Epidemiological investigation of equine herpesvirus in large-scale donkey farms in Liaocheng area and its effect on immunity and antioxidant capacity

doi:10.21203/rs.3.rs-3420287/v1

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Epidemiological investigation of equine herpesvirus in large-scale donkey farms in Liaocheng area and its effect on immunity and antioxidant capacity

https://doi.org/10.21203/rs.3.rs-3420287/v1

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Background

Equine herpesvirus (EHV) may cause respiratory, reproductive and neurological diseases in equine animals, including donkeys, of which EHV type 1 (EHV-1) and EHV-4 are the main pathogens. To investigate the prevalence of EHV in donkeys in the Liaocheng area (an important donkey breeding areas in China), and the effect of EHV infection on immunity and antioxidant capacity in donkeys.the epidemiological investigation of EHV was proceed by detected the EHV-1 and EHV-4 in 230 donkey serum collected from 27 large-scale donkey farms, and the serum samples of 10 normal (without EHV-infected) and 10 EHV-infected donkeys with similar age were used to detect the immune and antioxidant related indexs.

Result

The results showed that 62.96% (17/27) of farms were positive for EHV, and the total positive rate of EHV was 12.61% (29/230) with 7.82% (18/230) for EHV-1, 9.57% (22/230) for EHV-4 .Conclusion: Moreover, The differences of EHV infection among different regions in Liaocheng were not significant (P > 0.05), but the highest positive rate was found in Dong'e County (21.28%,10/47). The highest positive rate of EHV-1/4 was 21.18% (18/85) in adult donkeys aged 1–4 years, which was significantly different from other age groups (P < 0.05). The difference in seasons was not significant (P > 0.05), but the highest positive rate was 19.61% (10/51) in winter. Furthermore, EHV infection increased the levels of the immune related indexs IgA, IgG, IgM and IL-6, inhibited the activities of SOD and T-AOC, and improve the activities of GSH-PX and content of MDA.

Consclusions:

These results indicated that EHV infection is prevalent in large-scale donkey farms in the Liaocheng area, and EHV infection could interfere immune, cause inflammation and oxidative stress, which facilitate early warning of EHV epidemic risk.

Donkey

Equine herpesvirus

Epidemiological investigation

Immunity

Antioxidant capacity

Equine herpesvirus (EHV) infection is an infectious disease of equine animals caused by EHV with pneumonia and pregnant mare miscarriage as the main symptoms[1].EHV is a kind of double-stranded DNA virus that belong to the Herpesvirales and Herpesviridae. Currently, nine species of equine herpesviruses have been isolated from equine animals, of which EHV-1, EHV-3, EHV-4, EHV-6, EHV-8 and EHV-9 belong to the α herpesvirus subfamily, and EHV-2, EHV-5 and EHV-7 belong to the γ herpesvirus subfamily[2]. EHV-1 (known as equine abortion virus) and EHV-4 (known as equine rhinopneumonia virus) are the two most severe forms of the virus and the main pathogens of EHV infections, and EHV-1 mainly causes abortion, neurological disease and respiratory disease in pregnant horses, whereas EHV-4 mainly causes respiratory disease[3]. EHV was first discovered and reported in America in 1933 and then subsequently found in 40 countries and regions, including Japan, Turkey and Poland[4, 5]. It has been reported that approximately 80–90% of horses in America were infected with EHV-1 or EHV-4[6]. Similarly, horses in China are frequently infected with EHV. The initial report about EHV in China is that the thoroughbred horses trained in Hong Kong with respiratory disease caused by EHV-1[7]. In 2019, 45 horses in Yili Kazakh Autonomous Region, Xinjiang, China break out EHV-1 infection, which resulted in EHV myeloencephalopathy (EHM) and abortion[8]. Moreover, an abortion storm (43/800) in Yili horses in Zhaosu County (northern Xinjiang, China) was finally confirmed to be caused by EHV-1 infection In 2021[9].

EHV is highly contagious, which can spread rapidly through inhalation of respiratory secretions and direct contact, causing respiratory disease, neurological disease, abortion of pregnant mares and death of foals, resulting in incalculable economic losses. As one main equine animals, donkey has also been reported that infected with EHV-1 and EHV-4[10]. Abdelmoneim A Ali et al. successfully isolated EHV-1 from the fetus of an aborted female donkey in Egypt[11]. Y Yildirim et al. conducted the EHV investigations on donkeys in the northeastern region of Turkey, and found that EHV-1 and EHV-4 had a high positive rate[12]. Pregnant females donkeys infected with EHV-1 and EHV-4 may suffer from abortion. In addition, EHV-1 infection may cause fetal viremia and vascular damage, ultimately leading to brain damage. Although reports of EHV infection in donkeys are limited, EHV is also a great threat to donkey health.

Studies have shown that oxidative stress may be an important physiological feature of herpesvirus infection, which may be associated with increased production of reactive oxygen species, molecular oxidative damage, and changes in non-enzymatic and enzymatic antioxidant defenses[13]. EHV infection can cause innate immune responses in the body.EHV-1 infects the upper respiratory tract in horses, causing a large amount of IgG, IgA, and IgM in horses[14–16]. EHV-1 infected horses increased their susceptibility to EHV-4 and had high levels of immunoglobulin M (IgM), IgG after infection [17]. EHV-1 infects equine endothelial cells, interleukin 6 (IL-6) is consistently increased in infected endothelial cells, and specific pro-inflammatory cytokines in endothelial cells regulated by IL-6 by EHV-1 are identified [18]. Both EHV-1 and EHV-4 can evade host immune responses and establish latent infections, a constant threat to horses and other animals [19].

Recently, donkey breeding industry has developed rapidly in Shandong Province, and the degree of large-scale farming of donkeys in Liaocheng City ranks at the forefront of the province. However, the development of donkey husbandry from traditional natural breeding to large-scale production is hindered by the abortion of pregnant female donkey, diarrhea of donkey foal, and rhinopneumonia infection of donkeys and horses. Up to now, there has been no sero-epidemiological survey of EHV in large-scale donkey farms in China. To clarify the prevalence of EHV in large-scale donkey farms in Liaocheng city, serum samples were collected from large-scale donkey farms in Liaocheng for EHV testing, and risk factors affecting their infection were analyzed to provide reference data for the prevention and control of EHV.

2.1 EHV detection results of donkeys in Liaocheng area

The positive rate of EHV was 62.96% (17/27) of the 27 donkey farms from which serum samples were taken. 7.82% (18/230) were positive for EHV-1, and 9.57% (22/230) positive for EHV-4. Among them,and the total antibody positivity rate was 12.61% (29/230). Among all the positive samples, EHV-1/4 accounted for the lowest proportion of 37.93% (11/29), EHV-1 accounted for 62.07% (18/29), and EHV-4 accounted for the highest proportion of 75.86% (22/29), which indicated that EHV infection existed in donkeys in Liaocheng area, and there was simultaneous infection.

2.2 EHV detection results from different regions of donkeys

As shown in Table 1 and Fig. 1A, there was no significant difference in the antibody positive rate among counties (cities, districts) (P > 0.05). As shown in Fig. 1, the highest EHV-1/4 antibody positivity rate was 10/47 (21.28%) in large-scale donkey farms in Dong'e County, and the positive rate of anti-EHV-1/4 antibody in Shen County was the lowest (8.33%, 1/12). The positive rate of anti-EHV-1/4 antibody in other areas ranged from 9.09–13.95%, and the results indicated that EHV infection in different regions was related to regional location.

Table 1

Statistics of positive rates of EHV-1 and EHV-4 antibodies
Regions	EHV-1	EHV-4	Total
Chiping County	3/43(6.98%)	4/43(9.30%)	6/43(13.95%)
Dong'e County	5/47(10.64%)	7/47(14.89%)	10/47(21.28%)
Gaotang County	1/28(3.57%)	2/28(7.14%)	2/28(7.14%)
Yanggu County	2/31(6.45%)	3/31(9.68%)	3/31(9.68%)
Dongchangfu County	2/28(14.29%)	2/28(14.29%)	3/28(10.71%)
Guan County	2/30(6.67%)	3/30(10.00%)	3/30(10.00%)
Linqing City	1/11(9.09%)	1/11(9.09%)	1/11(9.09%)
Shen County	1/12(8.33%)	1/12(8.33%)	1/12(8.33%)

2.3 EHV detection results in donkeys of different ages

As shown in Table 2 and Fig. 1B, there were significant differences in the prevalence of EHV-1/4 infection among different age groups (P < 0. 05). The highest positive rate of antibody against EHV-1/4 was 21.18% (18/85) in adult donkeys aged 1 ~ 4 years. The positive rate of anti-EHV-1/4 antibody was 11.76% (8/68) in donkeys aged over 4 years. The lowest positive rate of antibody against EHV-1/4 was 3.90% (3/77) in donkey foal aged less than 1 year. The results showed that donkeys aged 1–4 years were more susceptible to EHV infection.

Table 2

EHV-1/4 antibodies at different ages
Age	Detection of the amount	Number of EHV-1/4 positives	EHV-1/4 positive rate
0 < Age ≤ 1	77	3	3.90%
1 < Age ≤ 4	85	18	21.18%
Age > 4	68	8	11.76%

2.4 EHV detection results in different seasons

For the continuous detection of EHV in the four quarters from 2019 to 2020, Table 3 and Fig. 1C shows that the positive rates of EHV in each quarter were 7.41% (4/54), 9.21% (7/76), 16.33% (8/49) and 19.61% (10/51), respectively. There was no significant difference in the positive rate of EHV-1/4 antibody in each quarter (P༞0.05). However, the positive rate in autumn and winter was higher than that in spring and summer. The results showed that donkeys in autumn and winter were more susceptible to EHV infection.

Table 3

EHV antibody results in different seasons
Season	Number of tests	Positive number	Positive rate
Spring	54	4	7.41%
Summer	76	7	9.21%
Autumn	49	8	16.33%
Winter	51	10	19.61%

2.5 Determination results of oxidation and antioxidant markers

It can be seen that the levels of T-AOC and SOD in the EHV1/4 group were lower than those in the Con group (Fig. 2A and 2B), and the level of GSH-PX and the content of MDA were higher than those in the Con group (P < 0.05) (Fig. 2C and 2E), and the level of CAT were not significantly different between Con and EHV1/4 group (P ≥ 0.05) (Fig. 2D). These results indicated that EHV infection could disturb the activity of antioxidant enzymes, and induce oxidative stress in donkeys.

2.6 Assay results of immune function markers

IgA、IgG、IgM、IL-6 and IL-10 are important markers of the body's immunity. It can be seen from Fig. 3 that the levels of IgA(p < 0.0001), IgG(p < 0.01), IgM (p < 0.001) and IL-6 (p < 0.0001) were higher than those in the control group. It can be seen from Fig. 3E that EHV infection has no significant impact on the content of IL-10. These results indicated that EHV infection.

EHV infections, especially EHV1 and EHV4 infection, are great threats to the equine health,especially to horses,which obstructed the development of the world horse breeding industry. In 2017, a large-scale EHV-4 respiratory infection occurred with a positive rate of up to 53.94% in a standard stud farm in northern Germany[20]. In 2021, an outbreak of EHV-1 was reported in Spain which caused infections and deaths to and affected horses in more than 10 countries[21]. However, the EHV infection situation and its effect in donkeys are unclear. In this study, it was found that EHV infection in donkeys was found to be widespread in large-scale donkey farms of Liaocheng area, and EHV infection activated immune function and disturbed antioxidant enzymes, inducing inflammation and oxidative stress in donkeys.

Donkeys could be infected with EHV through having close contact with horses[22]. Presently, EHV-1, EHV-4 and EHV-8 were successfully isolated from donkeys. Wang first isolated EHV-8 from a 2-year-old donkey with neurological disease in China, which revealed that the donkey population in China experienced the risk of EHV infection[23]. However, there are few reports about the prevalence of EHV in donkey farms in China and around the world. In this study, the serological survey of EHV-1 and EHV-4 was carried out in 27 large-scale donkey farms in Liaocheng, Shandong Province. It was found that 17 out of 27 donkey farms were detected positive for EHV, with a positive rate of up to 62.96%. The serological survey revealed that the total positive rate of EHV-1/4 in large-scale donkey herds in Liaocheng, Shandong Province was 12.61% (29/230), the positive rates of EHV-1 and EHV-4 were 7.82%, and 9.57%,respectively,which was lower than the 51.85% positive rate of EHV-1 and 64.20% positive rate of EHV-4 in donkey-herds in Kars and Ardahan provinces of northern Turkey investigated by Yildirim in 2014[12]. Moreover, EHV-4 posiitive accounted for the highest proportion of 75.86% (22/29), among all EHV-postive donkey,which was similar to the EHV survey in horse herds,proceed by Ruiz-Saenz et al. (2007–2008) in Colombia and Ataseven (2010) in Turkey[24, 25].

Further analysis revealed that EHV infection had age characteristics in large-scale donkey farms in Liaocheng, and 1-4-year old donkeys were more likely to be infected.In this study, the highest seropositive rate of adult donkey aged 1–4 years was 21.18%, which was similar to the report of Selvaraj Pavulraj et al., which may be related to the disappearance of maternal antibodies[20].The positive rate of EHV in autumn and winter was higher than in spring and summer. Among all counties of Liaocheng, Dong'e County was the area with highest positivity, which might be related to the high breeding density of donkeys in Dong'e County, which accounted for more than 50% of the total number of donkey-stock in Liaocheng. In addition, Foote et al. found that Equine animals infected with EHV could further spread during transport and under stress[26]. Donkeys in Liaocheng farms are mainly imported from Balinzuo Banner of Chifeng City in Inner Mongolia, Arukorqin Banner of Chifeng City in Inner Mongolia, and Jianping County of Fuxin City in Liaoning Province, and are transported by land to various donkey farms in Liaocheng. Stress response caused by long distance transportation and temperature change may easily lead to EHV infection and transmission.

The oxidation and antioxidant markers of positive samples were similar to those of Costantini D et al [27]. in 2018 for EHV infection in equine animals, with GSH-PX levels in the same experimental group being higher in the horse group than in the control group, and SOD levels in the Captive khulan and Captive plains zebra groups being lower than those in the control group. It was shown that EHV infection reduced SOD levels and total antioxidant capacity in donkeys. However, the increase in MDA levels indicated that EHV infection enhanced peroxidative damage to donkey tissue, promoting damage to cells. The results of IgM detection were the same as those of Chong YC and other EHV infection results in horses, and the IgM in the experimental group was higher than that in the control group, indicating that EHV infection caused the immune response to increase IgM levels and enhance antiviral effects. Foote had higher positive groups than control groups in equine antibody detection for EHV-1 infection, and the same results as this test, EHV infection with donkeys increased the levels of IgA and IgG, indicating that EHV infection caused an immune response, and the host improved its resistance to the virus through a large amount of immune antibody secretion[28]. In 2022, Hu Leyufound by establishing an EHV-8 mouse infection model that the level of IL-6 in the lungs of mice after EHV-8 infection was the same as the increase in serum IL-6 in EHV donkey infection in this trial, indicating that EHV infection caused an inflammatory response and improved the expression of pro-inflammatory factors[29].

The results of this epidemiological survey indicate that EHV (EHV-1 and EHV-4) were prevalent in the large-scale donkey farms in Liaocheng area and and EHV infection could cause oxidative stress and inflammatory response in donkeys, which is a potential threat to donkeys health. The EHV infection in donkeys,should arouse wide concern. Vaccination can effectively prevent EHV infection, moreover it is recommended to do hard work on breeding and management in the cold season (autumn and winter). In addition, self-propagation should be advocated in large-scale donkey farms, and the hidden transmission routes should be cut off. Isolation, observation and quarantine should be done if it is really necessary to introduce a fine variety. This study revealed the epidemic characteristics of EHV in large-scale donkey farms in Liaocheng area, facilitate the prevention and control of EHV in Liaocheng, and promotes the healthy development of donkey industry.

5.1 Sample collection

230 blood samples were randomly collected among 1156 non-EHV-immunized donkeys (27 donkey farms) in Liaocheng city and its surrounding 8 counties and cities from spring to winner through jugular vein and centrifuged at 2000 rpm/min for 10 min to collect serum. The serum samples were frozen at -80℃ and stored for further use.

5.2 Detection of EHV-1/4

The enzyme-linked immunosorbent assay (ELISA) was used to detect EHV1/4 antibodies in 230 serum samples using EHV1/EHV4-Ab antibody assay kit (SVANOVIR®), and the specific procedure was performed according to the kit instructions. The results were calculated according to optical density (OD) value at 450 nm of the serum samples.

5.3 Epidemiological investigation

Based on the test results, an investigation was conducted on the epidemiology of EHV1/4 from three aspects: region, age, and season.

5.4 Determination of oxidation and antioxidant markers

According to the kit instructions, the serum samples of 10 normal(named as Con group)and EHV1/4-positive༈named as EHV1/4 group༉donkeys (1–4 years old) were used to measure the activity of total antioxidant capacity (T-AOC), superoxide dismutase (SOD), glutathione peroxidase (GSH-PX) and catalase (CAT), and the content of malondialdehyde (MDA) by biochemical kits (Nanjing Jiancheng Biological Research Institute, China). The results were calculated according to OD value at 520 nm (T-AOC), 550 nm (SOD), 412nm (GSH-PX), 405 nm (CAT) and 532 nm (MDA) of the serum samples.

5.5 Determination of immune function markers

The serum samples of Con group and EHV1/4 group were used to measure the concentrations of IgM, IgA, IgG, IL-6 and IL-10 by ELISA kit (Shanghai Langton Biotechnology Co., Ltd., China.) according to the kit instructions. The concentrations were calculated based on the OD value at 450 nm.

5.6 Data Analysis

SPSS 17.0 was used for statistical analysis of the trial data. Significant differences between different regions, ages and seasons of EHV-1/4 were assessed using chi-square (χ²). GraphPad Prism 8 software was used for figures. The significant difference between Con group and EHV1/4 group was analyzed by T-test. P values < 0.05 were considered significant differences and P values ≥ 0.05 were considered no significant differences.

EHV

Equine herpesvirus

EHV-1

Equine herpesvirus type 1

EHV-4

Equine herpesvirus type 4

ELISA

Enzyme-linked immunosorbent assay

T-AOC

Total antioxidant capacity

GSH-PX

Glutathione peroxidase

SOD

Superoxide dismutase

CAT

catalase

MDA

Malondialdehyde

IgA

Immunoglobulin A

IgG

Immunoglobulin G

IgM

Immunoglobulin M

IL-6

Interleukin- 6

IL-10

Interleukin-10

Acknowledgements

We are very grateful to the donkey farm owners for their support of the trial.

Ethics approval and consent to participate

All procedures are approved by the Animal Welfare and Ethics Committee of the Institute of Animal Science, Liaocheng University (Protocol No. LC2019-05).All methods are carried out in accordance with the relevant guidelines and regulations of the Animal Welfare and Ethics Committee of the Institute of Animal Science, Liaocheng University.

Consent for publication

Not applicable.

Vailability of data and materials

The data supporting the conclusions of this case report are included in thisarticle. All data sets can be requested from correspondence with the authors.

Conflicts of Interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Funding

This research was supported by Shandong Provincial Donkey Industry Technology System Fund (SDAIT-27-11) and Liaocheng University Science and Technology Research Project (318011701).

Authors' contributions

YJ conducted experiments, analyzed data, and wrote a manuscript.QLand DX designed the study, modified and oversaw the study. XZ participated in this experimental research and provided valuable comments.All authors read and approved the final manuscript.

Author details

¹ College of Agricultural Science and Engineering, Liaocheng University, Liaochen, 252000, China

²Liaocheng Research Institute of Donkey High-Efficiency Breeding and Ecological Feeding, Liaocheng University, Liaocheng, 252000, China

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No competing interests reported.

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Epidemiological investigation of equine herpesvirus in large-scale donkey farms in Liaocheng area and its effect on immunity and antioxidant capacity

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Abstract

Background

Result

Consclusions:

Figures

1 Background

2 Results

2.1 EHV detection results of donkeys in Liaocheng area

2.2 EHV detection results from different regions of donkeys

2.3 EHV detection results in donkeys of different ages

2.4 EHV detection results in different seasons

2.5 Determination results of oxidation and antioxidant markers

2.6 Assay results of immune function markers

3 Discussion

4 Conclusion

5 Methods

5.1 Sample collection

5.2 Detection of EHV-1/4

5.3 Epidemiological investigation

5.4 Determination of oxidation and antioxidant markers

5.5 Determination of immune function markers

5.6 Data Analysis

Abbreviations

Declarations

References

Additional Declarations

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