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Molecular Epidemiology and Genome Analysis of Feline Morbillivirus In Chaiyasak et al. BMC Veterinary Research (2020) 16:240 https://doi.org/10.1186/s12917-020-02467-4 RESEARCH ARTICLE Open Access Molecular epidemiology and genome analysis of feline morbillivirus in household and shelter cats in Thailand Surangkanang Chaiyasak1,2, Chutchai Piewbang1,2, Anudep Rungsipipat1 and Somporn Techangamsuwan1,2* Abstract Background: Feline morbillivirus (FeMV) has been discovered in domestic cats associated with tubulointerstitial nephritis, but FeMV is also detected in healthy cats. This research aimed to identify and characterize the FeMV strains detected in a Thai cat population. Results: Two-hundred and ninety-two samples (131 urine and 161 blood) derived from 261 cats (61 sheltered and 200 household cats) were included for investigating the FeMV prevalence using real-time reverse transcription PCR. The overall prevalence of FeMV detection was 11.9% (31/261) among both samples, which accounted for 14.5% (19/131) and 7.5% (12/161) of the urine and blood samples, respectively. Among the FeMV-PCR positive cats, the FeMV-detected prevalence was insignificantly associated with healthy cats (58.1%; 18/31) or urologic cats (41.9%; 13/31). Full-length genome analysis of these FeMV-Thai strains revealed that their genomes clustered together in the FeMV-1A clade with up to 98.5% nucleotide identity. Selective pressure analysis showed that overall FeMV-1 has undergone negative selection, while positive selection sites were more frequently observed in the phosphoprotein gene. Conclusions: The detected FeMV infections in the Thai cat population were not correlated with urologic disorders, although the virus was more detectable in urine samples. The genetic patterns among the FeMV-1 Thai strains were more consistent. A large-scale study of FeMV in Thai cat samples is needed for further elucidation. Keywords: Feline morbillivirus, Fusion, Hemagglutinin, Phosphoprotein, Selective pressure analysis, Urine Background the host cells membrane, respectively [2]. Additionally, the Feline morbillivirus (FeMV), belonging to genus Morbilli- diversity of H gene characterization is potentially affected virus,familyParamyxoviridae, is a 16,050-bp length, non- the host range and virulence [3–6]. Since the first identifi- segmented, enveloped, single-stranded, negative-sense cation of FeMV in domestic cats showing tubulointersti- RNA virus, that encodes for six genes; nucleocapsid (N), tial nephritis in Hong Kong in 2012 [[1], the virus has phosphoprotein (P/V/C), matrix (M), fusion (F), been investigated in both clinically healthy and ill cats in hemagglutinin (H), and RNA polymerase (L) [1]. Among many countries, such as Japan, Turkey, Germany, Italy, the functional proteins, the H and F glycoproteins on the USA, Brazil, and Malaysia [7–16]. The prevalence of viral membrane play a key role for attaching and fusing FeMV detection ranges from 0.2–40% based on the tested samples, comprised such as blood, urine, rectal swab, fresh * Correspondence: [email protected] tissues, and formalin-fixed paraffin-embedded tissues [7– 1Department of Pathology, Faculty of Veterinary Science, Chulalongkorn 10, 12, 14–16]. Because the first emergence of FeMV was University, Bangkok 10330, Thailand 2Animal Virome and Diagnostic Development Research Group, Faculty of associating with renal disease, the initial studies on FeMV Veterinary Science, Chulalongkorn University, Bangkok 10330, Thailand identification were conducted in urine samples, while © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. 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 in a credit line to the data. Chaiyasak et al. BMC Veterinary Research (2020) 16:240 Page 2 of 9 comparison of FeMV detection in urine and other derived 6.5%). For the FeMV-positive urine samples, FeMV in- samples was also reported [1, 9]. Geographically, the fection was found in cats with UTD (11/19, 57.9%; all prevalence of FeMV-positive samples is seemingly were household cats), followed by no clinical significance inconsistent, with a higher detection rate in Japan (ranging or apparently healthy (6/19, 31.6%; all were shelter cats) from 6.1–23.1%) [9, 13, 17], Italy (ranging from 1.2– and chronic kidney disease (CKD) (2/19, 10.5%; both 31.8%) [8, 18], and Malaysia (50.8%) [12], while a lower were household cats) (Table 2). detection rate was reported in the USA, Germany, Brazil, and Turkey [7, 14–16, 18]. Association between the FeMV infection status, urine Currently, full-length genome analysis of FeMV has characteristics, urologic diseases and feline retrovirus categorized this virus into the two genotypes of FeMV-1 detection (former FeMV) [19, 20] and FeMV-2 (former FeMV- The urinalysis of the group A household cats was GT2), the latter of which was recently detected in cats determined in terms of the physical, chemical, and showing urinary tract disease (UTD) in Germany [19]. microscopic features and tabulated according to the The FeMV-1 genotype was subsequently clustered based FeMV-PCR positive results. Even though there were no on the partial L gene sequence into the FeMV-1A, −1B statistical significances between the presence of FeMV in and -1C subgroups [21]. However, neither the FeMV-1 the urine and the urine characteristics (P > 0.05), some nor FeMV-2 genotype is able to clarify the association features, such as hematuric, pyuric, proteinuric, and with nephropathy in cats [7, 11, 13, 14, 16, 19]. There- aciduric urines, had a higher numerical tendency to be fore, the genetic characteristics of FeMV in many positive with FeMV detection. Among the 91 urine regions remain to be elucidated for studying viral patho- samples with urologic conditions from 100 household genesis, such as different cellular tropism [19, 22]. cats examined, the positive FeMV in the urine was Since most RNA viruses are prone to mutation, due to evidenced at a six-fold lower rate (13/91, 14.3%), without the lack of an internal proof-reading mechanism during significance, than the negative FeMV counterpart (78/91, replication that results in a high rate of variant nucleo- 85.7%) (P > 0.05, Supplementary Table S2). Moreover, tide substitutions, the identification of local strains among the FeMV-PCR positive cats, only one shelter cat would be beneficial for the further future management each revealed a positive FeLV antigen (no. E27) and a of disease control and monitoring. The genetic FIV antibody (no. E61) (Table 2). characterization of the newly identified FeMV in Thailand would contribute to the basic knowledge of Phylogenetic analysis and genome organization of the not only the identification of FeMV but also on its full-length FeMV-Thai strains evolution. Thus, this study aimed to establish the identi- Three full-length FeMV-Thai strains were obtained and fication of FeMV Thai strains with viral genetic charac- have been submitted to GenBank as U16–2016 terizations. Molecular genetic recombination and (MF627832; 16,050 nt length), CTL16–2018 (MN1645 selective pressure analysis for evolutionary evaluation of 31; 15,946 nt length), and CTL43–2018 (MN164532; 15, the FeMV were also investigated. This fundamental data 949 nt length). After nucleotide alignment and analysis, on the molecular epidemiology of FeMV strains might all three FeMV-Thai strains displayed the six consecu- contribute to a more comprehensive understanding of tive gene sequences (N-P-M-F-H-L), comprised of the N FeMV evolution. (1,560 nt), P (1,476 nt), M (1,014 nt), F (1,632 nt), H (1, 788 nt), and L (6,609 nt) genes, which encoded for 520, Results 492, 338, 544, 596, and 2203 deduced amino acids, Detection of FeMV in the urine and blood of Thai cats respectively. The different genome lengths among these The presence of FeMV in all the samples was 11.9% (31/ three FeMV-Thai strains were due to the incomplete 261), as detected by the RT-qPCR assay. Among the nucleotide sequence at the 5′ end of CTL16–2018 and samples, the FeMV was detected at a two-fold higher CTL43–2018. rate in the urine (19/131, 14.5%; as six shelter and 13 Phylogenetic analysis of the full-length genome of the household cats) than in the blood (12/161, 7.5%; all were three FeMV-Thai strains revealed that they shared the shelter cats). However, from the 61 shelter cats same monophyletic topology of the FeMV-1 genotype examined, although 18/61 (29.5%) showed FeMV in and segregated into the FeMV-1A clade, clustered with either the blood or the urine, no any cat showed FeMV- the FeMV strains reported from Hong Kong (M252A) positive results in both sample types at the same time and Japan (strain ChJP073, MiJP003, SS2, and SS3) (Tables 1 and 2). (Fig. 1). Pairwise nucleotide identity analyses revealed Considering the category of tested cats, the presence that these FeMV-Thai strains had the highest nucleotide of FeMV detection in the shelter cats (18/61, 29.5%) was identity to the FeMV-1A strain SS3 (97.8–98.5%), and to 4.5-fold higher than in the household cats (13/200, a lesser extent, to the FeMV-1A strain M252A (97.5– Chaiyasak et al.
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