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Table of Contents
RESEARCH ARTICLE
Year : 2018  |  Volume : 55  |  Issue : 4  |  Page : 291-296

Mosquito abundance and pig seropositivity as a correlate of Japanese encephalitis in human population in Assam, India


1 Department of Veterinary Public Health, College of Veterinary Science, Assam Agricultural University, Guwahati, Assam, India
2 Department of Veterinary Microbiology, College of Veterinary Science, Assam Agricultural University, Guwahati, Assam, India
3 Department of Parasitology, College of Veterinary Science, Assam Agricultural University, Guwahati, Assam, India
4 ICAR–National Research Centre on Equines, Hisar, Haryana, India

Date of Submission22-Dec-2017
Date of Acceptance02-Apr-2018
Date of Web Publication18-Apr-2019

Correspondence Address:
Baldev R Gulati
ICAR–National Research Centre on Equines, Sirsa Road, Hisar–125 001, Haryana
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.256564

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  Abstract 

Background & objectives: Assam is the most vulnerable state for Japanese encephalitis (JE) in India. The situation warrants characterization of epidemiological patterns of JE in vectors, pigs and human population. This investigation was aimed to determine the relative abundance of mosquito species and seroprevalence of JE in pigs in order to draw an epidemiological association with reported human JE cases in Assam.
Methods: Pig sera and mosquitoes from selected farms in Sivasagar and Kamrup districts of Assam were collected fortnightly for one year during June 2015–May 2016. Pig sera were tested for JE antibodies by haemagglutination and virus neurtralization tests. Mosquito species were identified microscopically following the taxonomic keys. The results were analyzed with data on confirmed human JE cases in the selected districts.
Results: Culex gelidus (26.07%) and Cx. tritaeniorhynchus (24.07%) were the most abundant species in collected mosquitoes (n = 997). A total of 22.99% of pigs (n = 335) were JEV seropositive and 45.65% of human acute encephalitis syndrome cases (n = 230) were positive for JE virus (JEV) infection. Relative mosquito abundance, pig positivity and human cases were highest during monsoon (June–September) and least during winter (December–February). Rise in mosquito population was observed during pre-monsoon season (March–May) and concurrently higher number of human cases and pig seropositivity were recorded. A good correlation was observed between mosquito number and JEV positivity in pigs/human, and between pigs and human cases (p < 0.05). Human population in Sivasagar was at higher risk for JE infection (OR: 6.46, p < 0.0001) than in Kamrup rural district.
Interpretation & conclusion: This study indicates that a seasonal correlation exists between mosquito abundance and JEV seroconversion in pigs with concurrent human JEV outbreaks under field conditions in Sivasagar and Kamrup rural districts of Assam and that monitoring mosquito abundance/density and pig JEV seropositivity may help in predicting JEV outbreak in human population in the region.

Keywords: Assam; human; Japanese encephalitis, mosquito; pig


How to cite this article:
Baruah A, Hazarika RA, Barman NN, Islam S, Gulati BR. Mosquito abundance and pig seropositivity as a correlate of Japanese encephalitis in human population in Assam, India. J Vector Borne Dis 2018;55:291-6

How to cite this URL:
Baruah A, Hazarika RA, Barman NN, Islam S, Gulati BR. Mosquito abundance and pig seropositivity as a correlate of Japanese encephalitis in human population in Assam, India. J Vector Borne Dis [serial online] 2018 [cited 2021 May 11];55:291-6. Available from: https://www.jvbd.org/text.asp?2018/55/4/291/256564




  Introduction Top


Japanese encephalitis (JE) is a serious mosquitoborne zoonotic viral disease in Southeast Asia. The etiologic agent, Japanese encephalitis virus (JEV) is a RNA virus belonging to genus Flavivirus under Flaviviridae family. About 67,900 global human JE cases occur annually, with 30% case fatality[1],[2],[3]. Approximately three billion people live in JE endemic regions. The geographical distribution of JEV is expanding and it is now considered a potential global public health threat[4]. Among animals, JEV causes reproductive disorders in pregnant sows and encephalitis in horses. High viraemia in pigs without displaying any overt clinical signs except abortion, and still birth in pregnant sows contributes significantly to the perpetuation of the disease[5]. Moreover, the presence of JEV-infected pigs in peridomestic areas increases the chances of spill over of infection to human, especially when the mosquito density is high. In the present scenario, where ‘one health approach’ has become sine qua non of public health system, the vector borne zoonotic diseases like JE need careful attention of veterinarian[6].

The principal vector species is Culex tritaeniorhynchus, which has high abundance in rainy season in both the tropical and temperate regions[7]. The natural cycle of JEV consists of pig-mosquito-pig or bird-mosquito-bird cycles[8]. In India, maximum virus isolations have been made from Cx. vishnui group consisting of Cx. tritaeniorhynchus, Cx. vishnui and Cx. pseudovishnui[9].

Assam is the Northeastern state of India and its economy is mainly dependent on agriculture and allied activities. Rice is the main crop of Assam and occupies about two-third of the total cultivated area in the state. Assam also has the largest pig population in the country accounting for 17.96% of the country's total pig population and the state has witnessed over 6% growth in pig population[10] during 1994–2012. Abundance of rainfall, rice and pig farming makes Assam the most vulnerable state for spread of JE. The disease has appeared in sporadic outbreaks or epidemic forms in upper Assam since 1976, but deaths due to JE showed an increasing trend from 1999 with spread of the disease to newer areas in the state[11],[12],[13]. As per the National Vector Borne Disease Control Programme, India (www.nvbdcp.gov.in/index.php), maximum numbers of JE cases in India have been reported from Assam, continuously since 2011. The situation warrants characterization of epidemiological patterns of JE in mosquito vectors, pigs and human population in the state.

Although, JEV has been detected from pigs in other parts of India[6],[14],[15], there is limited information on JE status in pigs from Assam[16],[17]. The present investigation was undertaken to determine the relative abundance of mosquito species and seroprevalence of JE in pigs in different seasons and to draw an epidemiological association of reported human JE cases with pig seropositivity and mosquito abundance under field conditions in Sivasagar and Kamrup rural districts of Assam.


  Material & Methods Top


Study area

The study was conducted in Sivasagar and Kamrup rural districts of Assam, India from June 2015 to May 2016. Sivasagar district lies between 26.45–27.15 °N latitudes and 94.25–95.25 °E longitudes and is bounded by the Brahmaputra River on the north, Nagaland on the south, Charaideo district on the east and the Jhanji River on the west. Kamrup rural district lies between 25.46–26.49 °N latitudes and 90.48–91.50 °E longitudes and is bounded by Udalguri and Baska districts in north, Meghalaya in south, Darrang district and Kamrup metropolitan in the east; and Goalpara and Nalbari districts in the west.

Pigs sampling

A total of six pig farms from Sivasagar and five from Kamrup rural districts located close to rice fields and stagnant water were selected for collection of pig sera and mosquito samples. The pig serum samples were randomly collected from pigs of 3–6 months of age during the study period by fortnightly visits to the farms.

Collection and identification of mosquitoes

The mosquitoes were collected from inside and around the pig farms. Samples were collected during the dusk period (0500–0600 hrs) of the day. Collection method involved a sweeping mosquito net, measuring 12×12×12” with its sleeves completely folded, by a series of quick forward, backward, up and down movements for 2 min to disturb the resting mosquitoes on the vegetation; and in the process they were trapped in the net. The sleeve of the net was immediately folded and the trapped mosquitoes were retrieved by an aspirator tube. Such attempts were made 10 times and collected mosquitoes were pooled[18]. The collected mosquito specimens were anaesthetized with chloroform soaked in a cotton ball in a jar and preserved into separate plastic boxes. Adult female mosquito numbers were sorted, counted and identified under a stereoscopic binocular microscope following the taxonomic keys[19].

Data collection on human JE

The data regarding clinical cases of acute encephalitis syndrome (AES) and JE in human populations for the two districts for the period under study were procured from State Surveillance Officer, Integrated Disease Surveillance Programme, Guwahati, Assam. Data of only those human cases were included that matched the WHO Japanese encephalitis surveillance standards[20] for AES and were laboratory-confirmed for JEV IgM antibodies in sera or cerebrospinal fluid by MAC ELISA kit (ICMR-National Institute of Virology, Pune, India).

Haemagglutination inhibition test

JEV isolate (eq/India/H225/2009, GIII) maintained at the ICAR–National Research Centre on Equines, Hisar (Haryana state) was used in the study. The virus was propagated in Swiss albino suckling mice via intra-cerebral inoculation for preparation of sucrose-acetone extracted antigen. The haemagglutination inhibition (HI) test was carried out in duplicate in 96-well microplates as described previously[21]. Hyper-immune serum to JEV previously raised in rabbits was included in each test as positive control. The HI titre was expressed as the reciprocal of the highest dilution of serum showing complete inhibition of haemagglutination. An HI titre of 20 and above was considered as positive.

Virus neutralization test

The porcine stable (PS) cells procured from the National Centre for Cell Sciences, Pune, India were used for virus neutralization test (VNT). The PS cells were grown in Eagle's minimal essential medium (EMEM) supplemented with 10% fetal bovine serum (FBS), 100 IU/ml penicillin, 100 μg/ml streptomycin, and 0.25 μg/ ml amphotericin-B (Sigma-Aldrich, USA). VNT was performed in 96-well tissue culture plates using 300 TCID50 of the JEV isolate (eq/India/H225/2009, GIII), essentially according to method described previously[21]. The neutralization titres were expressed as the reciprocal of the highest serum dilution that completed inhibited CPE in the wells. A titre of 4 and above was considered positive.

Statistical analysis

ANOVA was used to calculate critical difference and correlation analysis was used to find the association between different factors. The odds ratios were calculated using 2 × 2 contingency table[22].

Ethical statement

The animal experiments were duly approved by the Institute's Animal Ethics Committee of Assam Agricultural University, Guwahati, Assam.


  Results & Discussion Top


In total, 997 adult female mosquito samples were collected from the selected farms during the study period. The collection data were analyzed species-wise, month-wise and season-wise. Culex gelidus (25.99%) and Cx. tritaeniorhynchus (24.17%) were the most abundant adult mosquito species in the study area followed by Armigeres spp (14.93%), Cx. vishnui (12.07%) and Mansonia spp (8.55%) [Table 1]. Although, there was no statistical difference in relative mosquito population in two districts, Cx. tritaeniorhynchus (27.78%) was the most abundant species in Sivasagar district, whereas Cx. gelidus (29.35%) was the most abundant in Kamrup rural district [Table 1]. These mosquitoes breed in rice fields and stagnant/muddy water[23],[24]. Culex gelidus, Cx. tritaeniorhynchus, Cx. vishnui and Cx. quinquefasciatus have been reported earlier to be the important vectors for JEV transmission in India[25],[26],[27],[28],[29],[30]. Vector population abundance is known to be associated with the positivity of JE cases in endemic region[31] and regular monitoring of vector population trends might help in forecasting emergence of disease in pigs and human populations.
Table 1: Relative abundance of adult mosquito species in Sivasagar and Kamrup rural districts of Assam, India

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Out of 335 pigs below six months of age, 77 (22.99%) were positive for JEV antibodies in both HI and VNT tests. There was significantly higher JEV positivity in pigs from Sivasagar district (31.31%) than in Kamrup rural district (11.51%) [Table 2]. Out of 230 reported human AES cases during the year 2015–16, 105 (45.65%) were laboratory confirmed as JEV positive. There was significantly higher prevalence of JEV infection in human population in Sivasagar district (74.49%) than in Kamrup rural district (24.24%) [Table 3]. In addition to higher JEV seropositivity in pig population, Sivasagar district had significantly higher risk of JE incidence in human population (Odds ratio: 6.46, 95% CI 3.74–11.15, p < 0.0001) than in Kamrup rural (OR: 2.46, 95% CI 1.28–4.74, p < 0.01). There was significant correlation between mosquito abundance and JEV positivity in pigs (coefficient of correlation ‘r’ = 0.88) and human cases (r = 0.66). A good correlation (r = 0.71) between JEV seroprevalence in pigs and human cases was also observed in the two districts of Assam [Table 4].
Table 2: District-wise JEV seroprevalence in pigs

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Table 3: Prevalence of acute encephalitis syndrome (AES) and Japanese encephalitis (JE) infection in human populations in Sivasagar and Kamrup rural districts of Assam, Northeast India during 2015–16

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Table 4: Seasonal association between mosquito population and prevalence of Japanese encephalitis (JE) infection in pigs and human populations in Assam, Northeast India

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Confirmation of JEV infection in human population is not straightforward due to low and transient viraemia, low sensitivity of viral diagnostics like isolation and RTPCR-based assays or by IgM-ELISA due to associated cross-reactivity[32]. Therefore, serosurveillance in pigs in JEV endemic regions could be a first step in detecting JEV outbreaks in human population. The sentinel pigs have been previously used as indicator to confirm the emergence of the virus in pigs and vectors and to forecast the time of transmission in human population[16],[33],[34]. However, this is the first report of seasonal correlation under field conditions in vector population, pig seropositivity and human JEV cases. The findings establish that mosquito density and pig JEV seropositivity in the field may act as indicator for concurrent JEV cases in human population in the region.

The results on vector population abundance in this study and its correlation with human JE cases might be interpreted with a caution as the study could not demonstrate JEV in the mosquito samples collected from the study area (data not shown). However, it has been demonstrated previously that controlling vector exposure result in 66% reduction in JEV infections in pigs[17].

Seasonal influence was evident on mosquito abundance, pig seropositivity and human JEV cases. The relative mosquito abundance in both the districts was at peak during monsoon months (June–September) and least during winter months (December–February). It started rising during pre-monsoon (March–May) [Table 4], [Figure 1]. JEV seroprevalence in pigs was maximum (36%) during monsoon (June–September) and none of the pigs in winter season was seropositive [Table 4]. Similarly, JEV was confirmed in maximum number of human AES cases (93 out of 164, i.e. 56.71%) during monsoon season and none of the AES cases reported during winter months was JEV positive. During the peak of mosquito abundance, higher number of human cases and JEV seropositive pigs were recorded in monsoon season [Figure 1].
Figure 1: Mosquito population abundance and prevalence of Japanese encephalitis infection in pig and human population—(a) Month-wise; and (b) Season-wise.

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One of the reasons for vector abundance in Assam during monsoon season is standing water in rice fields which is highly suitable for mosquito breeding. Changing agricultural practices like selecting cropping patterns with reduced rice cultivation or switching from winter rice to autumn or summer rice cultivation might help to control JE outbreaks. Swine vaccination plays considerable role in reducing the spread of infection in animals as well as human population, and needs active consideration by policy makers.


  Conclusion Top


The present investigation revealed significant seasonal correlation in mosquito abundance, pig seropositivity and human JEV cases in Sivasagar and Kamrup rural districts of Assam. Since, confirmation of JEV infection in human population is tedious and time consuming process, monitoring mosquito density and JEV seroconversion in pigs under field conditions can help in forecasting emergence of JEV outbreak in human population. Thus, the present work provides scope for managing the JE outbreaks in Assam state. Similar data on mosquito density and pig JEV infection are needed from other JE endemic districts to develop model for forecasting and managing human JE outbreaks.

Conflict of interest

The authors of the current study declare no conflict of interest.


  Acknowledgements Top


The authors wish to thank the Assam Agricultural University, Khanapara, Guwahati and ICAR–NRCE, Hisar for infrastructure support. The support of the State Surveillance Officer, Integrated Disease Surveillance Programme, Guwahati, Assam for providing retrospective data on human JEV is also acknowledged. This study was funded by the Department of Biotechnology, Ministry of Science and Technology, Government of India (Grant No. DBT-NER/LIVS/11/2012).



 
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    Figures

  [Figure 1]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4]


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