Japanese Encephalitis
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J Neurol Neurosurg Psychiatry 2000;68:405–415 405 NEUROLOGICAL ASPECTS OF TROPICAL DISEASE Japanese encephalitis Tom Solomon, Nguyen Minh Dung, Rachel Kneen, Mary Gainsborough, David W Vaughn, Vo Thi Khanh Although considered by many in the west to be West Nile virus, a flavivirus found in Africa, the a rare and exotic infection, Japanese encephali- Middle East, and parts of Europe, is tradition- tis is numerically one of the most important ally associated with a syndrome of fever causes of viral encephalitis worldwide, with an arthralgia and rash, and with occasional estimated 50 000 cases and 15 000 deaths nervous system disease. However, in 1996 West annually.12About one third of patients die, and Nile virus caused an outbreak of encephalitis in half of the survivors have severe neuropshychi- Romania,5 and a West Nile-like flavivirus was atric sequelae. Most of China, Southeast Asia, responsible for an encephalitis outbreak in and the Indian subcontinent are aVected by the New York in 1999.67 virus, which is spreading at an alarming rate. In In northern Europe and northern Asia, flavi- these areas, wards full of children and young viruses have evolved to use ticks as vectors adults aZicted by Japanese encephalitis attest because they are more abundant than mosqui- Department of to its importance. toes in cooler climates. Far eastern tick-borne Neurological Science, University of encephalitis virus (also known as Russian Liverpool, Walton Historical perspective spring-summer encephalitis virus) is endemic Centre for Neurology Epidemics of encephalitis were described in in the eastern part of the former USSR, and and Neurosurgery, Japan from the 1870s onwards. Major epidem- Western tick-borne encephalitis virus occurs in Fazakerley, Liverpool ics were reported about every 10 years, with Europe and has caused recent epidemics in L9 7LJ, UK Germany and Austria.8 In the United Kingdom Tom Solomon more than 6000 cases reported in the 1924 epidemic.3 The term type B encephalitis was the tick borne Louping Ill virus is is enzootic in Liverpool School of originally used to distinguish these summer sheep, and occasionally causes encephalitis in 9 Tropical Medicine, epidemics from von Economo’s encephalitis sheep and humans. Pembroke Place, lethargica (sleeping sickness, known as type A), Liverpool L3 5QA, UK but the B has since been dropped. In 1933 a ENZOOTIC CYCLE Tom Solomon filterable agent was transmitted from the brain Japanese encephalitis virus is transmitted natu- Centre for Tropical of a fatal case to cause encephalitis in monkeys; rally between wild and domestic birds, and pigs Diseases, Cho Quan the prototype Nakayama strain of Japanese by Culex mosquitoes—the most important for Hospital, Ho Chi Minh encephalitis virus was isolated from the brain of human infection being Culex tritaeniorrhynchus City, Vietnam a fatal case in 1935. The virus was later classed which breeds in pools of stagnant water (such Nguyen Minh Dung as a member of the genus Flavivirus (family as rice paddy fields).10 Although many animals Mary Gainsborough Vo Thi Khanh Flaviviridae) named after the prototype yellow can be infected with the virus, only those which fever virus (Latin; yellow=flavi). Although of develop high viraemias are important in the Royal Liverpool no taxonomic significance, the ecological term natural cycle. As well as maintaining and Children’s NHS Trust, arbovirus is often used to describe the fact that amplifying Japanese encephalitis virus in the Alder Hey, Liverpool Japanese encephalitis virus is insect (arthro- environment, birds may also be responsible for L12 2AP,UK pod) borne. the spread to new geographical areas. Pigs are Rachel Kneen the most important natural host for transmis- Centre for Tropical Epidemiology sion to humans, because they are often kept Medicine and NEUROTROPIC FLAVIVIRUSES: A GLOBAL close to humans, have prolonged and high Infectious Diseases, PERSPECTIVE viraemias, and produce many oVspring—thus NuYeld Department Japanese encephalitis virus is transmitted providing a continuous supply of previously of Clinical Medicine, uninfected new hosts. The virus does not typi- John RadcliVe between animals by Culex mosquitoes, and Hospital, Headington, occurs across eastern and southern Asia and cally cause encephalitis in these natural hosts, Oxford, OX3 9DU, UK the Pacific rim. However, related neurotropic athough abortions occur in pregnant sows. Mary Gainsborough flaviviruses are found across the globe (fig 1); they share many virological, epidemiological, EPIDEMIOLOGY OF HUMAN DISEASE Department of Virus and clinical features.2 Molecular virological Humans become infected with Japanese en- Diseases, Walter Reed Army Institute of studies suggest that all flaviviruses derived cephalitis virus coincidentally when living or Research, Washington, from a common ancestor some 10–20 000 travelling in close proximity to the enzootic DC 20307, USA years ago, and are rapidly evolving to fill cycle of the virus. Although most cases occur in David W Vaughn ecological niches.4 Examples of mosquito rural areas, Japanese encephalitis virus is also borne neurotropic flaviviruses include Murray found on the edge of cities. Epidemiological Correspondence to: Dr Tom Solomon Valley encephalitis virus in Australia, and St studies have shown that after the monsoon [email protected] Louis encephalitis virus in North America. rains mosquitoes breed prolifically, and as their 406 Solomon, Dung, Kneen, et al Figure 1 Map showing approximate global distribution of major neurotropic flaviviruses; JE=Japanese encephalitis; MVE=Murray valley encephalitis; WN=West Nile; WTBE=Western tick-borne encephalitis; FETBE=Far Eastern tick-borne encephalitis; LI=Louping Ill virus; SLE=St Louis encephalitis. numbers grow, so does their carriage of are also aVected.20 The susceptibility of immu- Japanese encephalitis virus and the infection nologically naive adults was also demonstrated rate of pigs.11 12 Human infection soon follows. by the incidence of Japanese encephalitis In sentinel studies, previously unexposed pigs among American troops during conflicts in placed in endemic areas were infected with the Japan, Korea, and Vietnam21–25 The rate of virus within weeks. symptomatic infection was higher in these Although the virus has occasionally been troops than in local populations. This may be isolated from human peripheral blood13 virae- explained by partial protection due to previous mias are usually brief and titres low; thus flavivirus exposure in the indigenous popula- humans are considered a dead end host from tion, age related diVerences, diVerent genetic which transmission does not normally occur. susceptibility to Japanese encephalitis, or more Cross sectional serological surveys have shown sensitive disease surveillance among United that in rural Asia most of the population are States troops. infected with Japanese encephalitis virus dur- Broadly speaking two epidemiological pat- ing childhood or early adulthood.14 About 10% terns of Japanese encephalitis are recognised.19 of the susceptible population is infected each In northern areas (northern Vietnam, northern year.15 However, most infections of humans are Thailand, Korea, Japan, Taiwan, China, Nepal, asymptomatic or result in a non-specific and northern India) huge epidemics occur flu-like illness; estimates of the ratio of sympto- during the summer months, whereas in south- matic to asymptomatic infection vary between ern areas (southern Vietnam, southern Thai- 1in2516 and 1 in 1000.17 land, Indonesia, Malaysia, Philippines, Sri Japanese encephalitis is mostly a disease of Lanka, and southern India) Japanese encepha- children and young adults. In northern Thai- litis tends to be endemic, and cases occur spo- land the incidence has been estimated to be up radically throughout the year with a peak after to 40 per 100 000 for ages 5 to 25, declining to the start of the rainy season.19 almost zero for those over 3514 18 The incidence Various explanations for this diVerent pat- is lower among young children (<3 years old) tern have been oVered. The finding that than in older children, possibly reflecting Japanese encephalitis virus isolates from epi- behavioural factors—for example, playing out- demic northern Thailand and endemic south- side after dusk.19 ern Thailand were of diVerent genotypes (see When epidemics first occur in new locations, below) led to the suggestion that diVering neu- such as in Sri Lanka, India, and Nepal, adults rovirulence among diVerent strains may be Japanese encephalitis 407 25 remains high through the year, the number of A cases each month is constant. In the north a sharp rise in cases of Japanese encephalitis 20 during the summer months corresponds with a rise in temperature above 20°C. The prolonged mosquito larval development time and longer 15 extrinsic incubation period of Japanese en- cephalitis virus at cooler temperature, which % thus reduce the rate of virus transmission, 10 could be one explanation for these findings. GEOGRAPHICAL DISTRIBUTION 5 In the past 50 years the geographical area aVected by Japanese encephalitis virus has expanded (fig 1). DiVerences in diagnostic capabilities and in reporting of encephalitis 0 make it impossible to plot this expansion precisely. However, the timing of the first 35 B reported cases or new epidemics in each area gives an impression of the relentless spread of 30 Japanese encephalitis. In China outbreaks of summer encephalitis occurred from 1935, and 25 the virus was first isolated there in 1940; there are currently 10–20 000 cases a year, although 20 in the early 1970s it was over 80 000 cases annually.19 In the far eastern Russian states, C ° Japanese encephalitis first occurred in 1938. In 15 1949, large epidemics were reported from South Korea for the first time. Epidemics in 10 Hanoi northern Vietnam followed in 1965 (currently Ho Chi Minh City 1000–3000 cases nationally a year), and in 5 Chiang Mai in northern Thailand in 1969 (currently 1500–2500 cases nationally a year). 0 Japanese encephalitis was recognised in south- ern India from 1955, but was confined to the south until the 1970s. Since then, large 400 C outbreaks (2000–7000 cases a year) have been 350 reported from eastern and northeastern states.