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. 2024 Jun 25;103(9):104006. doi: 10.1016/j.psj.2024.104006

FAdV-4 can cause more noticeable clinical symptoms compared to FAdV-8b after infecting specific pathogen free chickens

Qinqin Sun *,†, Yajuan Li *,†, Yunfei Huang *,†, Shun Li *,†, Qiang Fu ⁎,†, Sidang Liu ‡,1
PMCID: PMC11519683  PMID: 39002371

Abstract

Chickens infected with FAdV-4 and FAdV-8b both exhibit hepatic lesions characterized by hemorrhagic necrosis and intranuclear inclusion body formation. However, only FAdV-4 induces pericardial effusion and acute mortality in chickens. To investigate the similarities and differences in the pathogenicity of HPS and IBH, this study intends to compare the infectivity and pathogenicity of FAdV-4 and FAdV-8b, 2 serotypes of fowl adenovirus isolated in our laboratory. The 2 viruses were respectively inoculated subcutaneously into SPF chicks at the neck. The clinical manifestations and pathological changes in these infected groups of chickens differed to some extent. Chickens infected with FAdV-4 exhibit evident depression and acute mortality, with a mortality rate of 60%; while those infected with FAdV-8b only display mild depression. Postmortem examination reveals serosanguinous effusion in the pericardial sac, spot-like hemorrhage, and focal necrosis in the liver of chickens infected with FAdV-4. Additionally, various degrees of edema are observed in organs such as the lungs, spleen, kidneys, and pancreas. In contrast, chickens infected with FAdV-8b exhibit spot-like hemorrhage and focal necrosis in the liver but do not display pericardial effusion or widespread organ edema. Histopathological examination demonstrates that both FAdV-4 and FAdV-8b can induce inflammatory reactions of varying degrees in the kidneys, pancreas, and duodenum of chickens, while reducing the necrosis of bursa of Fabricius, thymus, and spleen lymphocytes. Our data preliminarily reveal that both FAdV-4 and FAdV-8b can induce strong pathogenicity in chickens.

Key words: FAdV-4, FAdV-8b, infection, pathogenicity

INTRODUCTION

Fowl adenoviruses (FAdVs) are non-enveloped, double-stranded DNA viruses belonging to the family Adenoviridae, genus Aviadenovirus. They are divided into 3 groups based on antigenic differences (FAdV-Ⅰ–III) (Zhao, et al., 2015). Group I comprises 5 species (A–E) and 12 serotypes (FAdV-1 to 11; FAdV-8 is further divided into types a and b) (Domanska-Blicharz, et al., 2011; Choi, et al., 2012; Asthana, et al., 2013). FAdV-I can cause chicken hydropericardium syndrome (HPS) and inclusion body hepatitis (IBH). HPS is primarily caused by serotype 4 fowl adenovirus (FAdV-4) (Vera-Hernández, et al., 2016), while IBH can result from infection with various serotypes of FAdV including FAdV-8b, FAdV-7, and FAdV-11;Affected chickens typically exhibit hemorrhagic necrosis in the liver, along with the formation of intranuclear inclusion bodies (Steer-Cope, et al., 2019). While the liver lesions are similar in both HPS and IBH cases, only HPS is characterized by pericardial effusion and acute mortality.

The main manifestations of chickens infected with FAdV-4 include ventricular dilation, softening of the myocardium, and 90% of the chickens have pericardial effusion, which appears as pale yellow fluid or gelatinous, with a volume ranging from 1 to 30 mL. The majority of serotypes of FAdV-I can harm a chicken's liver. For instance, both FAdV-4 and FAdV-8b infections in chicken livers show similar lesions, characterized by hemorrhagic necrosis and intranuclear inclusion body formation (Lu et al., 2022). The liver becomes enlarged, turns yellowish-brown, and exhibits focal or miliary necrosis or hemorrhage on the surface. Meanwhile, FAdV-4 induces vacuolar degeneration or granular degeneration of cardiac muscle fibers in infected chickens, accompanied by interstitial congestion, hemorrhage, and mononuclear cell infiltration (Xia, et al., 2017). However, only FAdV-4 shows lesions with pericardial effusion.

However, the pathogenic mechanism leading to pericardial effusion specifically in FAdV-4 infection remains to be explored.

In the present study, we conducted in vivo infection experiments to comparatively investigate the similarities and differences in pathogenicity among various phenotypes of FAdV infections, revealing the infective pathogenic features of FAdVs. This study could offer fresh insights into the epidemiological and pathogenic characteristics of FAdVs, potentially leading to innovative strategies for controlling FAdV infections.

MATERIALS AND METHODS

Ethics Statement

This research received approval from the Animal Care and Use Committee of Shandong Agricultural University (permit number: SDAUA-2015-003) and was conducted following the "Guidelines for Experimental Animals" issued by the Ministry of Science and Technology (Beijing, China). All chickens received humane care in accordance with established procedures.

Virus

The FAdV-4 strain and FAdV-8b strain utilized in this study was isolated from a broiler chicken liver sample during a recent outbreak of HPS in China (Niu et al., 2016b), and sequencing results showed that the hexon gene shared the highest nucleotide similarities with the hexon gene of group 1 serotype 4 (FAdV-4) and FAdV-8b. The virus was propagated in the LMH chicken hepatocellular carcinoma cell line (ATCC CRL-2117) and were cultured in DMEM/F-12 (Gibco) supplemented with 10% fetal bovine serum (FBS) and antibiotics (penicillin and streptomycin) at 37°C with 5% CO2. After 60 h of incubation, both supernatants and cells were collected, and the median tissue culture infectious dose (TCID50) of FAdV-4 and FAdV-8b in LMH cells was determined. Chicks were inoculated with a viral titer of 107 tissue culture infective doses per 0.2 mL.

Animal Trial

Ninety 6-day-old SPF chicks were randomly divided into 3 groups (FAdV-4 infection group, FAdV-8b infection group, and control group) and housed in negative pressure isolators with access to water and feed. After one day of feeding, chicks in the infection groups were subjected to subcutaneous injection challenge tests at the neck with an infectious dose of 0.2 mL containing 10^7 TCID50 of virus per chick. Weight and clinical symptom data were recorded from 12 randomly selected chicks in each group. To comprehensively compare FAdV-4 and FAdV-8b, considering their clinical pathogenic characteristics, the infection and control groups were studied on days 1, 3, 5, 7, 9, 11, and 14 post-infection. Three chicks were randomly selected from each group for blood collection via the wing vein and subsequent necropsy.

Histological and Immunohistochemistry Analyses and Measuring the Weight of Organs

After euthanasia, the body weights of all SPF birds from the 3 groups were measured and recorded individually. The heart, lungs, spleen, and kidneys from each bird were then collected and weighed, and their relative weights to the whole body were calculated using the formula: organ weight (g) = organ weight/body weight (g) × 1,000. Additionally, sample tissues were collected to analyze the ratio of wet to dry weight. These sample tissues were further preserved in 4% neutral-buffered formalin, embedded in paraffin blocks, and sliced into 4 μm sections. These sections were stained with hematoxylin and eosin and examined under a light microscope to identify any lesions associated with FAdV-4 and FAdV-8b infection. Immunocomplexes of FAdV-4 and FAdV-8b in liver and heart sections were detected as described previously (Niu, et al., 2017).

Determining the Viral Loads of Tissue and Cell Samples

Total DNA was extracted from serum with Tris-phenol (Solarbio) according to manufacturer's instructions. The absolute FAdV genomic load in serum was quantified using the following primers specific for 52k: the FAdV forward primer, 5′-ATGGCKCAGATGGCYAAGG-3′, and the FAdV reverse primer, 5′-AGCGCCTGGGTCAAACCGA-3′. qPCR was performed as described by Niu et al (Niu et al., 2017).

Statistical Analysis

Data analysis was conducted using SPSS 25 software. Statistical significance was determined at p < 0.05 (*) and p < 0.01 (**). An independent T-test was used to compare differences between groups. The values are shown as the mean ± standard deviation of triplicate analyses from 3 independent experiments. Charts were created using GraphPad Prism 6 software.

RESULTS

FAdV-4 and FAdV-8b Show Typical Clinical Symptoms After Infecting SPF Chickens

By observing the clinical signs of the chickens, it can be found that chickens in the FAdV-4 infected group began to exhibit mild depression on the 2nd day after infection, and on the 4th day, some chickens collapsed and died suddenly. By the 11th day, the chickens that survived were back to their normal levels. (Figure 1A). However, chickens in the FAdV-8b infected group began to show significant mental depression on the 3rd day after infection, and this process continued until the 7th day. None of the chickens died during the entire infection process (Figure 1B). By analyzing the death data, chickens began to die on the 3rd to 6th day after FAdV-4 infection, and the final survival rate was only 40%. This rate was significantly lower than that of the FAdV-8b infected group and the control group (P < 0.05) (Figure 1C). The body weights of the FAdV-4 and FAdV-8b infected groups were significantly lower than those of the control group within 11 to 21 d after infection by analyzing the body weight data. (Figure 1D).

Figure 1.

Figure 1

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The clinical indices after inoculation with fowl adenovirus serotype 4 and 8b. (A) Depression in the FAdV-4 infection group; (B) Mental disability caused by FAdV-8b; (C) Survival rate; (D) Trend of body weight change. (Red * indicate the difference between FAdV-8b and the control group, while green * indicate the difference between FAdV-4 and the control group).

The SPF Chickens Exhibit Typical Necropsy Lesions After Being Infected With the Virus

Following infection with FAdV-4 in chickens, a pale yellow fluid or gelatinous material was observed within the pericardial space, volumes ranging from 0.5 to 25 mL. The cardiac muscle presented with sponginess and congestion. The group infected with FAdV-8b demonstrated cardiac necropsy findings similar to those of the control group (Figure 2A). In the cohort afflicted with FAdV-4, hepatic enlargement and degeneration were noted, characterized by a pale or khaki hue and the presence of white necrotic areas or pinpoint hemorrhages. Chickens infected with FAdV-8b exhibited hepatic lesions akin to the FAdV-4 group, albeit with enhanced hepatic hypertrophy and modified texture (Figure 2B). Pulmonary assessment of the FAdV-4 infected ensemble revealed congestion, edema, and hemorrhage, whereas the lungs of the FAdV-8b group displayed no conspicuous pathology (Figure 2C). In the FAdV-4 group, splenic congestion and hypertrophy were observed, in contrast to the FAdV-8b group, which exhibited only splenic enlargement without congestion (Figure 2D). Renal necropsy findings in both FAdV-4 and FAdV-8b infected groups were largely congruent, marked by congestion, hypertrophy, and pallor. However, the FAdV-4 group showed more pronounced renal enlargement and focal changes attributable to urate deposits (Figure 2E).

Figure 2.

Figure 2

Figure 2

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Anatomical lesion. (A) heart; (B) liver; (C) lung; (D) spleen; (E) kidney of FAdV-4 infected chickens exhibited enlargement and showed increased levels of edema and congestion when compared to the organs of the FAdV-8b and control chickens.

FAdV-4 Caused Edema in Other Organs

In the tests conducted on chickens infected with FAdV-4 and FAdV-8b, it was observed that FAdV-4 induced edema in various organs. To accurately quantify and compare the extent of organ edema, the wet weight to dry weight ratio was utilized as a measure. Notably, significant edema in the lungs of the FAdV-4 infected group was evident from the 3rd day postchallenge, persisting until the 9th day post-infection (Figure 3A), displaying substantial disparities compared to both the FAdV-8b infected group and the control group. Kidneys, heart, and spleen exhibited signs of edema from the 5th day postinfection (Figure 3B-D), whereas the FAdV-8b infected group mirrored the control group, showing no significant differences in the wet weight/dry weight ratio of these organs. Consequently, it can be preliminarily inferred that FAdV-8b does not induce organ edema in chickens.

Figure 3.

Figure 3

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Edema of organs. (A) lung; (B) kidney; (C) spleen; (D) heart (Green* indicates the difference between FAdV-4 and the control group, and black* indicates the difference between FAdV-4 and FAdV-8b).

After Infection With the Virus, Histopathological Manifestations of the Liver and Heart in Chickens are Observed

Hepatocytes of chickens infected with FAdV-4 manifested granular and vacuolar degeneration, with focal necrosis being prominent. Histological examination of liver tissue revealed infiltration of a significant number of lymphocytes and macrophages, accompanied by the presence of eosinophilic or basophilic inclusion bodies within hepatic nuclei (Figure 4A). Similar hepatic lesions were evident in chickens infected with FAdV-8b (Figure 4B). Immunohistochemical staining demonstrated the presence of positive viral particles within infected hepatocytes of both FAdV-4 and FAdV-8b (Figures 4D and 4E). FAdV-4 infection led to degeneration or vesicular degeneration of myocardial fiber particles, accompanied by intramyocardial hemorrhage or blood accumulation (Figure 4G). Conversely, no significant pathological changes were observed in the hearts of chickens infected with FAdV-8b or in the control group (Figures 4H and 4I). Additionally, immunohistochemical staining failed to detect virus particles in heart tissue (Figures 4G and 4K).

Figure 4.

Figure 4

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HE staining and immunohistochemistry of liver and heart (A, B, and C) liver (HE × 200); (D, E, and F) liver (IHC × 200);G, H, I: heart (HE × 200); (J, K, and L) heart (IHC × 200).

Histopathological Changes in Other Organs

FAdV-4 induced severe congestion of capillaries and veins in the lungs, accompanied by exudative serous fluids in the lung chambers and interlobular stroma (Figure 5A). Additionally, mild hemorrhage was observed, with no obvious lesions in the lungs of chickens infected with FAdV-8b or in the control group (Figures 5B and 5C). Following infection with FAdV-4 and FAdV-8b, the renal interstitium exhibited congestion or hemorrhage, along with degeneration and necrosis of renal tubular epithelial cells and lymphocytic infiltration (Figure 5D). The pancreas displayed severe degeneration and necrosis (Figure 5G).

Figure 5.

Figure 5

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Pathological manifestations of lung, kidney, and pancreas (A, B, and C) lung (HE × 200); (D, E, and F) kidney (HE × 200); (G, H, and I) pancreas (HE × 200).

The mucosal epithelial cells of the duodenum exhibited degeneration, necrosis, and subsequent shedding, accompanied by congestion and bleeding in the lamina propria of the mucosa (Figures 6A and 6B). Vascular congestion was observed in brain tissue, with occasional mild viral encephalitis lesions, such as phagocytic phenomena (Figures 6D and 6E). Overall, the pathology of the liver, kidney, pancreas, bursa, thymus, spleen, duodenum, and brain tissue in both the FAdV-8b infected group and the FAdV-4 infected group showed substantial consistency.

Figure 6.

Figure 6

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Duodenal and cerebral pathology (A, B) duodenum (HE×200); (C) duodenum (HE×100); (D, E, and F) brain (HE × 400).

Proliferation of 2 Viruses in Liver and LMH Cells of Infected Chickens

After FAdV-4 and FAdV-8b were infected with SPF chickens respectively, as time goes on, the virus was detected in the liver, and FAdV-4 had better replicate effect than FAdV-8b. The 2 viruses showed significant differences 3 to 7 d after infected, and reaching the peak of replication on the 5th day after challenged (Figure 7A).

Figure 7.

Figure 7

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Virus proliferation (A) FAdV-4 and FAdV-8b can replicate in the liver; (B) 2 viruses in LMH proliferation.

FAdV-4 and FAdV-8b were inoculated into LMH cells, respectively. It was observed by q-PCR that both viruses proliferate well in LMH cells. The 2 viruses were infected with LMH cells at 6, 12, 24, 36, 48, and 60 h, respectively, and the proliferated peak was reached at 48 h. the virus copy number of FAdV-4 was higher than FAdV-8b (Figure 7B).

DISCUSSION

Most serotype I of FAdVs infect chickens usually causing punctiform hemorrhage and necrosis in the liver. HPS caused by FAV-4 infection also results in the accumulation of water or gelatinous fluid in the pericardial cavity. The sudden outbreak of the disease in our country in 2015 undoubtedly brought huge economic losses to the poultry industry. However, most of the current research hotspots on the virus are focused on epidemiological investigations, pathological studies, establishment of diagnostic methods, and prevention (Niu, et al., 2016a), with few studies on its pathogenic mechanisms. Epidemiological survey data shows that the main epidemic strains in China are currently FAV-4 and FAdV-8b. Both serotypes of FAdVs cause hemorrhagic necrosis and intranuclear inclusions in the liver, while only FAdV-4 infection leads to pericardial effusion.

This study conducted infection experiments in chicks using FAdV-4 strain SDLC3/28 and FAdV-8b strain ZGHB4/10. It was found that both viruses peaked in symptoms between d 3 and 7 postinfection. However, chicks infected with FAdV-4 showed more pronounced depression compared to those infected with FAdV-8b. Both viruses resulted in decreased feed intake and significant weight loss. Notably, FAdV-4 caused a mortality rate of 58% in the infected chickens, whereas no deaths occurred in the FAdV-8b infected group. Besides causing liver degeneration and necrosis, FAdV-4 also induced specific pericardial effusion, while FAdV-8b primarily caused similar liver lesions. Clinical statistics suggest that FAdV-I can lead to mortality rates ranging from 10% to 80%, indicating that the FAdV-8b strain used in this experiment is likely to be low-pathogenic. Moreover, investigations have shown that different serotypes, and even different isolates within the same serotype, can exhibit varying pathogenic phenotypes in chickens (Zhang, et al., 2024). Additionally, FAdV-4 infection can lead to varying degrees of edema in the lungs, kidneys, heart, and spleen, with lung edema being the most prominent. This suggests significant differences in the pathogenic characteristics of the 2 serotypes regarding the occurrence of edematous lesions. This difference may be attributed to varying direct pathogenic effects on above organs by different viruses, or differences in the inflammatory response induced by different viruses, leading to variations in the levels of vascular active substances such as leukotrienes (LT) and serotonin (5-HT), or vascular adhesion factors, resulting in varying degrees of increased vascular permeability and microcirculation dysfunction, thus causing different observable lesions in the heart and edematous organs by the 2 isolates (Mehmood et al., 2022; Zhang, et al., 2023). Common findings between the 2 serotypes include mottled kidneys, pinpoint hemorrhage at the edge of the pancreas, mucosal necrosis primarily in the duodenum, and congestion in brain tissue.

Fowl adenovirus, as a hepatotropic virus, can cause severe damage to the tissue structure and function of the liver (Lai et al., 2024). After infection with the 2 viruses, pathological observations of the liver show that both can cause liver bleeding, hepatocyte degeneration and necrosis, and intranuclear inclusions to varying degrees. However, statistical analysis of inclusion bodies in group 2 chickens infected with the 2 strains on the 5th day indicates that there are fewer inclusion bodies in the FAdV-8b infected group compared to the FAdV-4 infected group. This may be due to milder liver cell lesions in the selected slice areas, or differences in the timing of inclusion body formation by the 2 viruses. Immunohistochemical staining reveals positive complexes in the liver for both viruses, with no significant difference in quantity, consistent with Zhao J et al.'s findings (Zhao et al., 2015). The FAdV-4 isolate can also cause significant pathological changes in the heart, including thickening of the interstitium, degeneration of myocardial fibers, and capillary congestion and edema. FAdV-8b, on the other hand, apart from causing minor congestion in the aforementioned tissues, does not show significant pathological changes. However, there are no positive granules in the heart tissue after immunohistochemical staining for either virus post-infection, providing theoretical evidence for further investigation into FAdV-4-induced pericardial effusion and edema in other organs. Existing studies suggest that the direct cause of mortality in chickens infected with FAdV-4 is heart failure. Research has shown that when there is a large amount of fluid in the pericardial cavity, the pressure on the pericardium is higher than the diastolic pressure of the ventricle, leading to pericardial infarction and subsequent heart failure. To perform a proper comparison. We'd better perform Scores, but we haven't found a reasonable score criterion yet. Whether this functional impairment is a result of the virus's direct effect on the myocardium or impaired circulatory function requires further experimental verification. Both viruses can also cause degeneration and necrosis of renal tubular epithelial cells, pancreatic cell degeneration, duodenal degeneration and necrosis, and mild neuronal phagocytosis in the brain, which may be related to the observed clinical symptoms of depression and coma.

Over the years, we've been closely monitoring infections of avian adenovirus and have seen numerous cases of inclusion body hepatitis (IBH). We've isolated and purified 3 strains of FAdV-8b. When the hydropericardium syndrome (HPS) outbreak occurred, we promptly conducted epidemiological tracking of the disease. By 2017, we had diagnosed 125 cases and isolated 68 strains of the virus (Niu, et al., 2016b). Research findings indicated that all HPS cases in China were caused by FAdV-4 infection. This differs from the serotypes of avian adenovirus prevalent in China before 2014 when IBH, primarily caused by FAdV-8b, FAdV-7, and FAdV-11 infections, was dominant (Changjing, et al., 2016).FAdV-4 has become a hot topic in veterinary research. Most of the focus has been on epidemiological surveys (Ma, et al., 2022), pathogen studies (Li, et al., 2018), pathological observations, establishing disease detection and diagnostic methods, vaccine development, and diagnosis and prevention (Li, et al., 2017). FAdV-8b, as an early prevalent pathogen, shows hemorrhagic necrosis and intranuclear inclusion body formation in the livers of chickens infected with both FAdV-8b and FAdV-4. The liver lesions of both have similar characteristics, but only FAdV-4 presents pericardial effusion. The pathogenic mechanism behind this phenomenon requires further research and discussion.

DISCLOSURES

The authors declare no conflicts of interest.

Acknowledgments

This study was supported by the Basic and Applied Basic Research Foundation of Guangdong Province [2023A1515110264] and Funds of Shandong “Double Tops” Program.

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