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Korean J. Vet. Serv. 2022; 45(2): 71-77

Published online June 30, 2022

https://doi.org/10.7853/kjvs.2022.45.2.71

© The Korean Socitety of Veterinary Service

Clinical characterization of 3-month-old pigs infected with African swine fever virus from Vietnam

Sang-Ik Oh 1*, Vuong Nghia Bui 2, Duy Tung Dao 2, Ngoc Anh Bui 2, Seung-Won Yi 1, Eunju Kim 1, Han Gyu Lee 1, Eun-Yeong Bok 1, S.H.M.P Wimalasena 1, Young-Hun Jung 1, Tai-Young Hur 1, Hu Suk Lee 3*

1Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration, Wanju 55365, Korea
2Virology Department, National Institute of Veterinary Research, Hanoi, Vietnam
3International Livestock Research Institute (ILRI), Hanoi, Vietnam

Correspondence to : Sang-Ik Oh
E-mail: ohsangik@korea.kr
https://orcid.org/0000-0003-0877-9170

Hu Suk Lee
E-mail: h.s.lee@cgair.org
https://orcid.org/0000-0002-8731-9836

Received: April 9, 2022; Revised: May 15, 2022; Accepted: May 20, 2022

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0). which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

African swine fever (ASF) is a fatal viral disease in pigs, with a short incubation period and causing immediate death. Few studies exist on the Asian epidemic ASF virus (ASFV) challenge in older pigs, including growing and fattening pigs and sows. We aimed to investigate clinical outcomes, pathomorphological lesions, and viral distribution in organs of 3-month-old growing pigs that were inoculated with the ASFV isolated in Vietnam. The clinical outcomes were recorded daily, and the dead or euthanized pigs immediately underwent necropsy. Viral loads were determined in 10 major organs using quantitative polymerase chain reaction. The average incubation period in growing pigs was more delayed (5.2±0.9 dpi) than that in weaned pigs, and the clinical signs were milder in growing pigs than in weaned pigs. The digestive and respiratory clinical signs in growing pigs showed at the end period of life, but these were observed at an early stage of infection in weaned pigs. The pathomorphological features were severe and nonspecific with hemorrhagic lesions in various organs. The viral loads in organs from growing pigs were higher than those from piglets, and the number of viral copies was related to gross lesions in the tonsil and intestine. In the absence of vaccines against ASF, early clinical detection is important for preventing the spread of the virus. Our findings elucidated that the clinical signs and gross lesions in growing pigs differed from those in weaned pigs, which provide valuable information for diagnosis of pigs with suspected ASF infection.

Keywords African swine fever, Clinical sign, Growing pig, Gross lesion, Virus distribution

African swine fever (ASF) is a hemorrhagic viral disease that affects pigs of all ages with serious economic consequences (OIE, 2019). The African swine fever virus (ASFV) is genotyped based on a variable region within the central conserved region (Galindo and Alonso 2017; Sánchez-Vizcaíno et al, 2019). To date, 24 genotypes of ASFV have been reported worldwide, and the virulence of different ASFV isolates may vary within the same genotype (Sánchez-Vizcaíno et al, 2019). Genotype II ASFV was first detected in China in 2018 and has rapidly swept across various Asian countries, including Vietnam, the Philippines, and South Korea (Cho et al, 2021). A recent study revealed a 10-nucleotide insertion (5’-GGAATATATA-3’) in ASFV from China, South Korea, and Vietnam (Kim et al, 2020; Mai et al, 2021). These recent Asian epidemic ASFVs are known to be highly virulent strains, causing mortality in 90∼100% of the cases.

ASF can cause various lesions, from highly lethal to subclinical, depending on the virulence of the virus strains, the dose of viral infection, the breed of the host, and the age of the host (Costard et al, 2009). Our previous study already revealed that the virulence of the ASFV strain from Vietnam was classified as “from peracute to acute form” by analyzing weaned pigs (7∼8 weeks old) with experimental viral infection (Lee et al, 2021). Although previous studies have suggested that host age is an important factor in the clinical course and pathological characteristics of ASF-infected pigs, there have been few studies on ASFV inoculation in growing pigs (aged 3∼6-months) (Post et al, 2017; Wang et al, 2020; Oh et al, 2021; Pikalo et al, 2021). This study aimed to present the pathobiology of 3-month-old growing pigs from Vietnam experimentally infected with ASFV to provide detailed information to farmers, practitioners, and veterinarians. These valuable data could help early recognition of ASF-infected growing pigs based on their clinical features and gross lesions, contributing to the prevention of virus transmission.

Animal experiments in this study were approved by the Animal Ethics Committee of the National Institute of Animal Science in Korea and the rules of the National Institute of Veterinary Research in Vietnam. The study was approved by the Institutional Animal Care and Use Committee of the National Institute of Animal Science, Korea (approval number: NIAS 2020-463).

Six pigs [(Yorkshire×Landrace)×Duroc] aged 3 months were obtained from two commercial farms (Farm A: Pig case #75, #76, and #77; Farm B: #78, #79, and #80) in Vietnam. All pigs were antibody-negative for the major swine pathogens in Vietnam, including ASFV, classical swine fever virus, foot-and-mouth disease virus, porcine reproductive and respiratory syndrome virus, porcine circovirus 2, and Mycoplasma spp. Viral inoculation was conducted in a biosafety facility at the National Institute of Veterinary Research according to Vietnamese government rules. All pigs were intramuscularly inoculated with 1 mL of ASFV from the ASF outbreak farms in northern Vietnam 2019, at a titer of 103.5 HAD50/mL. Clinical signs and rectal temperatures were recorded just before the viral inoculation (0 day-post inoculation [dpi]), and then daily at 10:00 a.m. from the day after viral inoculation. The clinical signs of each ASFV-infected pig were scored according to the method described in our previous study (Lee et al, 2021). Total clinical sign scores >3 were indicative of ASFV infection. The endpoint criteria were based on the proposed two-tier evaluation by Galindo-Cardiel et al (2013).

Necropsy was conducted immediately after death in the ASFV-infected pigs. Gross lesions were investigated in 10 organs, including the submandibular lymph node (LN), mesenteric LN, inguinal LN, spleen, tonsil, lung, heart, liver, kidney, and colon, according to guidelines described in a previous study (Galindo-Cardiel et al, 2013). Viral DNA was extracted from 10 tissue samples using a commercial kit (WizPrep™ Viral DNA/RNA Mini Kit (V2), Wizbiosolutions Inc., Seongnam, Korea) according to the manufacturer’s instructions. DNA was analyzed for the quantification of ASFV DNA using a commercial quantitative polymerase chain reaction (qPCR) kit (VDx® ASFV qPCR kit, Median Diagnostics, Chuncheon, Korea), according to our previous protocol (Lee et al, 2021).

The 3-month-old growing pigs with experimental ASFV infection started to die 7 dpi, and three pigs were euthanized (one pig, 7 dpi; two pigs, 8 dpi). High fever (>40.5℃) emerged from 3 dpi in two pigs (33.3%). Table 1 presents the time-serial clinical sign scores and rectal temperatures for each ASFV-infected pig. The mean rectal temperatures in ASFV infected pigs were gradually increased from 39.9±0.4 (3 dpi) to 40.9±0.2℃ (at 7 dpi). At 4 dpi, two pigs showed clinical signs, with a decrease in the external stimuli response. The average clinical sign scores were also progressively increased from 4 dpi (3.0±1.4) to 7 dpi (6.0±0 scores). These results suggest that ASFV-inoculated growing pigs started to show initial symptoms, mainly behavioral problems, at approximately 4 days after viral infection.

Table 1 . Time-serial changes in clinical sign scores and rectal temperature in 3-month-old African swine fever virus-inoculated growing pigs (n=6)

Pig caseClinical sign scores (rectal temperature, ℃) at

0 dpi1 dpi2 dpi3 dpi4 dpi5 dpi6 dpi7 dpi8 dpi
#750 (38.2)0 (38.3)0 (38.5)1 (40.3)2 (41.0)3 (39.9)4 (41.0)6 (41.0)Euthanized
#760 (38.2)0 (38.4)0 (38.4)1 (39.7)2 (40.0)3 (40.1)5 (41.0)6 (40.4)Dead
#770 (39.1)0 (39.2)0 (39.2)0 (39.3)2 (39.9)3 (41.0)4 (40.9)6 (41.0)Dead
#782 (40.3)1 (39.1)1 (39.4)3 (41.0)5 (40.8)6 (41.0)7 (41.0)Dead-
#791 (38.2)1 (39.1)1 (39.3)2 (40.5)5 (41.0)4 (41.0)7 (42.0)Euthanized-
#802 (39.5)2 (39.9)1 (39.2)1 (39.1)2 (40.0)4 (41.0)6 (41.0)Euthanized-
Average0.80.70.51.33.03.85.56.0-


The major gross lesions in the ASFV-infected 3-month-old growing pigs are presented in Table 2. Enlarged submandibular LNs, hemorrhagic infarction in mesenteric LNs, and hemorrhagic lymphadenitis in inguinal LNs were observed in all pigs inoculated with the virus. Moreover, congestive splenomegaly, hemorrhagic pulmonary edema, and hemorrhagic petechiae were detected in the liver, renal cortex, and colon. Three pigs showed necrotic lesions in the inguinal LNs. Two pigs presented with petechial hemorrhage lesions in the tonsil, and one of them showed petechial lesions in the heart. Representative gross lesions are shown in Fig. 1.

Table 2 . Gross pathologic lesions from the 3-month-old African swine fever virus-inoculated growing pigs (n=6)

Major pathological observationPig case no.

#75#76#77#78#79#80
Skin erythema--
Abdomen exudative fluid---
Enlargement of submandibular LN
Hemorrhagic infarction in mesenteric LN
Hemorrhagic lymphadenitis in inguinal LN--
Congestive splenomegaly
Hyperemia of tonsil----
Hemorrhages in heart-----
Hyperemia of lung
Petechiae in liver
Petechiae in kidney
Petechiae in intestine

LN, lymph node.



Fig. 1.Gross pathological lesions in African swine fever virus-infected 3-month-old growing pigs. (A) Pig case #78. Multifocal petechiae in the ear region (arrows); (B) Pig case #76. Severe cyanosis and ecchymosis in the limb and abdomen (white arrows); (C) Pig case #79. Severe hemorrhagic hydropericardium (white arrow); (D) Pig case #77. Moderate hemorrhagic lymphadenopathy in the mesenteric lymph node (arrow); (E) Pig case #80. Congestive splenomegaly with dark colored and rounded edges; (F) Pig case #75. Multiple areas of lung consolidation and pulmonary edema; (G) Pig case #80. Moderative con­gestion and multifocal petechial in the liver; (H) Pig case #77. Multiple petechial hemorrhages in the renal cortex; (I) Pig case #76. Multiple petechial hemorrhagic lesions on the colon surface (white arrows).

All infected pigs (n=6) were identified as ASFV antigen-positive using qPCR in all the tested organs (Table 3). The highest mean viral copies were detected in the spleen (4.4×106), followed by the liver (3.7×106), inguinal LN (1.7×106), tonsil (1.6×106), submandibular LN (1.7×106), and mesenteric LN tissue (1.3×106 copies/μL). The heart tissue showed the lowest viral loads (9.7×104) among the collected organs, followed by colon (1.2×105), lung (5.0×105), and kidney tissue (5.5×105 copies/μL).

Table 3 . Genomic copy numbers of African swine fever virus in various organs from the 3-month-old viral inoculated growing pigs (n=6)

Pig caseGenome log copy numbers from organ tissue

Lymph nodeSpleenTonsilHeartLungLiverKidneyColon

SubmandibularMesentericInguinal
#754.86.36.26.35.34.85.66.36.25.1
#766.46.56.26.55.05.55.96.95.75.3
#776.35.46.37.14.85.05.56.55.84.7
#785.65.05.66.34.54.05.25.64.43.9
#796.46.46.56.66.74.85.96.65.75.4
#806.45.76.06.66.64.25.86.65.34.7
Average6.05.96.26.55.54.75.66.45.54.9

The clinical outcomes and blood parameters of pigs experimentally infected with a moderately virulent ASFV strain were reportedly related to their age distribution (Post et al, 2017). A recent study suggested that viral replication was age-related in naturally occurring genotype II ASFV from Vietnam, while the pathological lesions did not correlate with the viral loads in each organ (Oh et al, 2021). To date, most experimental Asian epidemic ASFV inoculation studies have been conducted in weaned pigs (Zhao et al, 2019; Sun et al, 2021). Our previous study also revealed the pathogenicity of the Vietnamese ASFV strain and the clinical outcomes of weaned pigs aged 7∼8 weeks (Lee et al, 2021).

All experimental 3-month-old pigs in the present study started to die at 7 dpi, which was later than the onset of lethality in 7∼8-week-old pigs (5 dpi) inoculated with the Vietnamese ASFV strain (Lee et al, 2021). The clinical signs were observed at 5.2±0.9 dpi (average), which was also delayed in the 7∼8-week-old pigs (3.7±1.2 dpi) (Lee et al, 2021). A total of three pigs (50%) began displaying abnormal behavior (e.g., decreased activity, mild–moderate clumsiness) at 4 dpi, and all pigs (100%) presented decreased external stimuli response at 6 dpi. Our previous study revealed that digestive and respiratory problems were the major symptoms in 7∼8-week-old pigs and could be detected at 3∼4 dpi (Lee et al, 2021). However, the 3-month-old growing pigs in this study presented with mild digestive/respiratory symptoms until they died or were euthanized. The clinical sign scores demonstrated that the growing pigs showed milder ASF infection symptoms (scores reached 7) than the weaned piglets (scores reached 15), which was in agreement with the results of previous studies with other ASFV strains (Lee et al, 2021; Oh et al, 2021; Pikalo et al, 2021). However, there is an important limitation in this study to establish general conclusion. The two pigs (#78 and #80) from Farm B showed slight fever before viral inoculation compared to pigs from Farm A, which could imply the possibility of other pathogens’ infection. However, we ruled out infection by major swine disease pathogens, which could have affected this ASFV inoculation experiment. Nevertheless, this study has a limitation because the pigs were not sourced from an identical farm. To exclude such individual differences, further studies are required to conduct experiments on similarly farmed pigs. Nevertheless, the overall results served as a crucial warning against missing the detection of ASF in pig farms due to their long incubation times and mild clinical courses.

A recent study on European ASFV-infected pigs in different age classes suggested that older pigs lacked pathomorphological presentation compared to young piglets (Pikalo et al, 2021). In this study, 3-month-old growing pigs presented severe macroscopic lesions in the spleen and lymph nodes (submandibular, mesenteric, and inguinal) but mild lesions in the lung, liver, kidney, and colon. Most of these pathomorphological findings were milder than those in 7∼8-weeks-old piglets in our previous experiment (data not shown). Hemorrhagic lesions in the tonsil and heart were observed in a few pigs in this study, unlike a previous study on piglets aged 7∼8 weeks (Lee et al, 2021). Moreover, hemorrhagic colons were found in all infected growing pigs in the present study, whereas they were detected in only 30% of piglets (Lee et al, 2021). These results suggest that the veterinarian should carefully diagnose ASF-suspected carcasses via post-mortem examination and consider the pigs’ age. In addition, hemorrhagic infarction in the mesenteric LN and petechial lesions in the intestine implied that older pigs commonly survived until the virus reached the intestinal organs, which was not observed in 7∼8-week-old pigs (Lee et al, 2021). Skin erythema lesions were more frequently observed in this study (n=4, 66.7%) than in the weaned piglets (n=1, 10.0%) from our previous study. Although the number of experimental pigs was too small to establish a definitive conclusion, these pathomorphological findings can assist veterinarians in the diagnosis of ASF infection in growing pigs through field postmortem examination.

All 3-month-old growing pigs showed higher viral loads in 10 major organs than 7∼8-week-old pigs, as reported previously (Lee et al, 2021). The current results showed that the spleen had the highest average viral load among the 10 sampled organs, followed by the liver and lymph nodes. The mean viral copy numbers (log10 6.5) from spleen tissues in this study were higher than those in the previous study on Vietnamese ASFV-infected pigs aged 7∼8 and 4∼5 weeks (average log10 5.5 and 4.3, respectively) (Lee et al, 2021; Goonewardene et al, 2022). The liver showed the second highest viral load in 3-month-old pigs (log10 6.4), which supports the suggestion made in our previous study that liver tissue is a useful sample and should be collected from ASF-suspected carcasses for diagnosis in all age classes (Lee et al, 2021). Viral loads in tonsil tissues from two pigs (pig nos. #79 and #80), which showed hyperemic lesions in post-mortem examination, were relatively higher (log10 6.7 and 6.6, respectively) than those from other pigs (ranged log10 4.5∼5.3). Colon tissue from pigs with exudative fluid in the abdomen (pig nos. #75, #76, and #79) also had higher viral loads (ranged log10 5.1∼5.4) than those from other pigs (log10 3.9∼4.7). Although histopathological analysis was not performed in the current study, these results disagree with those of a recent study, which reported that viral replication is not correlated with pathological lesions (Oh et al, 2021). However, other organs, including the LNs, spleen, heart, lung, liver, and kidney, did not show any correlation with the gross lesions.

In conclusion, 3-month-old growing pigs showed mild clinical signs and delayed onset of death compared to 7∼8-week-old weaned pigs. The onset of clinical signs was also delayed 2∼3 days in growing pigs compared to weaned pigs. The digestive/respiratory clinical signs appeared in weaned pigs at the early stage of infection (3∼4 dpi), according to our previous study (Lee et al, 2021). However, the major and first-observed clinical outcomes in ASFV-infected growing pigs were related to behavior, whereas digestive/respiratory symptoms appeared in the last few days of life. Overall, the clinical signs of ASFV-infected growing pigs were milder and hard to detect in the early period of infection than the weaned pigs. Farmers, practitioners, and veterinarians should carefully monitor the unidentified ASF-infected pigs in farms, considering the pigs’ age classes. The results also confirmed that gross lesions in ASF-infected pigs were highly variable and non-specific. However, lesions in growing pigs were milder than those in weaned pigs. To clarify the characteristics of ASF-infected growing pigs, further studies should be conducted on pigs of other age classes (fattening pigs and sows). Nevertheless, this detailed knowledge of clinical outcomes and pathological changes could help practical veterinarians in the field to promptly identify ASFV-infected growing pigs, which could minimize ASFV transmission.

This work was carried out with the support of the “Cooperative Research Program for Agriculture Science and Technology Development (Project title: Analysis and monitoring of clinical and epidemiological features of African swine fever, Project No. PJ01484301)”, Rural Development Administration, Republic of Korea.

No potential conflict of interest relevant to this article was reported.

  1. Cho KH, Kim HJ, Kim YJ, Kang HE, Lee JB. 2021. Quantitative risk assessment of the African swine fever introduction into the Republic of Korea via legal import of live pigs and pig products. Transbound Emerg Dis 68:385-396.
    Pubmed CrossRef
  2. Costard S, Wieland B, De Glanville W, Jori F, Rowlands R, Vosloo W, Roger F, Dixon LK. 2009. African swine fever: how can global spread be prevented? Philos Trans R Soc Lond B Biol Sci 364:2683-2696.
    Pubmed KoreaMed CrossRef
  3. Galindo-Cardiel I, Ballester M, Solanes D, Nofrarías M, López-Soria S, Argilaguet JM, Lacasta A, Accensi F, Segalés J. 2013. Standardization of pathological investigations in the framework of experimental ASFV infections. Virus Res 173:180-190.
    Pubmed CrossRef
  4. Galindo I and Alonso C. 2017. African swine fever virus: a review. Viruses 9:103.
    Pubmed KoreaMed CrossRef
  5. Goonewardene KB, Onyilagha C, Goolia M, Le VP, Ambagala A. 2022. Superficial inguinal lymph nodes for screening dead pigs for African swine fever. Viruses 14:83.
    Pubmed KoreaMed CrossRef
  6. Kim HJ, Cho KH, Lee SK, Kim DY, Nah JJ, Kim HJ, Kim HJ, Hwang JY, Sohn HJ, Choi JG, Kim YJ. 2020. Outbreak of African swine fever in South Korea, 2019. Transbound Emerg Dis 67:473-475.
    Pubmed CrossRef
  7. Lee HS, Bui VN, Dao DT, Bui NA, Le TD, Kieu MA, Nguyen QH, Tran LH, Roh JH, So KM, Oh SI. 2021. Pathogenicity of an African swine fever virus strain isolated in Vietnam and alternative diagnostic specimens for early detection of viral infection. Porcine Health Manag 7:36.
    Pubmed KoreaMed CrossRef
  8. Mai NTA, Vu XD, Nguyen TTH, Nguyen VT, Trinh TBN, Kim YJ, Kim HJ, Cho KH, Nguyen TL, Bui TTN, Jeong DG, Yoon SW0, Truong T, Ambagala A, Le VP. 2021. Molecular profile of African swine fever virus (ASFV) circulating in Vietnam during 2019-2020 outbreaks. Arch Virol 166:885-890.
    Pubmed CrossRef
  9. Oh T, Do DT, Lai DC, Nguyen TC, Chae C. 2021. Age-related viral load and severity of systemic pathological lesions in acute naturally occurring African swine fever virus genotype II infections. Comp Immunol Microbiol Infect Dis 79:101709.
    Pubmed CrossRef
  10. OIE. 2019. Technical disease card of African Swine Fever. https://www.oie.int/fileadmin/Home/eng/Animal_Health_in_the_World/docs/pdf/Disease_cards/AFRICAN_SWINE_FEVER.pdf. Accessed June 2019
  11. Pikalo J, Schoder ME, Sehl-Ewert J, Breithaupt A, Cay AB, Lhoëst C, van Campe W, Mostin L, Deutschmann P, Roszyk H, Beer M, Tignon M. 2021. Towards efficient early warning: pathobiology of African swine fever virus "Belgium 2018/1" in domestic pigs of different age classes. Animals 11:2602.
    Pubmed KoreaMed CrossRef
  12. Post J, Weesendorp E, Loeffen WL. 2017. Influence of age and dose of African swine fever virus infections on clinical outcome and blood parameters in pigs. Viral Immunol 30:58-69.
    Pubmed CrossRef
  13. Sánchez-Vizcaíno JM, Arias ML. 2019. African swine fever virus. Dis Swine : 443-452.
    Pubmed KoreaMed CrossRef
  14. Sun E, Zhang Z, Wang Z, He X, Zhang X, Wang L, Wang W, Huang L, Xi F, Huangfu H, Tsegay G, Huo H, Sun J, Tian Z, Xia W, Yu X, Li F, Liu R, Guan Y, Bu Z. 2021. Emergence and prevalence of naturally occurring lower virulent African swine fever viruses in domestic pigs in China in 2020. Sci China Life Sci 64:752-765.
    Pubmed CrossRef
  15. Wang S, Zhang J, Zhang Y, Yang J, Wang L, Qi Y, Han X, Zhou X, Miao F, Chen T, Wang Y, Zhang F, Hu R. 2020. Cytokine storm in domestic pigs induced by infection of virulent African swine fever virus. Front Vet Sci 7:601641.
    Pubmed KoreaMed CrossRef
  16. Zhao D, Liu R, Zhang X, Li F, Wang J, Zhang J, Liu X, Wang L, Zhang J, Wu X, Guan Y, Chen W, Wang X, Bu Z. 2019. Replication and virulence in pigs of the first African swine fever virus isolated in China. Emerg Microbes Infect 8:438-447.
    Pubmed KoreaMed CrossRef

Article

Original Article

Korean J. Vet. Serv. 2022; 45(2): 71-77

Published online June 30, 2022 https://doi.org/10.7853/kjvs.2022.45.2.71

Copyright © The Korean Socitety of Veterinary Service.

Clinical characterization of 3-month-old pigs infected with African swine fever virus from Vietnam

Sang-Ik Oh 1*, Vuong Nghia Bui 2, Duy Tung Dao 2, Ngoc Anh Bui 2, Seung-Won Yi 1, Eunju Kim 1, Han Gyu Lee 1, Eun-Yeong Bok 1, S.H.M.P Wimalasena 1, Young-Hun Jung 1, Tai-Young Hur 1, Hu Suk Lee 3*

1Division of Animal Diseases & Health, National Institute of Animal Science, Rural Development Administration, Wanju 55365, Korea
2Virology Department, National Institute of Veterinary Research, Hanoi, Vietnam
3International Livestock Research Institute (ILRI), Hanoi, Vietnam

Correspondence to:Sang-Ik Oh
E-mail: ohsangik@korea.kr
https://orcid.org/0000-0003-0877-9170

Hu Suk Lee
E-mail: h.s.lee@cgair.org
https://orcid.org/0000-0002-8731-9836

Received: April 9, 2022; Revised: May 15, 2022; Accepted: May 20, 2022

This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0). which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

Abstract

African swine fever (ASF) is a fatal viral disease in pigs, with a short incubation period and causing immediate death. Few studies exist on the Asian epidemic ASF virus (ASFV) challenge in older pigs, including growing and fattening pigs and sows. We aimed to investigate clinical outcomes, pathomorphological lesions, and viral distribution in organs of 3-month-old growing pigs that were inoculated with the ASFV isolated in Vietnam. The clinical outcomes were recorded daily, and the dead or euthanized pigs immediately underwent necropsy. Viral loads were determined in 10 major organs using quantitative polymerase chain reaction. The average incubation period in growing pigs was more delayed (5.2±0.9 dpi) than that in weaned pigs, and the clinical signs were milder in growing pigs than in weaned pigs. The digestive and respiratory clinical signs in growing pigs showed at the end period of life, but these were observed at an early stage of infection in weaned pigs. The pathomorphological features were severe and nonspecific with hemorrhagic lesions in various organs. The viral loads in organs from growing pigs were higher than those from piglets, and the number of viral copies was related to gross lesions in the tonsil and intestine. In the absence of vaccines against ASF, early clinical detection is important for preventing the spread of the virus. Our findings elucidated that the clinical signs and gross lesions in growing pigs differed from those in weaned pigs, which provide valuable information for diagnosis of pigs with suspected ASF infection.

Keywords: African swine fever, Clinical sign, Growing pig, Gross lesion, Virus distribution

INTRODUCTION

African swine fever (ASF) is a hemorrhagic viral disease that affects pigs of all ages with serious economic consequences (OIE, 2019). The African swine fever virus (ASFV) is genotyped based on a variable region within the central conserved region (Galindo and Alonso 2017; Sánchez-Vizcaíno et al, 2019). To date, 24 genotypes of ASFV have been reported worldwide, and the virulence of different ASFV isolates may vary within the same genotype (Sánchez-Vizcaíno et al, 2019). Genotype II ASFV was first detected in China in 2018 and has rapidly swept across various Asian countries, including Vietnam, the Philippines, and South Korea (Cho et al, 2021). A recent study revealed a 10-nucleotide insertion (5’-GGAATATATA-3’) in ASFV from China, South Korea, and Vietnam (Kim et al, 2020; Mai et al, 2021). These recent Asian epidemic ASFVs are known to be highly virulent strains, causing mortality in 90∼100% of the cases.

ASF can cause various lesions, from highly lethal to subclinical, depending on the virulence of the virus strains, the dose of viral infection, the breed of the host, and the age of the host (Costard et al, 2009). Our previous study already revealed that the virulence of the ASFV strain from Vietnam was classified as “from peracute to acute form” by analyzing weaned pigs (7∼8 weeks old) with experimental viral infection (Lee et al, 2021). Although previous studies have suggested that host age is an important factor in the clinical course and pathological characteristics of ASF-infected pigs, there have been few studies on ASFV inoculation in growing pigs (aged 3∼6-months) (Post et al, 2017; Wang et al, 2020; Oh et al, 2021; Pikalo et al, 2021). This study aimed to present the pathobiology of 3-month-old growing pigs from Vietnam experimentally infected with ASFV to provide detailed information to farmers, practitioners, and veterinarians. These valuable data could help early recognition of ASF-infected growing pigs based on their clinical features and gross lesions, contributing to the prevention of virus transmission.

MATERIALS AND METHODS

Animal experiments in this study were approved by the Animal Ethics Committee of the National Institute of Animal Science in Korea and the rules of the National Institute of Veterinary Research in Vietnam. The study was approved by the Institutional Animal Care and Use Committee of the National Institute of Animal Science, Korea (approval number: NIAS 2020-463).

Six pigs [(Yorkshire×Landrace)×Duroc] aged 3 months were obtained from two commercial farms (Farm A: Pig case #75, #76, and #77; Farm B: #78, #79, and #80) in Vietnam. All pigs were antibody-negative for the major swine pathogens in Vietnam, including ASFV, classical swine fever virus, foot-and-mouth disease virus, porcine reproductive and respiratory syndrome virus, porcine circovirus 2, and Mycoplasma spp. Viral inoculation was conducted in a biosafety facility at the National Institute of Veterinary Research according to Vietnamese government rules. All pigs were intramuscularly inoculated with 1 mL of ASFV from the ASF outbreak farms in northern Vietnam 2019, at a titer of 103.5 HAD50/mL. Clinical signs and rectal temperatures were recorded just before the viral inoculation (0 day-post inoculation [dpi]), and then daily at 10:00 a.m. from the day after viral inoculation. The clinical signs of each ASFV-infected pig were scored according to the method described in our previous study (Lee et al, 2021). Total clinical sign scores >3 were indicative of ASFV infection. The endpoint criteria were based on the proposed two-tier evaluation by Galindo-Cardiel et al (2013).

Necropsy was conducted immediately after death in the ASFV-infected pigs. Gross lesions were investigated in 10 organs, including the submandibular lymph node (LN), mesenteric LN, inguinal LN, spleen, tonsil, lung, heart, liver, kidney, and colon, according to guidelines described in a previous study (Galindo-Cardiel et al, 2013). Viral DNA was extracted from 10 tissue samples using a commercial kit (WizPrep™ Viral DNA/RNA Mini Kit (V2), Wizbiosolutions Inc., Seongnam, Korea) according to the manufacturer’s instructions. DNA was analyzed for the quantification of ASFV DNA using a commercial quantitative polymerase chain reaction (qPCR) kit (VDx® ASFV qPCR kit, Median Diagnostics, Chuncheon, Korea), according to our previous protocol (Lee et al, 2021).

RESULTS

The 3-month-old growing pigs with experimental ASFV infection started to die 7 dpi, and three pigs were euthanized (one pig, 7 dpi; two pigs, 8 dpi). High fever (>40.5℃) emerged from 3 dpi in two pigs (33.3%). Table 1 presents the time-serial clinical sign scores and rectal temperatures for each ASFV-infected pig. The mean rectal temperatures in ASFV infected pigs were gradually increased from 39.9±0.4 (3 dpi) to 40.9±0.2℃ (at 7 dpi). At 4 dpi, two pigs showed clinical signs, with a decrease in the external stimuli response. The average clinical sign scores were also progressively increased from 4 dpi (3.0±1.4) to 7 dpi (6.0±0 scores). These results suggest that ASFV-inoculated growing pigs started to show initial symptoms, mainly behavioral problems, at approximately 4 days after viral infection.

Table 1 . Time-serial changes in clinical sign scores and rectal temperature in 3-month-old African swine fever virus-inoculated growing pigs (n=6).

Pig caseClinical sign scores (rectal temperature, ℃) at

0 dpi1 dpi2 dpi3 dpi4 dpi5 dpi6 dpi7 dpi8 dpi
#750 (38.2)0 (38.3)0 (38.5)1 (40.3)2 (41.0)3 (39.9)4 (41.0)6 (41.0)Euthanized
#760 (38.2)0 (38.4)0 (38.4)1 (39.7)2 (40.0)3 (40.1)5 (41.0)6 (40.4)Dead
#770 (39.1)0 (39.2)0 (39.2)0 (39.3)2 (39.9)3 (41.0)4 (40.9)6 (41.0)Dead
#782 (40.3)1 (39.1)1 (39.4)3 (41.0)5 (40.8)6 (41.0)7 (41.0)Dead-
#791 (38.2)1 (39.1)1 (39.3)2 (40.5)5 (41.0)4 (41.0)7 (42.0)Euthanized-
#802 (39.5)2 (39.9)1 (39.2)1 (39.1)2 (40.0)4 (41.0)6 (41.0)Euthanized-
Average0.80.70.51.33.03.85.56.0-


The major gross lesions in the ASFV-infected 3-month-old growing pigs are presented in Table 2. Enlarged submandibular LNs, hemorrhagic infarction in mesenteric LNs, and hemorrhagic lymphadenitis in inguinal LNs were observed in all pigs inoculated with the virus. Moreover, congestive splenomegaly, hemorrhagic pulmonary edema, and hemorrhagic petechiae were detected in the liver, renal cortex, and colon. Three pigs showed necrotic lesions in the inguinal LNs. Two pigs presented with petechial hemorrhage lesions in the tonsil, and one of them showed petechial lesions in the heart. Representative gross lesions are shown in Fig. 1.

Table 2 . Gross pathologic lesions from the 3-month-old African swine fever virus-inoculated growing pigs (n=6).

Major pathological observationPig case no.

#75#76#77#78#79#80
Skin erythema--
Abdomen exudative fluid---
Enlargement of submandibular LN
Hemorrhagic infarction in mesenteric LN
Hemorrhagic lymphadenitis in inguinal LN--
Congestive splenomegaly
Hyperemia of tonsil----
Hemorrhages in heart-----
Hyperemia of lung
Petechiae in liver
Petechiae in kidney
Petechiae in intestine

LN, lymph node..



Figure 1. Gross pathological lesions in African swine fever virus-infected 3-month-old growing pigs. (A) Pig case #78. Multifocal petechiae in the ear region (arrows); (B) Pig case #76. Severe cyanosis and ecchymosis in the limb and abdomen (white arrows); (C) Pig case #79. Severe hemorrhagic hydropericardium (white arrow); (D) Pig case #77. Moderate hemorrhagic lymphadenopathy in the mesenteric lymph node (arrow); (E) Pig case #80. Congestive splenomegaly with dark colored and rounded edges; (F) Pig case #75. Multiple areas of lung consolidation and pulmonary edema; (G) Pig case #80. Moderative con­gestion and multifocal petechial in the liver; (H) Pig case #77. Multiple petechial hemorrhages in the renal cortex; (I) Pig case #76. Multiple petechial hemorrhagic lesions on the colon surface (white arrows).

All infected pigs (n=6) were identified as ASFV antigen-positive using qPCR in all the tested organs (Table 3). The highest mean viral copies were detected in the spleen (4.4×106), followed by the liver (3.7×106), inguinal LN (1.7×106), tonsil (1.6×106), submandibular LN (1.7×106), and mesenteric LN tissue (1.3×106 copies/μL). The heart tissue showed the lowest viral loads (9.7×104) among the collected organs, followed by colon (1.2×105), lung (5.0×105), and kidney tissue (5.5×105 copies/μL).

Table 3 . Genomic copy numbers of African swine fever virus in various organs from the 3-month-old viral inoculated growing pigs (n=6).

Pig caseGenome log copy numbers from organ tissue

Lymph nodeSpleenTonsilHeartLungLiverKidneyColon

SubmandibularMesentericInguinal
#754.86.36.26.35.34.85.66.36.25.1
#766.46.56.26.55.05.55.96.95.75.3
#776.35.46.37.14.85.05.56.55.84.7
#785.65.05.66.34.54.05.25.64.43.9
#796.46.46.56.66.74.85.96.65.75.4
#806.45.76.06.66.64.25.86.65.34.7
Average6.05.96.26.55.54.75.66.45.54.9

DISCUSSION

The clinical outcomes and blood parameters of pigs experimentally infected with a moderately virulent ASFV strain were reportedly related to their age distribution (Post et al, 2017). A recent study suggested that viral replication was age-related in naturally occurring genotype II ASFV from Vietnam, while the pathological lesions did not correlate with the viral loads in each organ (Oh et al, 2021). To date, most experimental Asian epidemic ASFV inoculation studies have been conducted in weaned pigs (Zhao et al, 2019; Sun et al, 2021). Our previous study also revealed the pathogenicity of the Vietnamese ASFV strain and the clinical outcomes of weaned pigs aged 7∼8 weeks (Lee et al, 2021).

All experimental 3-month-old pigs in the present study started to die at 7 dpi, which was later than the onset of lethality in 7∼8-week-old pigs (5 dpi) inoculated with the Vietnamese ASFV strain (Lee et al, 2021). The clinical signs were observed at 5.2±0.9 dpi (average), which was also delayed in the 7∼8-week-old pigs (3.7±1.2 dpi) (Lee et al, 2021). A total of three pigs (50%) began displaying abnormal behavior (e.g., decreased activity, mild–moderate clumsiness) at 4 dpi, and all pigs (100%) presented decreased external stimuli response at 6 dpi. Our previous study revealed that digestive and respiratory problems were the major symptoms in 7∼8-week-old pigs and could be detected at 3∼4 dpi (Lee et al, 2021). However, the 3-month-old growing pigs in this study presented with mild digestive/respiratory symptoms until they died or were euthanized. The clinical sign scores demonstrated that the growing pigs showed milder ASF infection symptoms (scores reached 7) than the weaned piglets (scores reached 15), which was in agreement with the results of previous studies with other ASFV strains (Lee et al, 2021; Oh et al, 2021; Pikalo et al, 2021). However, there is an important limitation in this study to establish general conclusion. The two pigs (#78 and #80) from Farm B showed slight fever before viral inoculation compared to pigs from Farm A, which could imply the possibility of other pathogens’ infection. However, we ruled out infection by major swine disease pathogens, which could have affected this ASFV inoculation experiment. Nevertheless, this study has a limitation because the pigs were not sourced from an identical farm. To exclude such individual differences, further studies are required to conduct experiments on similarly farmed pigs. Nevertheless, the overall results served as a crucial warning against missing the detection of ASF in pig farms due to their long incubation times and mild clinical courses.

A recent study on European ASFV-infected pigs in different age classes suggested that older pigs lacked pathomorphological presentation compared to young piglets (Pikalo et al, 2021). In this study, 3-month-old growing pigs presented severe macroscopic lesions in the spleen and lymph nodes (submandibular, mesenteric, and inguinal) but mild lesions in the lung, liver, kidney, and colon. Most of these pathomorphological findings were milder than those in 7∼8-weeks-old piglets in our previous experiment (data not shown). Hemorrhagic lesions in the tonsil and heart were observed in a few pigs in this study, unlike a previous study on piglets aged 7∼8 weeks (Lee et al, 2021). Moreover, hemorrhagic colons were found in all infected growing pigs in the present study, whereas they were detected in only 30% of piglets (Lee et al, 2021). These results suggest that the veterinarian should carefully diagnose ASF-suspected carcasses via post-mortem examination and consider the pigs’ age. In addition, hemorrhagic infarction in the mesenteric LN and petechial lesions in the intestine implied that older pigs commonly survived until the virus reached the intestinal organs, which was not observed in 7∼8-week-old pigs (Lee et al, 2021). Skin erythema lesions were more frequently observed in this study (n=4, 66.7%) than in the weaned piglets (n=1, 10.0%) from our previous study. Although the number of experimental pigs was too small to establish a definitive conclusion, these pathomorphological findings can assist veterinarians in the diagnosis of ASF infection in growing pigs through field postmortem examination.

All 3-month-old growing pigs showed higher viral loads in 10 major organs than 7∼8-week-old pigs, as reported previously (Lee et al, 2021). The current results showed that the spleen had the highest average viral load among the 10 sampled organs, followed by the liver and lymph nodes. The mean viral copy numbers (log10 6.5) from spleen tissues in this study were higher than those in the previous study on Vietnamese ASFV-infected pigs aged 7∼8 and 4∼5 weeks (average log10 5.5 and 4.3, respectively) (Lee et al, 2021; Goonewardene et al, 2022). The liver showed the second highest viral load in 3-month-old pigs (log10 6.4), which supports the suggestion made in our previous study that liver tissue is a useful sample and should be collected from ASF-suspected carcasses for diagnosis in all age classes (Lee et al, 2021). Viral loads in tonsil tissues from two pigs (pig nos. #79 and #80), which showed hyperemic lesions in post-mortem examination, were relatively higher (log10 6.7 and 6.6, respectively) than those from other pigs (ranged log10 4.5∼5.3). Colon tissue from pigs with exudative fluid in the abdomen (pig nos. #75, #76, and #79) also had higher viral loads (ranged log10 5.1∼5.4) than those from other pigs (log10 3.9∼4.7). Although histopathological analysis was not performed in the current study, these results disagree with those of a recent study, which reported that viral replication is not correlated with pathological lesions (Oh et al, 2021). However, other organs, including the LNs, spleen, heart, lung, liver, and kidney, did not show any correlation with the gross lesions.

In conclusion, 3-month-old growing pigs showed mild clinical signs and delayed onset of death compared to 7∼8-week-old weaned pigs. The onset of clinical signs was also delayed 2∼3 days in growing pigs compared to weaned pigs. The digestive/respiratory clinical signs appeared in weaned pigs at the early stage of infection (3∼4 dpi), according to our previous study (Lee et al, 2021). However, the major and first-observed clinical outcomes in ASFV-infected growing pigs were related to behavior, whereas digestive/respiratory symptoms appeared in the last few days of life. Overall, the clinical signs of ASFV-infected growing pigs were milder and hard to detect in the early period of infection than the weaned pigs. Farmers, practitioners, and veterinarians should carefully monitor the unidentified ASF-infected pigs in farms, considering the pigs’ age classes. The results also confirmed that gross lesions in ASF-infected pigs were highly variable and non-specific. However, lesions in growing pigs were milder than those in weaned pigs. To clarify the characteristics of ASF-infected growing pigs, further studies should be conducted on pigs of other age classes (fattening pigs and sows). Nevertheless, this detailed knowledge of clinical outcomes and pathological changes could help practical veterinarians in the field to promptly identify ASFV-infected growing pigs, which could minimize ASFV transmission.

ACKNOWLEDGEMENTS

This work was carried out with the support of the “Cooperative Research Program for Agriculture Science and Technology Development (Project title: Analysis and monitoring of clinical and epidemiological features of African swine fever, Project No. PJ01484301)”, Rural Development Administration, Republic of Korea.

CONFLICT OF INTEREST

No potential conflict of interest relevant to this article was reported.

Fig 1.

Figure 1.Gross pathological lesions in African swine fever virus-infected 3-month-old growing pigs. (A) Pig case #78. Multifocal petechiae in the ear region (arrows); (B) Pig case #76. Severe cyanosis and ecchymosis in the limb and abdomen (white arrows); (C) Pig case #79. Severe hemorrhagic hydropericardium (white arrow); (D) Pig case #77. Moderate hemorrhagic lymphadenopathy in the mesenteric lymph node (arrow); (E) Pig case #80. Congestive splenomegaly with dark colored and rounded edges; (F) Pig case #75. Multiple areas of lung consolidation and pulmonary edema; (G) Pig case #80. Moderative con­gestion and multifocal petechial in the liver; (H) Pig case #77. Multiple petechial hemorrhages in the renal cortex; (I) Pig case #76. Multiple petechial hemorrhagic lesions on the colon surface (white arrows).
Korean Journal of Veterinary Service 2022; 45: 71-77https://doi.org/10.7853/kjvs.2022.45.2.71

Table 1 . Time-serial changes in clinical sign scores and rectal temperature in 3-month-old African swine fever virus-inoculated growing pigs (n=6).

Pig caseClinical sign scores (rectal temperature, ℃) at

0 dpi1 dpi2 dpi3 dpi4 dpi5 dpi6 dpi7 dpi8 dpi
#750 (38.2)0 (38.3)0 (38.5)1 (40.3)2 (41.0)3 (39.9)4 (41.0)6 (41.0)Euthanized
#760 (38.2)0 (38.4)0 (38.4)1 (39.7)2 (40.0)3 (40.1)5 (41.0)6 (40.4)Dead
#770 (39.1)0 (39.2)0 (39.2)0 (39.3)2 (39.9)3 (41.0)4 (40.9)6 (41.0)Dead
#782 (40.3)1 (39.1)1 (39.4)3 (41.0)5 (40.8)6 (41.0)7 (41.0)Dead-
#791 (38.2)1 (39.1)1 (39.3)2 (40.5)5 (41.0)4 (41.0)7 (42.0)Euthanized-
#802 (39.5)2 (39.9)1 (39.2)1 (39.1)2 (40.0)4 (41.0)6 (41.0)Euthanized-
Average0.80.70.51.33.03.85.56.0-

Table 2 . Gross pathologic lesions from the 3-month-old African swine fever virus-inoculated growing pigs (n=6).

Major pathological observationPig case no.

#75#76#77#78#79#80
Skin erythema--
Abdomen exudative fluid---
Enlargement of submandibular LN
Hemorrhagic infarction in mesenteric LN
Hemorrhagic lymphadenitis in inguinal LN--
Congestive splenomegaly
Hyperemia of tonsil----
Hemorrhages in heart-----
Hyperemia of lung
Petechiae in liver
Petechiae in kidney
Petechiae in intestine

LN, lymph node..


Table 3 . Genomic copy numbers of African swine fever virus in various organs from the 3-month-old viral inoculated growing pigs (n=6).

Pig caseGenome log copy numbers from organ tissue

Lymph nodeSpleenTonsilHeartLungLiverKidneyColon

SubmandibularMesentericInguinal
#754.86.36.26.35.34.85.66.36.25.1
#766.46.56.26.55.05.55.96.95.75.3
#776.35.46.37.14.85.05.56.55.84.7
#785.65.05.66.34.54.05.25.64.43.9
#796.46.46.56.66.74.85.96.65.75.4
#806.45.76.06.66.64.25.86.65.34.7
Average6.05.96.26.55.54.75.66.45.54.9

References

  1. Cho KH, Kim HJ, Kim YJ, Kang HE, Lee JB. 2021. Quantitative risk assessment of the African swine fever introduction into the Republic of Korea via legal import of live pigs and pig products. Transbound Emerg Dis 68:385-396.
    Pubmed CrossRef
  2. Costard S, Wieland B, De Glanville W, Jori F, Rowlands R, Vosloo W, Roger F, Dixon LK. 2009. African swine fever: how can global spread be prevented? Philos Trans R Soc Lond B Biol Sci 364:2683-2696.
    Pubmed KoreaMed CrossRef
  3. Galindo-Cardiel I, Ballester M, Solanes D, Nofrarías M, López-Soria S, Argilaguet JM, Lacasta A, Accensi F, Segalés J. 2013. Standardization of pathological investigations in the framework of experimental ASFV infections. Virus Res 173:180-190.
    Pubmed CrossRef
  4. Galindo I and Alonso C. 2017. African swine fever virus: a review. Viruses 9:103.
    Pubmed KoreaMed CrossRef
  5. Goonewardene KB, Onyilagha C, Goolia M, Le VP, Ambagala A. 2022. Superficial inguinal lymph nodes for screening dead pigs for African swine fever. Viruses 14:83.
    Pubmed KoreaMed CrossRef
  6. Kim HJ, Cho KH, Lee SK, Kim DY, Nah JJ, Kim HJ, Kim HJ, Hwang JY, Sohn HJ, Choi JG, Kim YJ. 2020. Outbreak of African swine fever in South Korea, 2019. Transbound Emerg Dis 67:473-475.
    Pubmed CrossRef
  7. Lee HS, Bui VN, Dao DT, Bui NA, Le TD, Kieu MA, Nguyen QH, Tran LH, Roh JH, So KM, Oh SI. 2021. Pathogenicity of an African swine fever virus strain isolated in Vietnam and alternative diagnostic specimens for early detection of viral infection. Porcine Health Manag 7:36.
    Pubmed KoreaMed CrossRef
  8. Mai NTA, Vu XD, Nguyen TTH, Nguyen VT, Trinh TBN, Kim YJ, Kim HJ, Cho KH, Nguyen TL, Bui TTN, Jeong DG, Yoon SW0, Truong T, Ambagala A, Le VP. 2021. Molecular profile of African swine fever virus (ASFV) circulating in Vietnam during 2019-2020 outbreaks. Arch Virol 166:885-890.
    Pubmed CrossRef
  9. Oh T, Do DT, Lai DC, Nguyen TC, Chae C. 2021. Age-related viral load and severity of systemic pathological lesions in acute naturally occurring African swine fever virus genotype II infections. Comp Immunol Microbiol Infect Dis 79:101709.
    Pubmed CrossRef
  10. OIE. 2019. Technical disease card of African Swine Fever. https://www.oie.int/fileadmin/Home/eng/Animal_Health_in_the_World/docs/pdf/Disease_cards/AFRICAN_SWINE_FEVER.pdf. Accessed June 2019
  11. Pikalo J, Schoder ME, Sehl-Ewert J, Breithaupt A, Cay AB, Lhoëst C, van Campe W, Mostin L, Deutschmann P, Roszyk H, Beer M, Tignon M. 2021. Towards efficient early warning: pathobiology of African swine fever virus "Belgium 2018/1" in domestic pigs of different age classes. Animals 11:2602.
    Pubmed KoreaMed CrossRef
  12. Post J, Weesendorp E, Loeffen WL. 2017. Influence of age and dose of African swine fever virus infections on clinical outcome and blood parameters in pigs. Viral Immunol 30:58-69.
    Pubmed CrossRef
  13. Sánchez-Vizcaíno JM, Arias ML. 2019. African swine fever virus. Dis Swine : 443-452.
    Pubmed KoreaMed CrossRef
  14. Sun E, Zhang Z, Wang Z, He X, Zhang X, Wang L, Wang W, Huang L, Xi F, Huangfu H, Tsegay G, Huo H, Sun J, Tian Z, Xia W, Yu X, Li F, Liu R, Guan Y, Bu Z. 2021. Emergence and prevalence of naturally occurring lower virulent African swine fever viruses in domestic pigs in China in 2020. Sci China Life Sci 64:752-765.
    Pubmed CrossRef
  15. Wang S, Zhang J, Zhang Y, Yang J, Wang L, Qi Y, Han X, Zhou X, Miao F, Chen T, Wang Y, Zhang F, Hu R. 2020. Cytokine storm in domestic pigs induced by infection of virulent African swine fever virus. Front Vet Sci 7:601641.
    Pubmed KoreaMed CrossRef
  16. Zhao D, Liu R, Zhang X, Li F, Wang J, Zhang J, Liu X, Wang L, Zhang J, Wu X, Guan Y, Chen W, Wang X, Bu Z. 2019. Replication and virulence in pigs of the first African swine fever virus isolated in China. Emerg Microbes Infect 8:438-447.
    Pubmed KoreaMed CrossRef
KJVS
Jun 30, 2022 Vol.45 No.2, pp. 101~99

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