Abdullahi Abdullahi Raji1*
Abdul Rahman Omar2- 1Department of Veterinary Pathology, Faculty of Veterinary Medicine, Usmanu Danfodiyo University Sokoto, Sokoto, Nigeria
- 2Laboratory of Vaccine and Biomolecules, Institute of Bioscience and Department of Veterinary pathology and Microbiology Universiti Putra Malaysia, Serdang, Malaysia
Of the several known viruses, chicken astrovirus (CAstV) has been associated with diarrhea, runting-stunting syndrome, severe kidney disease, and gout, and white chick syndrome (WCS) in young broiler chicks. Discovered in 2004, CAstV consists of two genogroups with an expanding subgroup because of the diversity exhibited in its viral capsid sequence. Despite these findings, there exists a dearth of knowledge on its pathogenesis. This review highlights the pathogenesis and development of in vivo and in vitro models.
Introduction
Chicken astroviruses (CAstVs) are small, round, non-enveloped, positive-sense, single-stranded RNA viruses in the avian astrovirus genus of the Astroviridae family. They are ubiquitous in healthy and sick chickens and are capable of causing significant economic losses during infection. The prevalence and incidence of the virus have been reported in the UK, the US, Germany, China, Finland, Poland, Nigeria, South Africa, the Netherlands, and the Middle East (1–7). In the UK and Malaysia, a seroprevalence investigation reveals seropositivity of CAstV in four generations of broilers and broiler breeder flocks, respectively, (8, 9). Since the initial detection of CAstV in the flocks of commercial broiler chickens in 2004 (10), new strains of CAstV have been identified and characterized in chickens worldwide (5, 9, 11–17).
Previously, infections with astroviruses were assumed to be species specific; however, there are pieces of evidence strongly suggesting transmission between the avian species, such as turkey, chicken, and duck astroviruses, while exhibiting some share of identity in their genetic features (1, 18). In 2009, Todd et al. in a seroprevalence study, discovered CAstV antibodies in turkey breeder flocks in the UK. Similarly, a serosurvey on poultry abattoir workers has shown that the antibodies against turkey astrovirus are three times higher in the turkey processing workers when compared to the workers not in contact with turkey (19). Recently, CAstV was detected in cases of runting in day-old commercial turkey poults in southwestern Nigeria (20), and conceivably, this finding evidenced the possibility of cross-species transmission of CAstV to other avian species.
Despite the progress made in the detection and characterization of novel CAstVs (9, 14, 17, 21, 22), there is still a dearth of knowledge about its pathogenesis. Studies on both human and turkey astroviruses have demonstrated an increase in the permeability of intestinal epithelial cells, leading to the disruption of tight junctions between the cells (23, 24). Because the digestive system relies on cellular tight junctions to demarcate the lumen from the basal lamina, a loss of integrity increases water, solute, and ion movements through compartments, limiting the intestine's reabsorption capability and thus resulting in diarrhea (25). Furthermore, extra-intestinal astrovirus-related conditions have been reported in chickens, animals, and humans (11, 12, 26, 27), which could have stemmed from increased intestinal permeability. In addition, astroviruses, even while not replicating, exacerbate the permeability of renal epithelial cells (28). Although the exact pathway leading to diarrhea and spread to other organs/systems is continuously under investigation, the collective findings with turkey astrovirus (TAstV-2) suggest that astrovirus infection causes malabsorption of sodium salts, presumably as a result of redistribution of sodium transporters, thus resulting in osmotic diarrhea (25).
Like the turkey model, the murine model (murine astrovirus, MuAstV) was discovered by researchers in mice in 2012. However, in contrast to TAstV, diarrhea was absent in the infection caused by MuAstV. This finding is expected in mice because colitis must be induced before diarrhea (29, 30). Moreover, no intestinal damage was observed after the MuAstV infection. However, the virus caused an increase in intestinal permeability, indicating that increased permeability in the mouse model could be independent of diarrhea.
Recently, studies in chickens have helped to elucidate the molecular and cellular attributes of CAstV conditions (14, 31). This review, therefore, focuses on some of these findings and tries to outline the critical steps that need to be considered for further research on astroviruses.
Chicken Astrovirus (CAstV) Associated Diseases
Shortly after the discovery of astrovirus in 1975, small round virus particles with astrovirus morphology were recorded in domestic animals, particularly calves and lambs with gastroenteritis (32, 33) and ducks with viral hepatitis in the early 1980s leading to acute mortality (34), which conceivably served as the earliest indication of extra-intestinal tropism of astrovirus (35). Over the years, chickens, especially the broiler types, are found to be susceptible to varying conditions caused by astrovirus (4, 9). Within a few years of discovery, two distinct genogroups of CAstV (Group-A and Group-B) have been described. Group-B with six subgroups (Bi, Bii, Biii, Biv, Bv, and Bvi) is the most common worldwide and is majorly responsible for the three types of conditions related to CAstV (4, 9), while Group-A with three subgroups (Ai, Aii, and Aiii) is documented to be responsible for two out of the three conditions (4). However, there exists an extensive variation with regards to the geographic distribution in the prevalence of the conditions related to subgroup-B strains, and their link with the three clinical conditions remains unknown. For example, FP3 of the Bi subgroup, initially isolated from a dead-in-shell embryo in the UK, causes intestinal lesions 24 h post-inoculation and severe kidney lesions from day 1 up to 8 days post-inoculation (dpi) in specific pathogen-free (SPF) chickens (4, 36, 37), whereas the Indian strains have been identified to cause severe kidney disease with visceral gout in both broiler and SPF chickens (11). Similarly, with the exception of PL/059/2014 strain of Poland, a member of the Aiii subgroup, all the other strains responsible for white chick syndrome (WCS) originating from Canada and Brazil are clustered in Biv. Recently, in a study using SPF chickens, a Malaysian CAstV strain (UPM1019/2018) caused nephropathy and gouty lesions but were less severe compared to the UK and Indian strains (9).
Clinical manifestations vary from diarrhea (3–4 days after infection), to runting-stunting syndrome (6–12 days post-hatch), to weak and runted chicks in cases of hatchery disease or WCS, and to death, as a result of nephropathy and visceral gout, or in severe cases of WCS (10–12, 14, 31, 38). In a breeder flock, the clinical symptom is characterized by decreased production and hatchability, or mid-to-late dead-in-shell embryo (14, 26, 28, 38).
Chicken astrovirus infections are of clinical and economic concern due to their negative impact on production, owing to the increased severity of clinical symptoms and extra-intestinal involvement. Although other viruses have been implicated in cases of RSS, underperformance, and growth checks, recent studies have identified CAstV as the sole etiologic pathogen responsible for the condition in chickens and turkeys (10, 12, 20, 39). Similarly, DNA and RNA extracted from birds exhibiting underperformance, growth checks, and amplified using various enteric virus-specific primers were consistently positive for CAstV but negative for other enteric viruses (9, 17, 40). Next-generation sequencing and metagenomic approach, as an alternative, have been used to detect the presence of CAstV in the clinical samples (6, 41, 42). An experimental infection study with two US strains (CkP5 and CC_CkAstV) of subgroup-Biv (12) and a Malaysian strain (UPM1019/2018) of subgroup-Bv (9) presented decreased weight gain and cystic lesions in broiler and SPF chicks, respectively. These results are characteristic of RSS.
Furthermore, over the years, severe kidney disease and gout in chickens were associated with infectious bronchitis virus (IBV), avian nephritis virus (ANV) (a serologically and antigenically similar astrovirus identified before CAstV in chickens), and nutritional or managemental factors, but recently, these symptoms have been associated with CAstV (11, 39, 43, 44). Comparatively, the lesions caused by CAstV strains responsible for these conditions are severe and reported to cause 67.5 and 100% mortality in experimentally infected day-old broiler and SPF chickens, respectively. Remarkably, in a study by Bulbule et al. (11), a lower mortality rate was noticed in the broiler chickens when compared to that observed in the SPF chickens. This finding could be attributed to the presence of circulating maternal antibodies against CAstVs in the broiler chickens, which indicates that vaccination of broiler breeders against CAstV could possibly protect the chickens against CAstV infection during the first few days of life, thus preventing the disease.
On the other hand, kidney disease has also been observed in chickens with WCS in addition to the lesions seen on the feathers, intestine, and liver (4, 5, 14, 26, 38). The WCS was first recognized in the mid-1980s in Norway, Finland, Sweden, the US, and Canada (38, 45), with several cases documented in 2016 in Canada, Poland, Brazil, and the US (5, 40, 45, 46). Primarily, the disease is transmitted vertically and mostly affects the broiler-type of chicken (5, 47). A decrease in hatchability of 4 to 68%, mid-to-late dead-in-shell embryo and 100% mortality within the first few hours of weak hatched chicks have been documented in WCS (38, 46). The chickens affected by WCS present an enlarged intestine filled with yellow-green fluid and air bubbles, thus leading to decreased nutrient absorption by the intestinal epithelium (14, 25, 31, 48). The microscopic changes (biliary proliferation, accumulation of immature granulocytes, hyperplasia, and dilated epithelium with heterophils and eosinophilic debris) are observed in the liver and bile duct but absent in the intestines. The absence of microscopic lesions in the intestines was recently attributed to the activation of immunosuppressive cytokine, transforming growth factor-beta (TGF-β), during the course of CAstV infection (31). In addition, these alterations could lead to a lack of consumption and absorption of the yolk by the intestinal epithelium within the first few days of embryogenesis. The yolk sac is known to provide nourishment and equally supports the embryo in its early stage of life, and provides carotenoids for the maintenance of body movements before a normal yellow chick is hatched. This is primarily achieved by the utilization of zeaxanthin and lutein from the yolk sac (49, 50). WCS-affected chickens have a bigger and heavier yolk sac, as well as lower yolk absorption, leading to weak and uncolored chicks (31). Although the cause of depigmentation in “white chicks” is not known, it is speculated that alterations in the synthesis of melanin during embryogenesis could be responsible for this condition (40, 45, 46, 51). This alteration equally affects the eyes, as observed in chickens huddling together in a well thermoregulated pen house (52).
There are numerous similarities between the astrovirus infections in chickens and other animal species, including humans. Most animals infected with astrovirus, including humans, calves, piglets, turkeys, and lambs, develop diarrhea similar to chickens (4, 32, 53–57). However, some animal species remain asymptomatic (23, 33, 58). Therefore, the epidemiology and transmission mechanisms leading to asymptomatic astroviral infection in chickens and other animals, as corroborated by Schultz-Cherry et al. (22), remain unclear. Advancement in the area of molecular techniques will contribute to a greater understanding of the varying conditions of CAstV and other animal-related astroviral infections in terms of prevalence and genotype-specific infections.
Cell Culture And Animal Model
As with other astroviruses, the pathogenicity of CAstV remains unknown, although factors like chicken type and host age, virus strain and concentration, co-infections with other viruses, and maternal antibodies could influence the disease pattern (4). Similarly, propagation and isolation of the CAstV and other astroviruses in an in vitro system, such as embryonated chicken egg or cell culture, is complex and unpredictable (12, 59). Nevertheless, CAstV strains can replicate in different cell lines, and liver-derived LMH, chicken embryo kidney cells (CEKC), and chicken embryo liver (CEL) cell line are frequently used (10–12, 20, 39). LMH seems to be a suitable, permissive, and susceptible host cell line for the propagation and isolation of CAstV. In addition, different sites and routes in 5- to 8-day-old embryonated SPF chicken eggs, including chorioallantoic membrane (CAM) (5) and yolk sac (40, 60–62), have also been employed to isolate CAstV. However, some cell lines, such as MDCK, DFI, QM7, Vero, and Sf9, did not support the propagation of the virus (12).
The non-canonical HAstV-MLB (Melbourne) (MB1 to 3) and HAstV-VA/HMO (Virginia/Human-Mink-Ovine-like) strains were not supported by any cell line for propagation, similar to the majority of other avian and mammalian astroviruses (14, 62). However, with the identification of the human intestinal enteroids (HIE) (59) in 2020, the propagation of these viruses became possible. The reason behind why some isolates developed while others failed to grow is yet to be established. Unfortunately, till the receptor(s) of astrovirus are known, creating an appropriate cell culture system will be difficult (22, 58). With several groups working on the identification of astrovirus biding sites, crystallization of human and turkey astroviruses has discovered a polysaccharide motif in the capsid and spike proteins (22, 63, 64). As described by Kang et al. (12), trypsin usage in isolating CAstV in LMH cell line is not required as indicated for bovine, human, and swine astroviruses (59, 65–67).
In Kang et al. (12) study, cytopathic effect (CPE) and the detachment of predominant small round cells were observed in the third passage 72 and 120 h post-inoculation (pi), respectively, after inoculation of the subsequent passage. The observed CPE was further confirmed to be as a result of CAstV by using the alpha-beta neutralization test (12). Furthermore, the replication kinetics of CAstV was observed to be associated with the cell at 1 h pi with a few supernatant virions. Twelve hours later, the viral eclipse was noticed, with a complete replication cycle at 12 and 24 h. Analyses of post-inoculation time points (24, 48, 72, and 96 h) revealed a constant increase in the virus titers in both supernatant and cells (12).
Fluorescent in situ hybridization (FISH) of CAstV suggests that the replication of the virus is restricted to the enteric enterocytes. In the epithelial cells of the villous, the identification of the viral RNA was explicit within the first 12 hpi (12). The site of CAstV staining shifted from the villous epithelial cells to the crypt epithelial cells at 18 h pi. Viral RNA was detected abundantly in the crypt epithelial cells and also in the attenuated epithelial cells in a dilated crypt within 48 hpi (12).
In an experimental infection study using SPF day-old chickens, individual degenerating enterocytes of the small intestines were apparent along the basal edge of the villi by 3 dpi and continued through 5 dpi at the crypt epithelial cells. By 5 dpi, CAstV localized primarily in the small intestine. By 6 dpi, mild shortening of the villi was prominent, as well as the occasional clusters of necrotic enterocytes along the villous base correlating with the infection (22). Replication peaked at 2–5 dpi, and CAstV was intermittently observed at time points later than 12 dpi (12). Although CAstV restricts its viral RNA replication to the small intestine, its isolation from the spleen, kidney, thymus, bursa of Fabricius, pancreas, gut content, and liver in varying quantities, via conventional and real-time PCR, shows that it can be detected in a wide range of tissues (1, 14, 31, 61). Based on the replication kinetics of CAstV, the findings of the study indicated that villous epithelial cells were initially permissive and susceptible to CAstV infection but later became refractory to the entry of the virus. However, the virus disseminated and multiplied in the crypts of Lieberkühn. Since crypt epithelial cells actively divide and migrate toward the villi, it is hypothesized that CAstV would prefer immature intestinal cells. In addition, the CAstV replication cycle is documented to be short and self-limiting within a few days of infection (12, 68, 69).
Furthermore, immunity-related studies of CAstV showed that the relative levels of gene expression of some of the important cytokines are different in the various tissue samples, which include thymus, jejunum, liver, and spleen, of the chickens infected with CAstV-WCS isolates (31). It was also observed that several T-helper cells (Th1 and 2) were activated in response to these cytokines. While IFN-γ, IL-2, IL-8, IL-12 p40, IL-15, TGF-β4, TNF-SF-15, and t-BET were expressed in the liver of the chicks, some of the cytokines were expressed in the thymus, spleen, and jejunum. Interestingly, even with the significant viral concentrations in the spleen and jejunum, there was a lack of IFN-γ activation in both organs (31). At the nexus of non-specific and acquired immunities, increased IFN-γ expression, as well as the activation of IFN-γ-secreting NK and Th1 cells, indicates that the innate immune response is equally triggered (31). Similar to the turkey model (48), lesions were found to be absent in the gut epithelium due to the activation of transforming growth factor-beta (TGF-β), a potent immunosuppressive cytokine which was significantly expressed in the jejunum of the chickens infected with the CAstV-WCS isolates, thus leading to the downregulation of inflammatory response and consequently, absence of microscopic lesions (31, 70).
Furthermore, in Nuñez et al. (31) study, the liver expressed the highest levels of IL-8 and IL-15. In the same vein, a considerable quantity of heterophiles and lymphocytes were observed to infiltrate the liver. It is known that, in cases of viral infections, IL-15 exerts an anti-apoptotic effect on the cytotoxic cells, while keeping them alive, and simultaneously destroys a large number of infected cells (31). In contrast, in the liver, IL-8 contributes to the infiltration of heterophiles and macrophages (31). Moreover, in CAstV-WCS-related infections, TNF-SF-15 and IL-12 p40 were also observed in higher concentrations in the liver. As a cytokine expressed by endothelial cells, TNF-SF-15 induces apoptosis and reduces proliferation in an autocrine manner, which potentially explains the observed microscopic apoptotic processes. Accordingly, the activation of innate immunity is initiated by the expression of IL-12 p40 in an attempt to establish cellular-mediated immunity via Th1-mediated response.
With all these fascinating and limited findings and works on the pathogenesis of CAstV, it will be quite interesting to study the virus further.
Conclusion
With much still needed to be worked on, particularly on the pathogenesis of the virus, there has been progress in the areas of molecular characterization and typing of the virus. The recent discovery of Bv and Bvi subgroups reveals that CAstV-related conditions are widespread and affect the commercial poultry industry to a much greater extent than previously anticipated (9). In the same vein, the emergence of these novel CAstVs clearly shows the possibility of the virus to spread systematically and cause varying pathologies in chickens, as observed in human and bovine astroviruses that have been reported to cause meningitis and encephalitis. Similar to other astroviruses, it has also been established that CAstV causes diarrhea in the absence of microscopic lesions, by disrupting tight junctions and allowing water influx, and finally diarrhea. In addition, studies in the turkey and murine models revealed that the viral capsid alone can cause diarrhea in vivo. Even with all these advances in the study of CAstV and other astroviruses, we, nonetheless, confront hurdles in having a standardized animal model that will elucidate the pathogenesis of astrovirus and the subsequent production of the vaccine, therapeutics, and cross-species infections. Unlike HAstV, chickens or turkey poults can perfectly be utilized for the studies related to CAstV pathogenesis and hence serve as a basis for further research on astrovirus.
Author Contributions
AR: conceptualization, writing-preparation and writing of the first draft, writing-review and editing. AO: concept, formatting, initial review, approval for publication and agree with final publication of the article.
Conflict of Interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's Note
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References
1. Todd D, Wilkinson DS, Jewhurst HL, Wylie M, Gordon AW, Adair BM, et al. seroprevalence investigation of chicken astrovirus infections. Avian Pathol. (2009) 38:301–9. doi: 10.1080/03079450903055421
2. Kang K, El-gazzar M, Sellers HS, Dorea F, Williams SM, Kim T, et al. Investigation into the aetiology of runting and stunting syndrome in chickens. Avian Pathol. (2012) 41:41–50. doi: 10.1080/03079457.2011.632402
3. Smyth VJ, Todd D, Trudgett J, Lee A, Welsh MD. Capsid protein sequence diversity of chicken astrovirus. Avian Pathol. (2012) 41:151–9. doi: 10.1080/03079457.2011.652938
4. Smyth VJ. A review of the strain diversity and pathogenesis of chicken astrovirus. Viruses. (2017) 9:1–10. doi: 10.3390/v9020029
5. Sajewicz-Krukowska J, Pać K, Lisowska A, Pikuła A, Minta Z, Króliczewska B, et al. Astrovirus-induced “white chicks” condition – field observation, virus detection and preliminary characterization. Avian Pathol. (2016) 45:2–12. doi: 10.1080/03079457.2015.1114173
6. Kwoka KTT, Rooij MMT de, Messink AB, Wouters IM, Smit LAM, Heederik DJJ, et al. Comparative viral metagenomics from chicken feces and farm dust in the Netherlands. bioRxiv. (2021). doi: 10.1101/2021.03.09.434704
7. Oluwayelu DO, Todd D. Chicken astrovirus infection: minireview and preliminary serologic evidence of antigenically and genetically distinct chicken astroviruses in Nigerian indigenous chickens. African J Biomed Res. (2012) 15:71–6.
8. Todd D, Smyth VJ, Ball NW, Donnelly BM, Wylie M, Knowles NJ, et al. Identification of chicken enterovirus-like viruses, duck hepatitis virus type 2 and duck hepatitis virus type 3 as astroviruses. Avian Pathol. (2009) 38:21–9. doi: 10.1080/03079450802632056
9. Raji AA, Ideris A, Bejo MH, Omar AR. Molecular characterisation and pathogenicity of novel Malaysian chicken astrovirus isolates. Avian Pathol. (2021) 51:51–65. doi: 10.1080/03079457.2021.2000939
10. Baxendale W, Mebatsion T. The isolation and characterisation of astroviruses from chickens. Avian Pathol. (2004) 33:364–70. doi: 10.1080/0307945042000220426
11. Bulbule NR, Mandakhalikar KD, Kapgate SS, Deshmukh VV, Schat KA, Chawak MM. Role of chicken astrovirus as a causative agent of gout in commercial broilers in India. Avian Pathol. (2013) 42:464–73. doi: 10.1080/03079457.2013.828194
12. Kang KIl, Linnemann E, Icard AH, Durairaj V, Mundt E, Sellers HS. Chicken astrovirus as an aetiological agent of runting-stunting syndrome in broiler chickens. J Gen Virol. (2018) 99:512–24. doi: 10.1099/jgv.0.001025
13. Nuñez LFN, Parra SHS, Carranza C, Astolfi-Ferreira CS, Buim MR, Ferreira AJP. Detection and molecular characterization of chicken astrovirus associated with chicks that have an unusual condition known as “white chicks” in Brazil. Poult Sci. (2016) 95:1262–70. doi: 10.3382/ps/pew062
14. Palomino-Tapia V, Mitevski D, Inglis T, van der Meer F, Martin E, Brash M, et al. Chicken Astrovirus (CAstV) molecular studies reveal evidence of multiple past recombination events in sequences originated from clinical samples of White Chick Syndrome (WCS) in Western Canada. Viruses. (2020) 12:1096. doi: 10.3390/v12101096
15. Rajendra Bulbule N, Sanjay Kapgate S, Madhukar Chawak M. Infectious causes of gout. Adv Anim Vet Sci. (2014) 2:255–60. doi: 10.14737/journal.aavs/2014/2.4.255.260
16. Xue J, Han T, Xu M, Zhao J, Zhang G. The first serological investigation of Chicken astrovirus infection in China. Biologicals. (2017) 47:22–4. doi: 10.1016/j.biologicals.2017.03.005
17. Yin L, Zhou Q, Mai K, Huang J, Yan Z, Wei X, et al. Isolation and characterization of a novel chicken astrovirus in China. Poult Sci. (2021) 100:101363. doi: 10.1016/j.psj.2021.101363
18. Pantin-Jackwood MJ, Strother KO, Mundt E, Zsak L, Day JM, Spackman E. Molecular characterization of avian astroviruses. Arch Virol. (2011) 156:235–44. doi: 10.1007/s00705-010-0849-z
19. Meliopoulos VA, Kayali G, Burnham A, Oshansky CM, Thomas PG, Gray GC, et al. Detection of antibodies against Turkey astrovirus in. PLoS ONE. (2014) 9:e96934. doi: 10.1371/journal.pone.0096934
20. Adebiyi AI, Mcilwaine K, Oluwayelu DO, Smyth VJ. Detection and characterization of chicken astrovirus associated with hatchery disease in commercial day-old turkeys in southwestern Nigeria. Arch Virol. (2021) 166:1607–14. doi: 10.1007/s00705-021-05034-w
21. Day JM, Zsak L. Recent progress in the characterization of avian enteric viruses. Avian Dis. (2013) 57:573–80. doi: 10.1637/10390-092712-Review.1
22. Schultz-Cherry VMS, Meliopoulos V, Schultz-Cherry S. Astrovirus Pathogenesis. In: Schultz-Cherry S, editor. Astrovirus Research: Essential Ideas, Everyday Impacts, Future Directions. New York, NY: Springer US. p. 65–78.
23. Moser LA, Schultz-Cherry S. Pathogenesis of astrovirus infection. Viral Immunol. (2005) 18:4–10. doi: 10.1089/vim.2005.18.4
24. Koci MD, Kelley LA, Larsen D, Schultz-Cherry S. Astrovirus-induced synthesis of nitric oxide contributes to virus control during infection. J Virol. (2004) 78:1564–74. doi: 10.1128/JVI.78.3.1564-1574.2004
25. Nighot PK, Moeser A, Ali RA, Blikslager AT, Koci MD. Astrovirus infection induces sodium malabsorption and redistributes sodium hydrogen exchanger expression. Virology. (2010) 401:146–54. doi: 10.1016/j.virol.2010.02.004
26. Saif YM, Swayne DE, Pantin-Jackwood MJ, Spackman E, Johnson TJ, Day JM, et al. “Emerging diseases and diseases of complex or unknown etiology. In: Swayne DE, Boulianne M, Logue CM, McDougald LR, Nair V, Suarez DL, et al. Diseases of Poultry. Wiley Online Books: Wiley-Blackwell. p. 1383–410. doi: 10.1002/9781119371199.ch33
27. Janowski AB, Klein RS, Wang D. Differential in vitro infection of neural cells by astroviruses. MBio. (2019) 10:1–14. doi: 10.1128/mBio.01455-19
28. Rebel JMJ, Balk FRM, Post J, Van Hemert S, Zekarias B, Stockhofe N. Malabsorption syndrome in broilers. Worlds Poult Sci J. (2006) 62:17–30. doi: 10.1079/WPS200481
29. Marvin S, Meliopoulos V, Schultz-Cherry S. Human astrovirus propagation, purification and quantification. Bio Protocol. (2014) 4:1–23. doi: 10.21769/BioProtoc.1078
30. Melgar S, Karlsson A, Michaëlsson E. Acute colitis induced by dextran sulfate sodium progresses to chronicity in C57BL/6 but not in BALB/c mice: correlation between symptoms and inflammation. Am J Physiol Gastrointest Liver Physiol. (2005) 288:1328–38. doi: 10.1152/ajpgi.00467.2004
31. Nuñez LFN, Santander-Parra SH, Kyriakidis NC, Astolfi-Ferreira CS, Buim MR, De la Torre D, et al. Molecular characterization and determination of relative cytokine expression in naturally infected day-old chicks with chicken astrovirus associated to white chick syndrome. Animals. (2020) 10:1–18. doi: 10.3390/ani10071195
32. Snodgrass DR, Angus KW, Gray EW, Menzies JD, Paul G. Pathogenesis of diarrhoea caused by astrovirus infections in lambs. Arch Virol. (1979) 60:217–26. doi: 10.1007/BF01317493
33. Woode GN, Gourley NE, Pohlenz JF, Liebler EM, Mathews SL, Hutchinson MP. Serotypes of bovine astrovirus. J Clin Microbiol. (1985) 22:668–70. doi: 10.1128/jcm.22.4.668-670.1985
34. Gough RE, Borland ED, Keymer IF, Stuart JC. An outbreak of duck hepatitis yype II in commercial ducks. Avian Pathol. (1985) 14:227–36. doi: 10.1080/03079458508436224
35. De Benedictis P, Schultz-Cherry S, Burnham A, Cattoli G. Astrovirus infections in humans and animals - molecular biology, genetic diversity, and interspecies transmissions. Infect Genet Evol. (2011) 11:1529–44. doi: 10.1016/j.meegid.2011.07.024
36. Pantin-Jackwood MJ, Spackman E, Woolcock PR. Molecular characterization and typing of chicken and turkey astroviruses circulating in the United States: implications for diagnostics. Avian Dis. (2006) 50:397–404. doi: 10.1637/7512-020606R.1
37. Spackman D, Gough RE, Collins MS, Lanning D. Isolation of an enterovirus-like agent from the meconium of dead-in-shell chicken embryos. Vet Rec. (1984) 114:216–8. doi: 10.1136/vr.114.9.216-a
38. Smyth V, Trudgett J, Wylie M, Jewhurst H, Conway B, Welsh M, et al. Chicken astrovirus detected in hatchability problems associated with ‘white chicks. Vet Rec. (2013) 173:403–4. doi: 10.1136/vr.f6393
39. Zhao W, Wu Z, Yao Y, Qin A, Qian K. The isolation and molecular characterization of an astrovirus from “Yellow” chickens, China. Front Vet Sci. (2020) 7:1–10. doi: 10.3389/fvets.2020.581862
40. Nunez L, Parra SH, Mettifogo E, Catroxo MH, Astolfi-Ferreira CS, Piantino Ferreira AJ. Isolation of chicken astrovirus from specific pathogen-free chicken embryonated eggs. Poult Sci. (2015) 94:947–54. doi: 10.3382/ps/pev086
41. Devaney R, Trudgett J, Trudgett A, Meharg C, Smyth V. A metagenomic comparison of endemic viruses from broiler chickens with runting-stunting syndrome and from normal birds. Avian Pathol. (2016) 45:616–29. doi: 10.1080/03079457.2016.1193123
42. Pérot P, Lecuit M, Eloit M. Astrovirus diagnostics. Viruses. (2017) 9:1–14. doi: 10.3390/v9010010
43. Imada T, Yamaguchi S, Mase M, Tsukamoto K, Kubo M, Morooka A. Avian nephritis Virus (ANV) as a new member of the family astroviridae and construction of infectious ANV cDNA. J Virol. (2000) 74:8487–93. doi: 10.1128/JVI.74.18.8487-8493.2000
44. Patel AK, Pandit RJ, Thakkar JR, Hinsu AT, Pandey VC, Pal JK, et al. Complete genome sequence analysis of chicken astrovirus isolate from India. Vet Res Commun. (2017) 41:67–75. doi: 10.1007/s11259-016-9673-6
45. Long KE, Hastie GM, Ojkić D, Brash ML. Economic impacts of white chick syndrome in Ontario, Canada. Avian Dis. (2017) 61:402–8. doi: 10.1637/11592-012217-CaseR
46. Sajewicz-Krukowska J, Domanska-Blicharz K. Nearly full-length genome sequence of a novel astrovirus isolated from chickens with ‘white chicks' condition. Arch Virol. (2016) 161:2581–7. doi: 10.1007/s00705-016-2940-6
47. Lee A, Wylie M, Smyth VJ, Skibinska A, Patterson IA, Forster F, et al. Chicken astrovirus capsid proteins produced by recombinant baculoviruses: potential use for diagnosis and vaccination. Avian Pathol. (2013) 42:434–42. doi: 10.1080/03079457.2013.822467
48. Koci MD, Moser LA, Kelley LA, Larsen D, Brown CC, Schultz-Cherry S. Astrovirus induces diarrhea in the absence of inflammation and cell death. J Virol. (2003) 77:11798–808. doi: 10.1128/JVI.77.21.11798-11808.2003
49. Moreno JA, Díaz-Gómez J, Nogareda C, Angulo E, Sandmann G, Portero-Otin M, et al. The distribution of carotenoids in hens fed on biofortified maize is influenced by feed composition, absorption, resource allocation and storage. Sci Rep. (2016) 6:1–11. doi: 10.1038/srep35346
50. Weaver RJ, Santos ESA, Tucker AM, Wilson AE, Hill GE. Carotenoid metabolism strengthens the link between feather coloration and individual quality. Nat Commun. (2018) 9:73. doi: 10.1038/s41467-017-02649-z
51. Smyth JRJ. Genetics of plumage, skin and eye pigmentation in chickens. In: Crawford RD, editor. Poultry Breeding and Genetics. Amsterdam: Elsevier (1990). p. 109–67.
52. Chang CM, Coville JL, Coquerelle G, Gourichon D, Oulmouden A, Tixier-Boichard M. Complete association between a retroviral insertion in the tyrosinase gene and the recessive white mutation in chickens. BMC Genomics. (2006) 7:1–15. doi: 10.1186/1471-2164-7-19
53. Behling-Kelly E, Schultz-Cherry S, Koci M, Kelley L, Larsen D, Brown C. Localization of astrovirus in experimentally infected turkeys as determined by in situ hybridization. Vet Pathol. (2002) 39:595–8. doi: 10.1354/vp.39-5-595
54. Bosch A, Pintó RM, Guix S. Human astroviruses. Clin Microbiol Rev. (2014) 27:1048–74. doi: 10.1128/CMR.00013-14
55. Qureshi MA, Yu M, Saif YM. A novel “small round virus” inducing poult enteritis and mortality syndrome and associated immune alterations. Avian Dis. (2000) 44:275. doi: 10.2307/1592540
56. Reynolds DL, Saif YM. Astrovirus: a cause of an enteric disease in Turkey poults. Avian Dis. (1986) 30:728. doi: 10.2307/1590577
57. Woode GN, Bridger JC. Isolation of small viruses resembling astroviruses and caliciviruses from acute enteritis of calves. J Med Microbiol. (1978) 11:441–52. doi: 10.1099/00222615-11-4-441
58. Meliopoulos V, Schultz-Cherry S. Astrovirus pathogenesis. astrovirus res essent ideas, everyday impacts. Futur Dir. (2013) 9781461447:65–77. doi: 10.1007/978-1-4614-4735-1_4
59. Kolawole AO, Mirabelli C, Hill DR, Svoboda SA, Janowski AB, Passalacqua KD, et al. Astrovirus replication in human intestinal enteroids reveals multi-cellular tropism and an intricate host innate immune landscape. PLoS Pathog. (2019) 15:1–30. doi: 10.1371/journal.ppat.1008057
60. de Wit JJ, ten Dam GB, vande Laar JMAM, Biermann Y, Verstegen I, Edens F, et al. Detection and characterization of a new astrovirus in chicken and turkeys with enteric and locomotion disorders. Avian Pathol. (2011) 40:453–61. doi: 10.1080/03079457.2011.596813
61. Smyth JA, Connor TJ, McNeilly F, Moffet DA, Calvert VM, McNulty MS. Studies on the pathogenicity of enterovirus-like viruses in chickens. Avian Pathol. (2007) 36:119–26. doi: 10.1080/03079450601161398
62. Smyth VJ, Jewhurst HL, Adair BM, Todd D. Detection of chicken astrovirus by reverse transcriptase-polymerase chain reaction. Avian Pathol. (2009) 38:293–9. doi: 10.1080/03079450903055397
63. Dong J, Dong L, Méndez E, Tao Y. Crystal structure of the human astrovirus capsid spike. Proc Natl Acad Sci U S A. (2011) 108:12681–6. doi: 10.1073/pnas.1104834108
64. DuBois RM, Freiden P, Marvin S, Reddivari M, Heath RJ, White SW, et al. Crystal structure of the avian astrovirus capsid spike. J Virol. (2013) 87:7853–63. doi: 10.1128/JVI.03139-12
65. Taylor MB, Grabow WOK, Cubitt WD. Propagation of human astrovirus in the PLC/PRF/5 hepatoma cell line. J Virol Methods. (1997) 67:13–8. doi: 10.1016/S0166-0934(97)00071-2
66. Aroonprasert D, Fagerland JA, Kelso NE, Zheng S, Woode GN. Cultivation and partial characterization of bovine astrovirus. Vet Microbiol. (1989) 19:113–25. doi: 10.1016/0378-1135(89)90077-1
67. Indik S, Valíček L, Šmíd B, Dvoráková H, Rodák L. Isolation and partial characterization of a novel porcine astrovirus. Vet Microbiol. (2006) 117:276–83. doi: 10.1016/j.vetmic.2006.06.020
68. Pantin-jackwood MJ, Spackman E, Day JM, Spackman E, Day JM, Pantin-jackwood MJ, et al. Pathogenesis of type 2 turkey astroviruses with variant capsid genes in 2-day-old specific pathogen free poults. Avian Pathol. (2008) 37:193–201. doi: 10.1080/03079450801932200
69. Toffan A, Catania S, Salviato A, de Battisti C, Vascellari M, Toson M, et al. Experimental infection of poults and guinea fowl with genetically distinct avian astroviruses. Avian Pathol. (2012) 41:429–35. doi: 10.1080/03079457.2012.704980
Keywords: chicken astrovirus, pathogenesis, pathology, animal model, genotypes
Citation: Raji AA and Omar AR (2022) Pathogenesis of Chicken Astrovirus Related Illnesses. Front. Vet. Sci. 9:899901. doi: 10.3389/fvets.2022.899901
Received: 19 March 2022; Accepted: 26 April 2022;
Published: 10 June 2022.
Edited by:
Jun Ji, Nanyang Normal University, ChinaReviewed by:
Ziqiang Cheng, Shandong Agricultural University, ChinaCopyright © 2022 Raji and Omar. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Abdullahi Abdullahi Raji, YWJkdWxsYWhpLnJhamkmI3gwMDA0MDt1ZHVzb2suZWR1Lm5n