Movement of arboviruses between Indonesia and Western Australia

Dengue is the most medically important mosquito-borne viral disease in humans, associated with significant morbidity, mortality, and economic cost¹. The disease is caused by infection with any of four dengue virus (DENV-1 to DENV-4) serotypes. Since the first cases were documented in the Indonesian capital city of Jakarta in 1968², dengue has become prevalent in all provinces and nearly 60% of the Indonesian population of 270 million people live in areas where DENV is known to be circulating. In Australia transmission of DENV is currently restricted to urban areas of northern Queensland and the Torres Strait where Aedes aegypti, the main DENV vector, is well established. Modernisation of transportation systems has enhanced introduction of DENV from endemic countries and led to regular outbreaks in Australia where the number of imported dengue cases increased by 298% and 155%, in 2010 and 2011 respectively, compared with the 5-year mean³. More than half of all dengue cases imported to Australia are acquired in Indonesia^3–6.

In Western Australia (WA), dengue outbreaks were reported in the north of the state up until the mid-1940s. Ae. aegypti mosquitoes were eradicated by the end of the 1960s⁷ and currently, there are no endemic mosquito species with potential to vector DENV in WA⁸. Although autochthonous DENV transmission does not occur in WA, the state has reported the highest number of dengue cases in the country in recent years⁹; approximately 80% were acquired in Bali¹⁰, one of the most popular tourist destinations for WA residents especially after new budget airlines began offering affordable package holidays in the early 2000s. Dengue notification in WA increased from an annual average of 14 cases in 2006 to 558 cases in 2015¹⁰.

We have monitored long-term molecular epidemiology of DENV in WA and in Indonesia to understand virus movement from the Asia Pacific region to the state. Our analysis of DENV imported by travellers returning to WA identified a DENV-2 (Cosmopolitan genotype) lineage that emerged during a major dengue outbreak in Bali during 2011–2012⁶. The virus was exported to other Asian and European countries in subsequent years^11,12. As introduction of new lineages to unaffected regions may be associated with more severe forms of dengue disease^13–16, circulation of this lineage and other newly emergent lineages should be monitored. DENV genomic surveillance among returning travellers provides valuable and timely information to understand DENV transmission in Indonesia and neighbouring countries; monitor emergence and transmission dynamics of virulent DENV lineages in the Asia Pacific region, and also to identify genetic and biological features of DENV introduced to WA.

Data from the WA Notifiable Infectious Diseases Database, Communicable Disease Control Directorate, Department of Health, indicate that between 1 January 2016 and 31 December 2017 there were 739 imported dengue fever (DF) notifications¹⁷. In this surveillance system both confirmed and probable cases are included. Case definitions for confirmed and probable cases, based on WHO criteria, have been published elsewhere by WA Department of Health¹⁸.

There was a sharp decrease in DF notifications in WA in 2017 (181 cases) compared with 2016 (558 cases) and case numbers continued to decrease in 2018 (137 cases). DF case notifications in WA mirrored the number of dengue haemorrhagic fever (DHF) cases reported by Ministry of Health (MoH) of Indonesia (Figure 1). In Indonesia, DHF cases decreased from 201 885 cases in 2016 to 59,047 cases in 2017, with incidence rate 77.9 and 22.5 per 100 000 population, respectively^19,20. In 2018, there were 65 602 DHF cases and 467 deaths²¹.

Figure 1.  Dengue notification in WA and Indonesia, 2014–2018. WA Department of Health and MoH of Indonesia data indicate that DF notifications in WA reflected the pattern of DHF cases in Indonesia during that period.

During 2016–2017 we isolated and/or sequenced 67 DENV (58 in 2016 and 9 in 2017). In 2016, 48 of 58 DENV (82.7%) originated in Indonesia, of which 37 (77.1%) were derived from travellers returning from Bali. One virus was imported to WA from Solomon Islands and one from an unspecified Pacific nation; one each from Thailand and an unspecific Southeast Asian country, in addition to six DENV of unknown origin (Figure 2). In 2017, a low number of dengue cases was reported in WA. Nine DENVs were successfully sequenced and only two viruses (serotypes DENV-1 and DENV-3) were isolated from travellers known to have returned from Bali; six samples originated in East Timor, Vietnam, Solomon Island, Thailand, Malaysia and India, and travel history was unknown for the remaining DENV.

Figure 2.  Origin of isolated and sequenced DENV imported to WA, 2016–2017.

Of the 67, 2016–2017 DENV sequenced the predominant serotype was DENV-2 (25; 37.3%) followed by DENV-3 (22; 32.8%), DENV-1 (14; 20.9%) and DENV-4 (6; 8.9%) (Figure 3). This serotype distribution was similar to diagnostic RT-PCR serotyping data obtained from PathWest Laboratory. Among 419 DENV diagnostic serotype reports from 2016–2017, DENV-2 accounted for 37.2% followed by DENV-3 (28.6%), DENV-1 (23.1%) and DENV-2 (10.9%) (Figure 3).

Figure 3.  Serotype of DENV imported to WA, 2016–2017. DENV selected for molecular epidemiology studies were representative of imported viruses.

All four serotypes were identified in WA travellers during 2016 with DENV-2 at highest frequency. As is often reported globally, DENV-4 circulated less frequently than the other three DENV serotypes.

Chikungunya virus (CHIKV) is endemic in Indonesia. CHIKV is vectored by Ae. aegypti and Ae. albopictus mosquitoes, the same species that transmit DENV. The first chikungunya outbreak reported in Indonesia occurred in June 1982 in Jambi province of Sumatra Island, followed by multiple outbreaks between 1983 and 1984²² in Yogyakarta on the island of Java. Cases were then rarely reported in the country, until CHIKV re-emerged throughout Indonesia in early 2001. Multiple outbreaks have been reported subsequently, of which two were nation-wide, during 2009–2010 and in 2013, with 137 655 and 15 324 cases respectively^23,24.

Modernisation of transportation systems has also contributed to the global expansion of CHIKV. CHIKV-infected travellers have been documented in more than twenty countries throughout Asia, Europe, and North America²³. In Australia, data from the National Arbovirus and Malaria Advisory Committee indicate that between 2008 and 2014, there were 327 notified chikungunya cases in the country and almost 40% originated from Indonesia^24–29. There was a significant increase in cases during 2012–2013 from 20 cases in the previous year²⁶ to 96 cases in 2012–2013²⁵. Exported chikungunya cases that originated from Indonesia have been reported, of which most are travellers returning to Australia²².

Chikungunya was included as notifiable infectious disease in WA from May 2008. Since that time, the average annual incidence was six cases until 2013 when the case count increased significantly to 51 cases for the period January to September³⁰. The majority (92%) originated from Indonesia, of which most (94%) were travellers returning from Bali³⁰. In Indonesia, during the same year, there was a nationwide chikungunya outbreak in which 15 324 cases were reported to MoH³¹. The increase in imported chikungunya cases in WA, and Australia, reflected the increased incidence in Indonesia identified by national chikungunya surveillance during 2012–2013. Phylogenetic analysis of CHIKV E gene sequences provides important information on CHIKV movements to Australia, and our studies have identified importation of CHIKV associated with the nation-wide chikungunya outbreak in Indonesia in 2013²².

Dengue outbreaks have been reported in Australia since 1879. International travel plays an important role in introduction of dengue and chikungunya although autochthonous transmission is dependent on presence of the mosquito vectors locally. Aedes mosquito species known to vector DENV, CHIKV, and other medically important arboviruses were previously present in WA, New South Wales, Northern Territory and Queensland and in WA dengue outbreaks were reported in the north of the state up until the mid-1940s. Improvements in public health infrastructure led to eradication of the vectors in many areas and they have not been present in WA since the 1960s. DENV introduced to Australia by travellers is associated with regularly reported outbreaks⁶. During 1990–2009, 31 dengue outbreaks were recorded in northern Queensland alone. During 2004–2013, there were 5943 imported dengue cases nationally with an average incidence of 7.78 per 100 000 travellers over the 9-year period⁴, ranging between 1.65 to 17.75 per 100 000 travellers in 2005 and 2013, respectively. The number of affected areas across the country also increased significantly⁴. More than half of all imported dengue cases were acquired in Indonesia^3,4 and Indonesia is the main source of dengue and chikungunya importation cases^9,22–32.

WA demonstrates the highest relative risk of imported dengue compared to other states³, associated with high rates of travel to endemic countries in the Southeast Asian region such as Indonesia. More than 80% of imported dengue cases in WA were acquired in Bali³. A modelling study using the assumption that Aedes mosquitoes are introduced solely by human transport, indicates that the risks of dengue outbreak are higher in northern part of WA but can extend to the Perth metropolitan area during summer³³. In 2013, the first acquired DENV infection in WA after 1960 was reported⁸, thought to be caused by a bite from a single infected mosquito vector that was transiently introduced to the region. This case highlights the public health importance of maintaining surveillance efforts to ensure that any incursions of dengue vectors into WA are promptly identified and do not become established, particularly given the large numbers of viraemic travellers returning from dengue-endemic regions.

Currently, although autochthonous transmission of dengue in Australia is restricted to urban areas of north Queensland and the Torres Strait where Ae. aegypti remains well established, large parts of Australia including WA are climatically suitable for dengue vector species⁷. A modelling study using the current distribution of Ae. aegypti and climate change scenarios for 2030 and 2050 suggested that WA is one of the regions at high risk for Ae. aegypti expansion. These data indicate there is a risk of both mosquito vectors and DENV becoming established in WA. In addition, Australia has several other mosquito species potentially capable of facilitating an outbreak of CHIKV should the virus be introduced. Aedes spp. were highly competent laboratory vectors of CHIKV, particularly Ae. vigilax, Ae. procax, as well as other species including Culex linealis^34,35. Therefore, case and vector surveillance as well as population health responses are crucial for minimising any potential impact of DENV and CHIKV establishment in Australia. In summary, our molecular epidemiology studies indicate that continuous surveillance using WA travellers as sentinels provides timely information on transmission dynamics of major arboviruses in the Asia Pacific region. These data provide important indicators that support and strengthen preparedness for emerging epidemic threats, including mosquito-borne diseases, in Australia and the region.

The authors declare no conflicts of interest.

This research did not receive any specific funding.