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Transmission of Japanese Encephalitis Virus from the Black Flying Fox, Pteropus Alecto , to Culex Annulirostris Mosquitoes, Despite the Absence of Detectable Viremia

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Transmission of Japanese Encephalitis Virus from the Black Flying Fox, Pteropus Alecto , to Culex Annulirostris Mosquitoes, Despite the Absence of Detectable Viremia Am. J. Trop. Med. Hyg., 81(3), 2009, pp. 457–462 Copyright © 2009 by The American Society of Tropical Medicine and Hygiene Transmission of Japanese Encephalitis Virus from the Black Flying Fox, Pteropus alecto , to Culex annulirostris Mosquitoes, Despite the Absence of Detectable Viremia Andrew F. van den Hurk , * Craig S. Smith , Hume E. Field , Ina L. Smith , Judith A. Northill , Carmel T. Taylor , Cassie C. Jansen , Greg A. Smith , and John S. Mackenzie Virology, Queensland Health Forensic and Scientific Services, Coopers Plains, Queensland, Australia; School of Chemical and Molecular Biosciences, University of Queensland, St Lucia, Queensland, Australia; Department of Primary Industries and Fisheries, Animal Research Institute, Yeerongpilly, Queensland, Australia; Australian Army Malaria Institute, Gallipoli Barracks, Enoggera, Queensland, Australia; Australian Biosecurity Cooperative Research Centre, Curtin University of Technology, Perth, Western Australia, Australia Abstract. To determine the potential role of flying foxes in transmission cycles of Japanese encephalitis virus (JEV) in Australia, we exposed Pteropus alecto (Megachiroptera: Pteropididae) to JEV via infected Culex annulirostris mosquitoes or inoculation. No flying foxes developed symptoms consistent with JEV infection. Anti-JEV IgG antibodies developed in 6/10 flying foxes exposed to infected Cx. annulirostris and in 5/5 inoculated flying foxes. Low-level viremia was detected by real-time reverse transcriptase polymerase chain reaction in 1/5 inoculated flying foxes and this animal was able to infect recipient mosquitoes. Although viremia was not detected in any of the 10 flying foxes that were exposed to JEV by mosquito bite, two animals infected recipient mosquitoes. Likewise, an inoculated flying fox without detectable viremia infected recipient mosquitoes. Although infection rates in recipient mosquitoes were low, the high population densities in roosting camps, coupled with migratory behavior indicate that flying foxes could play a role in the dispersal of JEV. INTRODUCTION in eastern Australia. Certainly, the behavioral ecology of fly- ing foxes deems them potential dispersal hosts of mammalian Japanese encephalitis virus (JEV) is a mosquito-borne fla- viruses, and several recently emerged zoonotic viruses, includ- vivirus of Southeast Asia responsible for over 40,000 clinical ing Hendra virus (HeV) and Australian bat lyssavirus, have 1 cases annually, with a 25% fatality rate. Japanese encephali- been described in flying foxes in Australia. 12 Furthermore, tis virus is an emerging virus in the Australasian region with both experimental and natural infection studies have sug- 2 potentially serious public and animal health implications. gested a possible role for bats in the transmission cycles of Widespread JEV activity was first detected in Australia in 1995 a number of arboviruses, including JEV (reviewed by Sulkin on Badu Island in Torres Strait, when it caused an outbreak and Allen). 13 However, the majority of these experiments have 3 consisting of three human cases and two deaths. Subsequently, examined insectivorous bats of the order Microchiroptera. except for 1999, JEV activity was recognized every year in the The only experimental infection of Megachiropteran bats Torres Strait between 1995 and 2005, when the sentinel pig with JEV has been undertaken in India. In these earlier stud- program was discontinued. In 1998, human and pig infections ies, viremia developed in both Rousettus leschenaulti and were identified for the first time on the Australian mainland Cynopterus sphinx , with the latter species able to infect recip- 4 at the mouth of the Mitchell River on Cape York Peninsula. ient mosquitoes. 14,15 Entomologic studies implicated Culex annulirostris as the pri- We undertook laboratory-based infection and transmis- 5,6 mary mosquito vector of JEV in northern Australia. sion experiments to determine whether flying foxes can Pigs and ardeid wading birds, such as herons and egrets are act as amplifying hosts for JEV. Specifically, we examined the primary amplifying hosts of JEV, as they produce viremia 1) the ability of flying foxes to develop clinical illness, vire- 7–10 sufficient to infect mosquitoes. Although humans and horses mia, and specific antibodies after being exposed to JEV via can develop fatal encephalitis, they are considered to be dead- infected mosquitoes or by inoculation; and 2) the likelihood 11 end hosts of the virus, developing only low-level viremia. of recipient mosquitoes becoming infected after feeding on Should JEV become established on the Australian main- flying foxes that had been previously exposed to JEV. The land, the potential importance of Australian fauna species Black flying fox, Pteropus alecto , was chosen because of acting as vertebrate amplifying hosts is largely unknown. its widespread geographic distribution throughout north- Experimental studies at the Commonwealth Scientific and ern Australia, including areas where JEV has previously Industrial Research Organization Australian Animal Health occurred. 16 Laboratory previously examined the possible role of a num- ber of Australian native species (such as wallabies and pos- sums) as reservoir or amplifying hosts.2 However, flying MATERIALS AND METHODS foxes (Megachiroptera: Pteropididae) were not included in All animal experimentation complied with the Queensland these studies, and mosquitoes were not used as the route of Animal Care and Protection Act 2001 and was approved by virus exposure or to show transmission of JEV. Flying foxes the Queensland Department of Primary Industries Animal are of particular interest as a potential reservoir or amplify- Ethics Committee (AEC; approval no. 33/08/02), University ing host of JEV as a result of their nomadic behavior, and of Queensland AEC (approval no. MICRO/PARA/463/02/), because of their increasing abundance in major urban areas and Queensland Health Forensic and Scientific Services AEC (QHFSS; approval no. VIR 1/03/32). In addition, the collection of wild flying foxes was approved by the * Address correspondence to Andrew F. van den Hurk, Virology, Queensland Parks and Wildlife Service (Scientific Purposes Queensland Health Forensic and Scientific Services, 39 Kessels Rd, Coopers Plains, Queensland 4108, Australia. E-mail: andrew_hurk@ permit no. WISP01419503). As JEV is considered an exotic health.qld.gov.au virus in Australia, all infection and transmission experiments 457 458 VAN DEN HURK AND OTHERS were undertaken at the Physical Containment Level 3 the commencement and cessation of feeding, samples of the insectary/animal house at QHFSS , Brisbane. blood/virus suspension were diluted 1:20 in growth media Animals. Pteropus alecto were collected from flying fox (GM; Opti-MEM [Invitrogen, Grand Island, NY] with 3% colonies located in the Brisbane suburbs of East Brisbane fetal bovine serum, antibiotics and fungizone) and stored at (27°28′S, 153°03′E) and Indooroopilly (27°30′S, 152°58′E), −70°C for later titration. which also contained the Grey-headed flying fox, Pteropus After 18 hr, mosquitoes were anesthetized with CO2 and poliocephalus and the Little red flying fox, Pteropus scapulatus . blood engorged mosquitoes were placed into 1 L contain- Flying foxes returning from overnight foraging were captured ers within an environmental growth cabinet (Sanyo Electric, using mist nets for a period of approximately 90 min before Gunma, Japan) maintained at 28°C, 70–75% RH, and 12:12 sunrise. Flying foxes were anaesthetized using the inhalation (L:D), and offered 10% sucrose as a nutrient source. Mosqui- anesthetic Isoflurane (Isoflurane Inhalation Anesthetic, Laser toes were held under such conditions for an extrinsic incuba- Animal Health, Salisbury, Australia) administered by a portable tion period of 13 d. To determine if the mosquitoes intended Ohmeda Isotec 3 vaporizer (BOC Health Care, West Yorkshire, for the infection of the flying foxes were indeed infected, a England) at a concentration of 5% for induction and 1.5% sample of ≤ 6 individual mosquitoes were removed on day 12 during maintenance with an oxygen flow rate of 1 L/min.17 Each post virus exposure and tested for the presence of virus. bat was assessed for age, weight, forearm length, and female Flying fox husbandry. On the afternoon before the infection bats for pregnancy status by abdomen palpitation. Pregnant experiments, flying foxes were moved from ARI to QHFSS females were excluded from the study and released. To aid and placed in individual cages in a room within the PC3 in future identification, each flying fox was injected with a animal house. The dimensions of the cages were 900 × 900 × microchip containing a unique identification number (LifeChip, 900 mm, and were of wire mesh construction (25 × 25 × 25 Destron Fearing, South St. Paul, MN). A 1–2 mL blood sample mm aperture), elevated 1 m above the ground, with 10–15 cm was obtained from the propatagial vein using a 3 mL syringe between cages. Seasonal fruits (including rockmelon, bananas, (Terumo [Philippines] Corporation, Laguna, Philippines), a mangoes, apples, etc.), supplemented by full cream milk 0.50 × 16 mm needle (Terumo [Philippines] Corporation), powder, were fed to the flying foxes between 4 and 6 pm daily; and lithium heparin (Heparin Injection BP, David Bull water was provided ad libatum via drip bottles. Artificial light Laboratories, Mulgrave North, Australia) as an anticoagulant. was provided for the flying foxes each day between the hours The serum
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