Vector Control Research Centre, Field Station, Madurai, Department of Health Research, No.4, Sarojini Street, Chinnachokkikulam, Madurai-625002, Tamil Nadu
India
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0972-9062.321740
Background & objectives: Japanese encephalitis (JE) is a major public health problem in many states of India. Uttar Pradesh state contributes 75% of the total cases reported. A longitudinal study was undertaken to find out the seasonal abundance, infection in the JE vectors in Gorakhpur region of Uttar Pradesh, and intervention strategies like indoor residual spraying and long-lasting insecticidal nets were adopted.
Methods: The vector abundance was monitored from July 2013 to August 2016 at fortnightly intervals and identified using standard mosquito identification keys and screened for viral infection. Intervention measures like indoor residual spraying with lambda-cyhalothrin 10% WP at 25 mg/m2 in 58 gramasabha in Bhathat Block and long-lasting insecticidal nets were distributed @ 2 LLIN for each household with 5-6 members in 5 villages of Korabar block.
Results: A total of 5,36,609 mosquitoes constituting 34 species and 10 genera were collected during this study period. Among the JE vector, peak abundance of Culex tritaeniorhynchus was recorded just before the JE season from July to October in all the blocks. There was a marked reduction in the density of Cx. tritaeniorhynchus from July compared to baseline year 2014 in Bhathat Block where indoor residual spraying (IRS) was performed in June 2015. The vector density declined in 5 villages of Khorabar Block where long-lasting impregnated bed nets (LLINs) were distributed during July 2016.
Interpretation & conclusion: The present study provided knowledge about the seasonal JE vector density and JE virus infection in mosquitoes during the monsoon season in Gorakhpur region of Uttar Pradesh. IRS and the personal protection measure like LLINs were distributed to interrupt the JE transmission in this area which gave encouraging results. Keywords: Japanese encephalitis; mosquito; Gorakhpur; Cx. tritaeniorhynchus
How to cite this article:
Paulraj PS, Thenmozhi V, Mishra SK, Nagaraj J, Paramasivan R. Seasonal abundance and infection of Japanese encephalitis vectors from Gorakhpur district, Uttar Pradesh, India. J Vector Borne Dis 2021;58:265-72 |
How to cite this URL:
Paulraj PS, Thenmozhi V, Mishra SK, Nagaraj J, Paramasivan R. Seasonal abundance and infection of Japanese encephalitis vectors from Gorakhpur district, Uttar Pradesh, India. J Vector Borne Dis [serial online] 2021 [cited 2023 Mar 29];58:265-72. Available from: http://www.jvbd.org//text.asp?2021/58/3/265/321740 |
| Introduction | |  |
Japanese encephalitis (JE) is a severe viral zoonotic disease[1],[2],[3]. An estimated 3 billion population lives in JE prone areas and JE is reported in new areas globally[4] and regionally[5]. About 45,000 cases of JE, ten thousand deaths and 15,000 survivors were reported to the WHO each year. Only about 1 in 250–500 infected individuals manifest clinical disease[6]. Annually 50,000 JE cases are reported in Asia, including India[7]. Japanese encephalitis transmission includes Culex mosquitoes as vector and Ardeid water birds as primary reservoirs, while pig acts as an amplifier host[8]. A higher incidence of JE was reported in Gorakhpur from 1978 onwards[9],[10],[11],[12],[13],[14]. The incidence of JE varies between 0.8 and 3.5 cases per lakh population in different blocks. Gorakhpur district of Uttar Pradesh showed 10.4% clinical samples found positive for JE by IgM ELISA[15]. Several studies on JE were undertaken in different parts of the country as recorded from south to North - Cuddalore, Tamil Nadu[16],[17],[18],[19],[20],[21], Thanjavur, Tamil Nadu[5],[19],[21], Kuttanadu, Kerala[22],[23], Kurnool, Andhra Pradesh[24], Karnataka[25],[26],[27], West Bengal[28], and Gorakhpur[29],[30],[31],[32],[33]. The information on vector mosquito species distribution in Uttar Pradesh is carried out in different time intervals[31],[32],[33],[34]. Gorakhpur underwent drastic ecological changes by the construction of irrigation canals and small dams. Promotion of agriculture in many areas of this region resulted in the extension of water bodies to far-flung areas which supported and promoted vector mosquito breeding and thus made several environmental changes by habitat modification. These factors must have caused the outbreak of JE in this area. The basics of mosquito fauna along with the vector population from this area are considered as very useful information to take up vector control strategies[31]. Therefore, this study was undertaken in Gorakhpur from 2013–16 to determine the vector species distribution pattern in the Gorakhpur area of UP and to undertake vector control measures like indoor residual spraying and long-lasting impregnated bed nets before peak vector abundance and JE season to reduce the disease burden.
| Material & Methods | | |
Study area
Gorakhpur is a main paddy cultivating area in Uttar Pradesh. Gorakhpur district, in Uttar Pradesh, is found situated at 26° 46’ North latitude and 83° 22’ East longitude and occupies a total region area of 3483.8 sq.km. with a population of 44, 40, 895 (2011 census). Rice is the major crop during the Kharif season (1,52,497 hectares) in this area and 84.72% of total 2,48,723 hectares agricultural land is irrigated. Canals, ponds, and open wells are used as sources of irrigation in 5472, 1628, and 608 hectares respectively. There are several water sources present acting as potential breeding grounds for many migratory birds. In the paddy region, cultivated areas found many egrets and herons which are reservoirs of JEV. Paddy is cultivated in all the 3 seasons, i.e., October to February (winter season), March to June (summer season) and July to September (monsoon season). Sugarcane, wheat, pea, and rapeseed mustard are identified as the other crops cultivated in this district. Many water resources are found throughout the year and paddy cultivation yielded maximum income in rural areas. In the urban areas, agriculture and pig rearing is prevalent and practiced by many small and marginal farmers in that area. Gorakhpur district comprised of 19 blocks and one municipality. From this, three blocks viz. Bhatahut, Khorabar, and Chargawan reported JE incidence: 3.5, 1.8, and 3.5, per lakh population respectively (population: ~1.5 lakh; households: ~30,000 per block) were selected for implementing research-cum-intervention studies [Table 1] & [Figure 1]. The villages of Gorakhpur constitute many water bodies and promote paddy cultivation during the JE transmission season (July–November). Entomological investigations were conducted in JE affected villages in the Gorakhpur district. | Table 1: List of index villages selected for this studies (Gorakhpur district, India)
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Mosquito collections, identification and control
Resting mosquitoes were collected after dusk hours from vegetation and bushes around cattle sheds and pigsties using mechanical aspirators and transported to the laboratory for identification. JE vector abundance was determined by indoor resting collections conducted in human dwellings and cattle sheds, outdoor resting collections on outdoor vegetation using drop nets and dusk collections in three blocks Bhatahut, Khorabar and Chargawan of Gorakhpur area on fortnightly basis for the period of three years, i.e., July 2013 to August 2016 by hand collection using the battery-operated aspirators. The trapped mosquitoes were transferred to the field laboratory for further investigation. All the collected mosquitoes were finally identified into different species level using standard mosquito identification keys[35], segregated, counted, and screened for viral infection[16]. Per man hour density for the dusk collections were calculated individually for all the species based on female mosquitoes collected in the dusk period. Indoor residual spraying (IRS) Lamdacyhalothrin 10% was carried out in 58 gramasabha in Bhathat Block in June 2015. In addition to this 2187 long-lasting impregnated bed nets (LLINs-PermaNet 2.0) were distributed to 1978 households covering 4870 populations distributed @ 2 LLIN for each household with 5–6 members in 5 villages of Korabar block during July 2016.
Meteorological data collection
The Gorakhpur Climate data with meteorological variables like temperature, relative humidity, and rainfall were obtained from World Weather Online (www.worldweatheronline.com)[36].
Statistical analysis
All the data sets were carefully stored in Microsoft Excel and analyzed using SPSS software (version 26.0). PMHD was expressed as the Geometric Mean ± SD. ANOVA test was used to whether check any significant difference found between the seasons and blocks into vector abundance (individual species wise) variations were considered statistically significant when the P-value was less than 0.05.
Ethical statement: This study was approved by the Centre’s human ethics committee.
| Results | | |
A total of 5, 36, 609 mosquitoes constituting 34 species and 10 genera were obtained during this study period. Culex quinquefasciatus (77.16%) was the predominant mosquito in the collection followed by Cx. tritaeniorhynchus (6.16%), Cx. gelidus (0.95%), Cx. vishnui (0.46%), Cx. pseudovishnui (0.41%), Cx. whitmorei (0.32), Cx. epidesmus (0.06) and Cx. infula (0.01%) [Supplementary Table 2]. There is a peak abundance of Cx. tritaeniorhynchus mosquitoes recorded from July to September in all the blocks. A total of 24 species including major JE vectors were collected in the mosquito collections from pigsties. This study showed a seasonal JE vector pattern in the dusk collections with one peak by Cx. tritaeniorhynchus seen in July to December (monsoon and post-monsoon) whenever paddy cultivation is in progress. The maximum population of the JE vector was observed during the monsoon and post-monsoon period [Table 2] & [Figure 2]. | Figure 2: PMH and pools positive of Culex vishnui subgroup species in Gorakhpur district, India (2013–2016)
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 | Table 2: Mosquito catches in 3 blocks of Gorakhpur district, India during 2013–2016
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Culex tritaeniorhynchus density is significantly high in the monsoon season in all three blocks (P<0.05). Cx. vishnui has significantly differed between seasons (P<0.05) in two blocks except for Khorabar and PMHD significantly high in Monsoon season in two blocks Bhatahut and Chargawan (P<0.05). Culex pseudovishnui is significantly different between seasons (P<0.05) in three blocks and PMHD is significantly high in the monsoon season in all three blocks (P<0.05). Culex tritaeniorhynchus is the predominant species and PMHD is high in monsoon season for all three species [Table 3]. In the Pigsties collection, Cx. tritaeniorhynchus is the predominant species and PMHD is significantly high in Monsoon season in all three blocks (P<0.05).Culex vishnui and Cx. pseudovishnui are not statistically significant (P>0.05) in three blocks and seasons in Pigsties collection [Table 4]. | Table 3: Seasonal geometric mean abundance (PMHD ± SD) by area and season for Cx. tritaeniorhynchus, Cx. vishnui and Cx. pseudovishnui in Gorakhpur district, India (Indoor resting collection - IRC).
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 | Table 4: Seasonal geometric mean abundance by area and season for Cx. tritaeniorhynchus, Cx. vishnui and Cx. pseudovishnui in Gorakhpur district, India (Pig shed collection - PSC).
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In the Khorabar block, per man-hour density (PMHD) and pool positives were high in Cx. tritaeniorhynchus species with 8 positive pools from Cx. tritaeniorhynchus, 1 positive pool from each Cx.vishnui and Cx. pseudovishnui reported 2 JE cases and 113 AES cases between July 13 to December 15. In the Bhatahat block, PMHD and pool positives were high in Cx. tritaeniorhynchus species (4 pools) detected positive on July 13 to Aug 16. 2 out of 4 positive pools observed in 2014 reported more AES cases (22) in 2014. No positive pools were observed from Cx. vishnui and Cx. pseudovishnui species during the period of 2013 -2016. In Chargawan block, PMHD and pool positives were high in Cx. tritaeniorhynchus species with positive pools in Cx. tritaeniorhynchus (7) and 1 positive Cx. vishnui pool found positive on July 2013 to December 2015. 6 out of 8 pools positives were observed in 2014 and 2015.AES cases were reported high in 2014 (101 cases) and 2015 (75-AES and 1-JE) during this period. No pools were observed positive in the Cx. pseudovishnui species of mosquitoes during this period 2013–2016. PMHD positive pools and cases showed the relationship in [Figure 3] [Supplementary Table 1] [Additional file 1] & [Supplementary Table 2] [Additional file 2]. The density of Cx. tritaeniorhynchus is significantly correlated (P < 0.05) with climatic factors (rainfall and minimum temperature) in all types of collections. Vector abundance and climatic factors correlation with Cx. vishnui and Cx. pseudovishnui was shown in [Supplementary Table 3] [Additional file 3]. | Figure 3: Correlation of rainfall (Avg.) and JE & AES cases in Gorakhpur district, India (2013-2016)
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In Gorakhpur, we collected 93.98% mosquitoes from indoor collections and only 6.02% in outdoor collections. This is a major study carried out very recently which showed the shifting of resting behavior of these mosquitoes towards indoors (endophilic). This observation prompted us to use the IRS and LLIN for control. After completion of the IRS in June 2015, there was a marked reduction in the density of Cx. tritaeniorhynchus as compared to the previous year in Bhathat Block [Figure 4]a. Vector density declined in the Korabar block, where LLINs were distributed in 5 villages during July 2016 [Figure 4]b. | Figure 4: (a) Effect of intervention (IRS spray) on indoor resting density (per man-hour) of Cx. tritaeniorhynchus in human dwellings in Bhathat block. Arrow indicated the time point when IRS was sprayed (b) Effect of intervention (LLIN distribution) on indoor resting density (per man-hour) of Cx. tritaeniorhynchus in human dwellings in Khorabar block. Arrow indicated the time point when LLINs were distributed
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| Discussion | | |
JE virus has been isolated from 16 mosquito species[17]. Culex tritaeniorhynchus was the predominant species in this investigation. PMHD vector abundance of Cx. tritaeniorhynchus was significantly higher in monsoon season. The overall vector population showed a peak during the monsoon months from July to December. This study showed a seasonal variation in the mosquito population and its peak abundance was observed from July to September and October to December. In UP state, only one paddy cultivation is practiced per year from May–July to September–December. Due to this reason, only one peak JE vector density was observed during September. Thus more JE cases occurred in this season. Earlier Gorakhpur studies showed a peak abundance of Cx. tritaeniorhynchus prevalent in July–November. Average rainfall also recorded high in this period (July–November) in Gorakhpur [Figure 3].
In most of the JE vector studies conducted in south India showed two peaks of JE vectors abundance recorded as per the rice cultivation are practiced two times a year[16],[17],[18],[19],[20],[21],[23],[24],[26],[38],[39],[40],[41],[42]. In north West Bengal, the adult mosquitoes’ collections indicated that various habitats were contributing vectors throughout the year. More than 50 percent of the potential JE vector species obtained through the dusk collection and the remaining through other collections pointed out that people in this area were at a risk for transmission of JE[28]. In Gorakhpur area, extensive paddy cultivation, many water bodies, and puddles found in uncultivated areas act as the potential immature breeding grounds of many Culex species[29],[32],[33],[43] and the peak abundance of the primary vector Cx. tritaeniorhynchus and rest of the Culex vishnui species subgroup mosquitoes were observed in the JE occurring period in Gorakhpur[15],[32],[33],[37].
In the JE affected areas, many JEV isolations were reported from the Cx. vishnui subgroup reported from different areas[16],[18],[19],[20],[21],[22],[23],[24],[26],[34],[38],[39],[40],[41] of mosquitoes which again showed their capacity to transmit the virus in the laboratory[22],[41]. Most of the studies showed higher infection recorded in Cx. tritaeniorhynchus as observed here. Cx. vishnui subgroup mosquitoes were recognized as the principal vectors and play a major part in the transmission of JE in India. JEV isolation was reported from 1991 to 2007 outbreaks[16],[22],[33],[44]. Pigs are widely seen in many places and reared in many places of Gorakhpur[33]. Pigs in large numbers and peak vector abundance are responsible for the JEV transmission[32]. In this study, more pools were found positives in Cx. tritaeniorhynchus in 2014 and 2015 particularly monsoon season with JE case (n-2) and also more AES (n-266) cases in 2014 and 2015. In this study Cx. tritaeniorhynchus was found nearby pigsties that help to feed and promote transmission[18],[45]. Rice cultivation in the fields and pig rearing by many people noticed are associated with the risk of JE. Due to this, potential risk factors are playing outdoors after dinner, residence nearby rice fields, and pig ownership by the family or next-door neighbours[46]. This study showed peak vector density and the presence of the amplifying hosts’ pigs in many areas which will facilitate and maintain a complete transmission cycle in this area. Similarly, many areas are at risk for this disease expansion and recently its spread to new territories has been reported globally[4] and regionally[5]. To check the further spread of this disease to new areas and to protect the vulnerable target group present in this area, IRS and distribution of LLINs were undertaken in these areas which showed encouraging results. LLINs will kill, repel, and prevent man and mosquito vector contact. Some studies have already proved this technique for control of JE vectors[47].
| Conclusion | | |
Vector abundance determined by vector surveillance from this study in the Gorakhpur, Uttar Pradesh, India showed the vulnerability of this area for JE outbreaks. The peak vector abundance was observed during the monsoon period. Intervention methods like IRS and the distribution of LLINs employed in this area yielded encouraging results. Implementation of the continuous vector surveillance program, vector control, and JE vaccination in Gorakhpur areas of Uttar Pradesh curtailed the JE transmission. The available technologies and knowledge should be attempted to be transferred to the communities for regular utilization and practice by them to prevent the occurrence of new cases of JE.
Conflict of interest: None
| Acknowledgements | | |
Authors thank the Secretary, Department of Health Research (DHR), Ministry of Health & Family Welfare, and the Director-General, ICMR for financial support. Sincere thanks are due to Director, ICMR-VCRC, Dr. P. Jambulingam previous Director of ICMR-VCRC, Puducherry and Dr. B. K. Tyagi, Director in-charge, CRME, Madurai for providing all the requisite facilities and for the constant encouragement, guidance and useful suggestions for undertaking this study and all the supporting staff of CRME, Madurai for their wholehearted support in this endeavor. We thank the state health authorities of Uttar Pradesh state, BRD Medical College, Gorakhpur, and Officials from NIV FS, Gorakhpur for providing the needed facilities to undertake these studies.
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[Figure 1], [Figure 2], [Figure 3], [Figure 4]
[Table 1], [Table 2], [Table 3], [Table 4]
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