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Experimental Co-Infection of Variant Infectious Bursal Disease Virus And Xu et al. Vet Res (2021) 52:61 https://doi.org/10.1186/s13567-021-00932-y RESEARCH ARTICLE Open Access Experimental co-infection of variant infectious bursal disease virus and fowl adenovirus serotype 4 increases mortality and reduces immune response in chickens A‑hui Xu, Lu Sun, Kai‑hang Tu, Qing‑yuan Teng, Jia Xue* and Guo‑zhong Zhang* Abstract Infectious bursal disease virus (IBDV) and fowl adenovirus serotype 4 (FAdV‑4) cause infectious bursal disease (IBD) and hydropericardium‑hepatitis syndrome, respectively. Recently, studies have reported co‑infections of poultry with IBDV and FAdV‑4, which is an important problem in the poultry industry. Here, the variant IBDV strain ZD‑2018‑1 and FAdV‑4 isolate HB1501 were used to assess the pathogenicity of co‑infection in 1‑day‑old specifc pathogen‑free (SPF) chickens. Compared with chickens infected with only FAdV‑4, those coinfected with IBDV and FAdV‑4 showed enhanced clinical symptoms, higher mortality, more severe tissue lesions, and higher biochemical index levels. Fur‑ thermore, the expression of interleukin (IL)‑6, IL‑1β, and interferon‑γ mRNAs in the IBDV‑FAdV‑4 coinfected chickens was delayed, and the antibody response levels were signifcantly lower in those birds compared with the FAdV‑ 4‑infected chickens. These results indicate that co‑infection with variant IBDV ZD‑2018‑1 and FAdV‑4 HB1501 could signifcantly promote the pathogenicity of FAdV‑4 and reduce the immune response in chickens. This study provides the foundation for further investigation of the interaction mechanism in IBDV and FAdV‑4 co‑infection. Keywords: Infectious bursal disease virus, Fowl adenovirus serotype 4, Co‑infection, Pathogenicity Introduction susceptibility to secondary infection and vaccination fail- Infectious bursal disease virus (IBDV) is an icosahedral, ure [4]. IBDV has two serotypes. Serotype I viruses are non-enveloped, double-stranded RNA virus belonging to pathogenic to chickens, whereas serotype II viruses are the genus Avibirnavirus, in the family Birnaviridae, which not. Serotype I IBDV can be classifed into four pheno- can cause an acute, highly contagious, immunosuppres- types: antigenic variant strains, classical strains, attenu- sive disease known as infectious bursal disease (IBD) [1, ated strains, and highly virulent strains [5]. Recently, a 2]. Tis disease of young chickens is characterized mainly novel antigenic variant IBDV has been prevalent in east- by gelatinous material exudation, atrophy, or hemorrhage ern China [6, 7]. Notably, the present commercial IBDV of the bursa of Fabricius (BF) [3]. Te damage to the BF vaccine cannot provide protect against this novel variant impairs the immune function of infected chickens, lead- IBDV [6, 8], which poses a new challenge for the poultry ing to immunosuppression and resulting in increased industry. Fowl adenovirus (FAdV), is an icosahedral, non-envel- oped, double-stranded DNA virus belonging to the genus *Correspondence: [email protected]; [email protected] Aviadenovirus in the family Adenoviridae [9]. Aviad- Key Laboratory of Animal Epidemiology of the Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, enoviruses can classifed into fve species, FAdV-A to Beijing 100193, China FAdV-E, and 12 serotypes, FAdV-1 to -8a and FAdV-8b © The Author(s) 2021. 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:// creat iveco mmons. org/ licen ses/ by/4. 0/. The Creative Commons Public Domain Dedication waiver (http:// creat iveco mmons. org/ publi cdoma in/ zero/1. 0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Xu et al. Vet Res (2021) 52:61 Page 2 of 11 to -11 [10]. Infection with FAdVs can cause various clini- FAdV-only, IBDV-FAdV co-infection, and IBDV-only. At cal symptoms, including gizzard erosion, inclusion body 1 day of age, the chickens in the IBDV-FAdV co-infection hepatitis, and hydropericardium-hepatitis syndrome or IBDV-only groups were orally inoculated with 200 µL 3 [11]. FAdV-4 was frst reported in Angara Goth, Pakistan of 10 CID50 of IBDV-ZD-2018-1 while those in the con- in 1987 and subsequently spread worldwide [12], caus- trol or FAdV-only groups were orally inoculated with 200 ing huge economic losses to the poultry industry. Since µL of normal saline solution. At 14 days of age, the chick- 2015, FAdV-4 has occurred in several provinces in China ens in the FAdV-only or IBDV-FAdV co-infection groups 6 [11, 13–15] and attracted much attention in the poul- were challenged with 200 µL of 10 TCID50 of FAdV- try industry. Furthermore, some studies have reported 4-HB1501 via the oral route, while those in the control that poultry can become coinfected with FAdV and or IBDV-only groups were inoculated with 200 µL of other avian diseases, such as avian infuenza virus (AIV), normal saline solution via the same route. Ten chickens IBDV, and chicken infectious anemia virus (CIAV) [16– in each group were marked for clinical observation, and 19]. FAdV co-infection with other infectious agents has the remainder was used for sample collection. Food and become a non-negligible issue. water were provided ad libitum throughout the study. Te interactions between FAdV, the coinfecting agents, Te 10 marked chickens from each group were observed and their hosts need to be further investigated. Previ- daily for clinical signs over the 14 days following FAdV ous research has shown that highly virulent IBDV can infection. Symptoms were scored as described in a previ- enhance the pathogenicity of inclusion body hepati- ous study [7]. At 1, 3, 5, and 7 days post-infection (dpi) tis virus (IBHV) [20]. Te objective of this study was to with FAdV-4-HB1501, three birds randomly selected investigate the interaction mechanism between FAdV, from each group were euthanized for necropsy and phys- IBDV, and their host by examining specifc pathogen-free ical examination. Te liver, spleen, kidneys, thymus, BF, (SPF) chickens coinfected with the currently circulating and duodenum were collected for use in virus detection novel variant IBDV and the epidemic FAdV-4 isolate. and temporarily stored at −80 °C. Samples of the tissues described above were also preserved in 10% neutral for- Materials and methods malin for histopathological examination. Cloacal swabs Cell line, animals, and ethics statement were collected for the detection of viral shedding. Serum A male leghorn hepatoma cell line (LMH) was kept in samples were collected for the detection of biochemical our laboratory. One-day-old and 3-week-old SPF chick- indices. ens were purchased from the Beijing Boehringer Ingel- heim Vital Biotechnology Co., Ltd. (China) and housed Histopathology test in isolators at China Agricultural University. All animal Tissue samples fxed in 10% neutral formalin were pro- experiments were approved by Beijing Administration cessed routinely, embedded in parafn, cut into 5-µm Committee of Laboratory Animals under the leadership sections, and stained with hematoxylin and eosin. Te of the Beijing Association for Science and Technology microscopic lesions of the tissue sections were then (approval ID SYXK [Jing] 2018-0038). Te protocols for observed under a light microscope. Te lesions at 5 dpi this experiment were approved by the Animal Welfare were scored according to the severity of the histopathol- and Ethical Censor Committee at China Agricultural ogy change. Samples with a lack of obvious lesions were University. scored as 0, while those with slight, moderate, and severe lesions were scored as 1, 2, and 3, respectively. Viruses Te IBDV strain ZD-2018-1 (IBDV-ZD-2018-1) was FAdV detection with RT‑qPCR propagated in SPF chickens infected orally, and the titer Total DNA was extracted from the tissues and cloacal of IBDV-ZD-2018-1 in 3-week-old SPF chickens was swabs described above using a TIANamp Genomic DNA 4.2 10 the median chicken infectious dose (CID50)/0.2 mL Kit (Tiangen Biotech, Beijing, China) in accordance with [7]. Te FAdV-4 strain HB1501 (FAdV-4-HB1501) the manufacturer’s instructions. Te obtained DNA was was reproduced in LMH cells grown at 37 °C and was used to quantify the viral load by RT-qPCR. Primers titrated by 50% tissue culture infection dose (TCID50) in were designed based on conserved regions of the FAdV LMH cells [21]. Te titer of FAdV-4-HB1501 was 107.5 genome using Primer Premier 5.0 (N-F: 5′AAA ACT GAG ′ ′ TCID50/0.1 mL. ACT TTC CCA CAA 3 ; N-R: 5 AGA TAC CCT CCG AAG AAC TAC 3′), as described by Li et al. [17]. All samples Experimental design were tested in triplicate, and assays were repeated at least A total of 140 1-day-old SPF chickens were randomly twice. Te FAdV load was calculated from a standard divided into four groups of 35 birds each: control group, curve. Xu et al. Vet Res (2021) 52:61 Page 3 of 11 Expression assessment of immune‑related genes chickens in each group at 7 days post-co-infection.
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