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(Pteropus Lylei) in Thailand

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(Pteropus Lylei) in Thailand Wacharapluesadee et al. Virology Journal (2018) 15:38 https://doi.org/10.1186/s12985-018-0950-6 RESEARCH Open Access Longitudinal study of age-specific pattern of coronavirus infection in Lyle’s flying fox (Pteropus lylei) in Thailand Supaporn Wacharapluesadee1* , Prateep Duengkae2, Aingorn Chaiyes2, Thongchai Kaewpom1, Apaporn Rodpan1, Sangchai Yingsakmongkon3, Sininat Petcharat1, Patcharakiti Phengsakul2, Pattarapol Maneeorn4 and Thiravat Hemachudha1 Abstract Background: Bats are natural reservoirs for several highly pathogenic and novel viruses including coronaviruses (CoVs) (mainly Alphacoronavirus and Betacoronavirus). Lyle’s flying fox (Pteropus lylei)‘s roosts and foraging sites are usually in the proximity to humans and animals. Knowledge about age-specific pattern of CoV infection in P. lylei, prevalence, and viral shedding at roosts and foraging sites may have an impact on infection-age-structure model to control CoV outbreak. Methods: P. lylei bats were captured monthly during January–December 2012 for detection of CoV at three areas in Chonburi province; two human dwellings, S1 and S2, where few fruit trees were located with an open pig farm, 0.6 km and 5.5 km away from the bat roost, S3. Nested RT-PCR of RNA-dependent RNA polymerase (RdRp)genefromrectalswabs was used for CoV detection. The strain of CoV was confirmed by sequencing and phylogenetic analysis. Results: CoV infection was found in both juveniles and adult bats between May and October (January, in adults only and April, in juveniles only). Of total rectal swab positives (68/367, 18.5%), ratio was higher in bats captured at S1 (11/ 44, 25.0%) and S2 (35/99, 35.4%) foraging sites than at roost (S3) (22/224, 9.8%). Juveniles (forearm length ≤ 136 mm) were found with more CoV infection than adults at all three sites; S1 (9/24, 37.5% vs 2/20, 10%), S2 (22/49, 44.9% vs 13/ 50, 26.0%), and S3 (10/30, 33.3% vs 12/194, 6.2%). The average BCI of CoV infected bats was significantly lower than uninfected bats. No gender difference related to infection was found at the sites. Phylogenetic analysis of conserved RdRp gene revealed that the detected CoVs belonged to group D betacoronavirus (n =64)andalphacoronavirus (n =4). Conclusions: The fact that CoV infection and shedding was found in more juvenile than adult bats may suggest transmission from mother during peripartum period. Whether viral reactivation during parturition period or stress is responsible in maintaining transmission in the bat colony needs to be explored. Keywords: Coronavirus, Chiroptera, Pteropus, Thailand Background the gene source of αCoV and βCoV, while avian CoVs are Coronaviruses (CoVs) are classified into four genera: sources of Gammacoronavirus,andDeltacoronavirus [2]. Alphacoronavirus (αCoV), Betacoronavirus (βCoV), Gam- Although there is single lineage in αCoV, βCoVs are fur- macoronavirus,andDeltacoronavirus [1]. CoVs infect ther separated into four lineages (A – D) [3]. Lineage A wide variety of mammals and birds, causing upper and βCoV, including bovine CoVs, human CoV (HCoV)-OC43 lower respiratory, hepatic, enteric and neurological ill- and related viruses, have been detected in various mam- nesses with varying severity. Bat CoVs (BtCoVs) are likely mals such as cows, horses, deer, antelopes, camels, gi- raffes, waterbucks, dogs, and humans worldwide, but not * Correspondence: [email protected] in bats. Lineages B-D βCoVs have been detected in bats 1Thai Red Cross Emerging Infectious Diseases - Health Science Centre, World Health Organization Collaborating Centre for Research and Training on Viral worldwide [4]. Zoonoses, Chulalongkorn Hospital, Faculty of Medicine, Chulalongkorn Currently, six CoV strains are known to cause human University, Bangkok, Thailand infection; four CoVs cause mild respiratory illness, Full list of author information is available at the end of the article © The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Wacharapluesadee et al. Virology Journal (2018) 15:38 Page 2 of 10 including two αCoVs: HCoV-NL63 and HCoV-229E, and viral quasispecies, and the degree to which the reservoir two βCoVs: HCoV-HKU1and HCoV-OC43 [5]. The other host interacts with humans [25]. To better understand two βCoVs cause severe respiratory tract infection with the prevalence, persistence, phylogeny, and potential for high-fatality rates, such as severe acute respiratory syn- interaction with humans, here we describe a comprehen- drome (SARS) and Middle East respiratory syndrome sive longitudinal study to detect CoV in LFF, and factors (MERS), belonging to lineages B and C, respectively. Bat influencing infectivity. Bat rectal swabs were collected related MERS-CoVs phylogenetically-related to humans monthly from their roosting area and from two human have been previously discovered in Tylonycteris pachypus dwellings (foraging sites) nearby. Individual bats were (BtCoV-HKU4) and Pipistrellus abramus (BtCoV-HKU5) weighed and forearm (FA) lengths were measured for in Hong Kong, in 2006 [6], Neoromicia capensis (Neo- further characterization on its body composition index CoV) from South Africa, in 2011 [7], and Pipistrellus cf. (BCI). Our results demonstrated for the first time that hesperidus (PREDICT/PDF-2180 CoV) from Uganda, in α- and β-CoVs are endemically circulating in LFFs in 2013 [8]. SARS-like BtCoV was initially identified from Thailand, and that age and BCI are significantly different the genus Rhinolophus in 2005, after the SARS outbreak between infected and uninfected bats. in humans in 2002–2003, and identification of virus in palm civets (Paguma larvata) from live animal market in Methods Guangdong, China in 2003 [9, 10]. Study sites BtCoVs have been identified in many insectivorous and LFFs were captured from the largest colony in Thailand frugivorous (family Pteropodidae) bats on many conti- (total population of around 10,000 bats) [22] at Chonburi nents: America, Europe, Africa, and Asia [4]. Different spe- province (Luang temple, 13,830,018.9”N, 101809054.9″E, cies of Pteropodidae have been identified as a major source 6 m asl) in Central Thailand. Bats were sampled from of lineage D βCoV (HKU9) in Africa (Rousettus aegyptia- three different sites: two human dwellings (bat foraging cus, Kenya [11], Pteropus rufus and Eidolon dupreanum, areas) situated at a mean distance of 0.6 km (S1) and Madagascar [12]), and Asia (R. leschenaulti,China[13], 5.5 km (S2 with a small open-system pig farm, 40 pigs) Cynopterus brachyotis, Philippines [14], Ptenochirus jagori, from a bat roost, and the bat roost (S3). Sampling was car- Philippines [15], Pteropus giganteus, Bangladesh [16], ried out under protocols approved and permitted by the Cynopterus sphinx,Thailand[17]. Department of National Parks, Wildlife and Plant Conser- Thailand is home to 146 bat species (125 insectivorous vation, Thailand (No. 0909.204/2686) and the Animal Use and 21 frugivorous) [18]. The prevalence and diversity of Protocol No.1473001 approved by Chulalongkorn Univer- BtCoVs in Thailand has been studied in the last decade sity Animal Care and Use Committee. [17, 19, 20]. CoVs were found in 11 insectivorous bat spe- cies and in 2 frugivorous bat species. However, data from Bat capture and sample collection Pteropus bats have been lacking despite Pteropus being LFFs were captured monthly during January – Decem- the biggest colony of Pteropodidae in Thailand. Three spe- ber 2012 from the three sites, S1–3 (Table 1). At S1 and cies (P. lylei, P. vampyrus and P. hypomelanus) are reser- S2, bats were captured 2 nights per month, where the voirs of Nipah virus (NiV) in Thailand [21]. The nets were set in the late evening, and captured animals prevalence of NiV RNA in urine of P. lylei has been sea- were removed immediately. At S3, 10–20 bats were cap- sonally detected during the months of May and June [22]. tured using mist-nets on the same nights as S1 and S2. P. lylei (Lyle’s flying fox (LFF)) ranges from Yunnan in Bats were not euthanized, and they were released after China, and extends to Cambodia, Thailand, and Vietnam measurements were taken and samples were collected. [23]. Up to 20 colonies have been identified in Thailand Bats were identified morphometrically and species, sex, [24] and the largest known colony comprises of about reproductive status, FA length and body mass were de- 10,000 individuals [22]. It shares foraging areas with termined. Rectal swab was collected from each individ- other frugivorous bats in fruit trees, from which the ual bat and immediately put into Lysis buffer fruits are also shared by humans. Moreover, trees in (bioMérieux, SA, France). The samples were transported populated temple grounds and cultivated land are com- to laboratory on ice within 48 h and stored at -80o C mon roosting sites for LFF. Thus, consumption of par- until further analysis. tially eaten fruit, uncooked meat, or contact with saliva, urine or faeces, which can be contaminated with bat vi- Nucleic acid extraction and CoV RNA detection ruses, poses a risk of viral transmission from LFF to Total nucleic acid was extracted from 1 ml of suspended humans or domestic animals. rectal swab using easyMAG® platform (bioMérieux, SA, The potential for emergence of zoonotic viruses into France). Elution volume was 50 μl. Hemi-nested Reverse the human population depends on the prevalence of the Transcription PCR (RT-PCR) was performed using virus in its host species, host range mutations within broadly reactive consensus PCR primers for CoV, Wacharapluesadee et al. Virology Journal (2018) 15:38 Page 3 of 10 Table 1 CoV positive bats, categorized by possible influential factors - collection site, age, sex and BCI (367 bats) Possible influential factor CoV PCR results: No.
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