記住我
REVIEW ARTICLES
Year : 2022 | Volume
: 59
| Issue : 4 | Page : 312-319
Changing Paradigm in the epidemiology of Japanese encephalitis in India
Philip Samuel Paulraj1, Veeramanoharan Rajamannar1, Govindarajan Renu1, Ashwani Kumar2
1 ICMR-Vector Control Research Centre, Field Station, Madurai, Tamil Nadu, India
2 ICMR Vector Control Research Centre, Puducherry, India
Correspondence Address:
Dr. Philip Samuel Paulraj
ICMR-Vector Control Research Centre Field Station, Department of Health Research, No. 4, Sarojini Street, Chinna chokkikulam, Madurai-625002
India
Source of Support: None, Conflict of Interest: None
CheckDOI: 10.4103/0972-9062.345180
Japanese encephalitis (JE) is a very serious public health problem in India and the conducive environment permit its emergence in non-endemic areas in the country. There are constant changes taking place in the pattern of current agricultural practices and vector breeding habitats which had far-reaching consequences on the epidemiology of JE and the severity of epidemic outbreaks today. Due to the continuous ecological changes taking place, vectors changed in their breeding dynamics, feeding, and resting behavior and started invading previously non-endemic areas. JE has recently spread to new territories due to land-use changes, including forest fragmentation and concentrated livestock production. Changes in the livestock population decreased the cattle pig ratio which enhanced the Japanese encephalitis virus (JEV) infection. This review brings forth the present widespread changes encountered that grossly impact the risk of infection in many places for the emergence of Japanese encephalitis and to address the implications for its control.
Keywords: Mosquito vectors; JE virus; distribution pattern; endemic; outbreak
Japanese encephalitis (JE) has its natural maintenance cycle involving pigs and/ or birds and man being only the incidental dead-end host in this devastating disease cycle. JE caused >1,00,000 cases and 25,000 deaths in 2015 globally[1]. Most JE virus infections are mild but 1 in 250 infections result in severe clinical illness. Japanese encephalitis virus (JEV) has transmission risk in many places[1] and more than 3 billion people i.e., approximately 60% of the world's population, lives in countries where JE is endemic. These populations are at risk of contracting JEV infection associated with areas supporting both rice paddies and pig farming[2]. Since the JEV is circulated in a zoonotic cycle within ardeid birds, pigs, and mosquito vectors, the presence of mosquito vector and infection in human/pig reported from different areas confirmed the geographical emergence in new regions for the expansion of Japanese encephalitis making this disease a public health concern in India. This study aims to bring out the changing paradigm in the transmission pattern of Japanese encephalitis as observed in many areas and to insist upon the necessity to implement JEV vaccination along with the required effective vector control strategies.
Key changes observed in the transmission of Japanese encephalitis (JE)
Disease scenario
The epidemiology of JE is continuously changing as there is a change in the incidence of JE, due to spread of JEV into new environments. Only one percent of the JE infections were symptomatic characterized by encephalitis and 99% are asymptomatic[3]. In an endemic Cuddalore district, Tamil Nadu state, the ratio of apparent to inapparent infection was found out to be 1:270[4]. JE mortality rate increases up to 30% in the confirmed cases[2]. Due to the rapid expansion of human population, JE global cases increased from 1.7 billion from the 1950s to 3.5 billion after fifty years[5]. Every year 1500 to 4000 JE cases are recorded in India as 43.08% population resides in the JE-reported areas. Since many JE cases are not recorded properly, the actual proportion of JE cases reported must be higher than recorded both in India and the world[6].
In India, the geographical range of JEV and several outbreaks of viral encephalitis are newly reported from many parts. At present, JE infection expanded throughout the country except for states of Gujarat, Jammu Kashmir, Dadra Nagar and Haveli, Daman and Diu, Lakshadweep, and Sikkim [Figure 1] & [Figure 2]. JE epidemics reported from 1955 to 2012 affected 152 districts of 20 states in India[7]. Due to the expanding geographical distribution in India [Figure 3], JE was declared as a notifiable disease in India.
Figure 1: Japanese encephalitis endemic and worst affected states in India (1973–2006).
Figure 2: Japanese encephalitis cases and outbreaks reported in India (1955–2005).
Figure 3: Geographical expansion of Japanese encephalitis in India (2006–2020).Vertebrate hosts
Many vertebrate hosts were found naturally infected with JEV, like cattle, goats, cats, dogs, birds, bats, snakes, pigs, and toads. During the new JEV transmission seasons, frogs, bats, lizards, and snakes develop viraemia which could infect the vector mosquitoes feeding on them[8]. Generally, pigs and ardeid birds found infected with this virus act as amplifying hosts and play a pivotal role in the natural infection cycle. Pig rearing and the industrialization of pig farming has increased significantly. The livestock census conducted in India comprised of 2.01% pigs to the total livestock population (www.dahd.nic.in). The pig population in India is estimated to be 10.29 million and it ranks 5th in the world. Out of the total pigs, 23.85% are either exotic or crossbred and the rest are indigenous; 89.62% of the total pigs are found in rural areas. Farmers in the rural areas keep these pigs as scavengers which makes them more susceptible to diseases. In some areas pig rearing is being promoted by the local veterinary departments. Scavenging by pigs also exposes them to JE virus and pigs serve as an important reservoir for most of the zoonotic diseases and thus pose a great threat to the human and animal population. From the financial year 2009-2010, pork production increased at a slow pace with a compound annual growth rate of 1.4% due to population growth. The ever-increasing demand of pork as an exceptional and cheap source of animal protein, provides a good market for a better return of investment in pig farming[9].
Longitudinal studies undertaken in Thanjavur district, Tamil Nadu showed JE incidence very low during 1991-1993 with infection rates 1.8 and 5.1%. But JE infection rates increased to 32.2% and 65.2% in the same district during 2011-2012 and 2012-2013 due to the marked decrease in the cattle:pig ratio at 123:1[10]. Thus cattle:pig ratio played a vital role in the transmission of JE in many areas. Earlier works suggested that the JE virus was circulating among Indian pigs for several decades[11] implying their vital role in the transmission and spread of JEV to different places.
Birds play an important role in the maintenance and transmission of JEV. Birds are ubiquitous and often share urban and suburban habitats with humans and mosquitoes. The important epidemiological factor in the spread of JEV is the regular migration of birds from endemic to non-endemic regions. Peninsular India is an ideal location for the nesting and feeding of egrets and herons (ardeid birds) found in the scrub forests. The large number of water bodies available in these areas stimulates paddy fields and acts as an ideal breeding ground for the JE vectors. Thus, the presence of JE vectors, the ardeid avian hosts, and human beings found inhabited in the nearby villages with the available pigs, poultry, and cattle creates a suitable environment for the spread of JE. Paddy cultivation is associated with this disease endemicity since this crop requires plenty of water. Unusual rainfall recorded nowadays in many places, cyclonic storms, and flooding in the low-lying areas creates plenty of vector breeding grounds. In Burdwan, West Bangal increased duck farming and animal husbandry practiced was also recorded. All these natural risk factors like presence of vector, its abundance and ecology which are influenced by environmental conditions and human behavior became conducive for vector proliferation and simultaneously the disease occurrence. Prolonged drought followed by excessive rainfall flooded the fields and provided an ideal breeding ground for the vectors. Villagers practicing mixed dwellings with cattle present on their doorstep were found preferred by the vectors as ideal resting places which is a major risk factor for the occurrence of JE in a particular area. In some areas epidemic season coincided with the breeding season of birds as noticed in fledglings of ducks reared in large numbers and this played the role of amplifiers.
JE virus sequencing studies conducted on isolates from different worldwide geographic locations showed 5 different genotypes. Among the 5 classified genotypes, Genotype III (GIII) is mostly found in Asian countries Sri Lanka, Nepal, India, Philippines, Vietnam, Taiwan, South Korea, Japan, and China. During the last decade, the GI genotype of JEV was introduced into China, South Korea, and Thailand replacing the GIII genotype of JEV already found circulating in Japan and Vietnam[12]. Indian city Gorakhpur's studies showed the circulation of both GI and GIII genotypes of JEV in that area[13]. Thus there is a change in the distribution pattern of different genotypes of the JE virus in India.
In addition, birds are considered as well-known reservoir hosts especially migratory birds that play a major role in the infection spread from one country to another. Migratory waterfowl such as pond herons and cattle egrets found in large lakes, swamps and rice fields breeding vector mosquitoes in which JEV antibodies were detected introduced JEV GI strains of other Asian countries into India which share a close genetic relationship. JEV spread from birds increased with urban husbandry of birds, and there are reports of mosquitoes carrying JEV increase risk in urban areas. GI viruses replicated more efficiently in bird-derived cells such as ducklings/chicks than GIII which played a role in the genotype shift from GIII to GI[14].
In China, it was found out that the presence of pigsties near human dwellings resulted from the large number of mosquitoes carrying the virus[15]. The same trend was observed in South Korea, where more human cases occurred among the people who live near pigsties[16]. In India, it is common in rural areas in states of Uttar Pradesh, Andhra Pradesh, Tamil Nadu as people reside side by side near pigsties which increase the risk for human infection.
Role of vectors
Changing patterns of agriculture from other crops to rice cultivation made a great impact on the epidemiology of JE in many parts of Southeast Asia which experienced severe epidemic outbreaks. More than one crop viz. double or triple crops are raised in many areas where previously only one rain-fed crop was possible, thus there was a moderate increase in area under rice cultivation[17]. Precipitation and temperature are the two vital determinants for the abundance of vector density and subsequent spread of JE disease[3]. The risk of JE increased with increased rice farming. Population densities of the Culex vishnui subgroup members follows rainfall patterns, being least abundant in the hot dry season and most abundant during and after the Northeast monsoon. There is a correlation in the abundance of Cx. vishnui subgroup members and occurrence of Japanese encephalitis cases. Thus, there is a widespread practice of rice cultivation that increased the yield as well as the appearance and expansion of JE disease to new areas. There is also an increase in the larval population after nitrogenous fertilizer application which influenced the oviposition of mosquitoes[18],[19]. There is an increase in the abundance of Cx. vishnui subgroup larvae in rice fields after the application of inorganic fertilizer[20]. Due to the increased usage of fertilizers, multiplication of main JE vector Cx. tritaeniorhynchus increased by 50% and resulted in more cases. Without nitrogenous fertilizer, blue-green algae (BGA) increased paddy yield without enhancing mosquito production. Therefore, the use of BGA with less nitrogenous fertilizer is recommended which is beneficial economically and agronomically to the farming community and also significantly reduced mosquito production in rice fields[20]. Rice-production systems, particularly irrigated rice farming, have increased both in cropping area and cropping intensity[21].
Earlier studies in Cuddalore district of erstwhile South Arcot district showed few isolations of JEV in the Cx. gelidus mosquitoes and by the abundance it was the fifth dominant among the JE vectors in that area. Thus they played a role in amplifying JEV transmission[4]. Cx. gelidus usually breeds in the ground pools containing weed marshy tracts. The changes in the agricultural practices and the change in the environmental conditions facilitated the proliferation of the breeding of Cx. gelidus in urban areas of Kurnool JE affected district of Andhra Pradesh[22]. Similarly, in a few Asian countries increased risk of JE was reported from peri-urban areas especially in South Korea as relative risk of JE infection was recorded in urban and suburban areas[23]. JE cases were reported in urban areas of Delhi[24]. In some urban areas, Cx. quinquefasciatus showed JEV infection[25]. Thus there is a change in the risk from rural to urban agglomeration. Culex gelidus became an important vector dominant after Culex tritaeniorhynchus[26],[27],[28]. Cx. tritaeniorhynchus dominated the total catch and Cx. gelidus steadily increased in its abundance during this period compared to the earlier studies conducted from these areas in which it acts as the secondary vector along with the major vector Cx. tritaeniorhynchus in Cuddalore district[26].
JE virus was isolated from over 30 species of mosquito from genera, Aedes, Anopheles, Armigerus, Culex, and Mansonia[29]. But in India JEV was isolated from 16 species of mosquitoes; 10 species of Culex, three species of each Anopheles and Mansoinioides. In India, maximum isolations were reported from principal vector Culex tritaenorhynchus[30]. In some of the JE-affected areas, a 3% infection rate was recorded in the vector mosquitoes[31]. Besides the aforementioned mosquito vectors, JEV was isolated from many other common vector mosquito species such as An. peditaeniatus, An. barbirostris, An. subpictus, Cx. vishnui, Cx. pseudovishnui, Cx. epidesmus, Cx. bitaeniorhynchus, Cx. infula, Cx. whitmorei, Cx. fuscocephala, Cx. quinquefasciatus, Mansonia annulifera, Ma. indiana, and Ma. uniformis as observed in different places[30]. Minor vectors may also play a role in the virus transmission when there is conducive condition that prevails for transmission[32]. Anopheles subpictus mosquitoes collected in all types of breeding habitats showed higher abundance than other anophelines in its distribution with moderate anthropophilic index and high survival rate in all seasons, indicating its role in JE transmission as a secondary or bridge vector[33]. The first JEV outbreak from Malkangiri district in Odisha state showed Cx. vishnui (30.4%) and the detection of JEV in Cx. vishnui showed important implications for public health for JE control[34].
Culex quinquefasciatus, was found abundantly collected and infected with JE virus during the 1980s and also currently collected from different states like Uttar Pradesh and West Bengal[35], suggesting its probable role as a vector. Similarly, another common mosquito species available aplenty named Armigeres subalbatus, were also found infected with JE virus and reported to be implicated in the JEV transmission in India[37]. There is a cumulative increase in the total number ofspecies reportedly involved in the JEV transmission in India [Figure 4].
Figure 4: Confirmed Japanese encephalitis vector species and status of the vector incrimination in India49–50Host-feeding behavior
The JE vector Culex vishnui played a significant role in preferring human blood (7.14%) in the endemic area, but not in the non-endemic area. The preference of Cx. tritaeniorhynchus to feed on other hosts than those tested was high in a non-endemic area when compared to that in an endemic area[28]. Culex tritaeniorhynchus species is predominantly zoophilic and acts as the connecting link between livestock and humans[37]. Thus, vector mosquitoes generally feed at night showing the biphasic biting time[38]. This vector remains infected throughout its lifetime after ingesting the virus from the host. They will be in a position to transfer the virus after completion of the extrinsic incubation period[38]. Isolation of JEV in larval stages of vectors demonstrated vertical transmission and its prevalence in the natural cycle[25].
Culex tritaeniorhynchus vector mosquitoes enhanced feeding habitat on the less-preferred host like humans and pigs and are considered as an important factor for the spread of JE. Nowadays pig rearing is considered a lucrative business in many areas. Thus, promotion of pig rearing by the veterinary department is considered as an alternative business. A decrease in the cattle:pig ratio enhanced the JEV infection among the children compared to 20 years before in Tanjore which is a non-JE area[10].
Resting behavior of vectors
An increased change was observed in the feeding and resting pattern of the vectors collected in Bellary district, Karnataka state, India which showed rapid changes in the dynamics of disease transmission[40]. There was an unusual abundance in the indoor resting collection of Cx. tritaeniorhynchus recorded during the daytime as noticed in a JE endemic area Bellary district, Karnataka. The principal vector Cx. tritaeniorhynchus was predominantly collected which demonstrated two times peak abundance coinciding with the 2 rice cultivation seasons in the district. The resting behavior of Cx. tritaeniorhynchus is just opposite to the behavior observed in many other JE infected areas where these vector mosquitoes were observed in low density from indoors collection[39]. The mixed dwelling of cattle and humans observed in this area prompted the zoophilic Cx. tritaeniorhynchus vector mosquitoes to rest indoors which created an ideal condition for its existence as observed in the Bellary area. The density observed in the mixed dwellings was 6.65 times higher compared to the human dwelling. Thus there was no genetic variation observed in these Cx. tritaeniorhynchus populations[41]. Human and animal feeding pattern was also observed in these vectors. These mosquitoes may disperse hundreds of kilometers during one night[42] which will help these vectors to move far away from their breeding ground and involve in the JE transmission[43].
JEV vector species are collected from urban households with and without pigs and show that keeping pigs in an urban area increases the number of mosquitoes competent as vectors for JEV[44],[45]. Due to the aforementioned changes observed, JE can also be considered as an urban disease. The present estimate showed 50% of the world's urban populations are residing in Asia and out of that, 60% of urbanites are found to be economically weak[46],[47].
In some proven cases, the progeny from the infected female mosquito can transmit the virus immediately after emergence when they take the first blood meal which is considered epidemiologically important in JEV transmission. This phenomenon of the JE virus using many Culex species of mosquitoes as reservoir hosts and exhibition of vertical transmission ensures local survival of the virus during adverse conditions of hot seasons when the vector abundance is low and non-immune pigs are few[48].
There are significant changes taken place in the risk of JE which is now under geographic expansion. The risks are also increased with rice farming which has significantly increased in production acreage. The transmission of JE is dependent on the transmission to humans by mosquitoes and the amplification in pigs and birds. Birds are known amplifying and reservoir hosts. Many species are widely distributed and migratory birds have been associated with spread from one place to other place resulting in the geographic increase in endemic areas. Climate change can have a significant impact due to temperature changes. Temperature increase may cause a change in the peak and duration of the transmission season and an increased risk particularly in temperature climates. The increased risk of peri-urban areas has been reported. The increasing exposure in peri-urban settings questions the thought that the risk is limited to rural areas. Thus there are a number of epidemiologic changes that impact the risk of infection with the Japanese encephalitis virus.
ConclusionThis work summarizes several changes observed in the transmission of Japanese encephalitis (JE) and the risk of its spread of infection to many areas. Thus the risk of contracting the virus is growing unnoticed in many places. Still, there is no sufficient knowledge obtained on the JE viruses circulating in humans, pigs, and vector mosquitoes. Due to its spread in an endemic fashion, it is increasing in many endemic areas of India. Many environmental and ecological factors play a vital role in the spread of this dreaded disease. Since there is no effective antiviral therapy available, vaccination is the choice for the prevention. Modified agricultural practices integrating JE vector control strategies in paddy fields must be demonstrated through the State agricultural units to implement larval control measures effectively. JE vectors behavioral changes should be always observed in an area and accordingly Indoor residual spraying (IRS) and distribution of Long-lasting insecticidal nets (LLINs) can be undertaken which showed encouraging results as observed in Gorakhpur, India. Agriculture and dairy experts should guide the public to have their paddy cultivation and pig farming in separate locations to protect the public from this disease. A well-established, strong, rigorous improved vector surveillance networking system should be established to identify the high-risk areas to initiate appropriate vector control measures in addition to JE immunization to be undertaken well before the JE season in children residing in JE-prone areas in the country to avoid impending outbreaks.
Ethical statement: Not applicable
Conflict of interest: None
AcknowledgementsWe are thankful to our Director General, Indian Council of Medical Research (ICMR), New Delhi, India. We want to express our deep sense of gratitude to all our departmental colleagues of ICMR-Vector Control Research Centre Field station erstwhile ICMR-Centre for Research in Medical Entomology, Madurai.
References
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