Epidemiological Investigation, Risk Factors, Spatial-Temporal Cluster, and Epidemic Trend Analysis of Pseudorabies Virus Seroprevalence in China (2017 to 2021)

PRV is a critical pathogen threatening the global swine industry. Our research fills knowledge gaps regarding PRV prevalence, infection risk factors, spatial-temporal clustering of high PRV gE seroprevalence, and the epidemic trend of PRV gE seroprevalence in China in recent years. These findings are valuable for the clinical prevention and control of PRV infection and suggest that PRV infection is likely to be successfully controlled in China. ABSTRACT Pseudorabies virus (PRV) is a double-stranded linear DNA virus capable of infecting various animals, including humans. We collected blood samples from 14 provinces in China between December 2017 and May 2021 to estimate PRV seroprevalence. The PRV gE antibody was detected using the enzyme-linked immunosorbent assay (ELISA). Logistic regression analysis identified potential risk factors associated with PRV gE serological status at the farm level. Spatial-temporal clusters of high PRV gE seroprevalence were explored using SaTScan 9.6 software. Time-series data of PRV gE seroprevalence were modeled using the autoregressive moving average (ARMA) method. A Monte Carlo sampling simulation based on the established model was performed to analyze epidemic trends of PRV gE seroprevalence using @RISK software (version 7.0). A total of 40,024 samples were collected from 545 pig farms across China. The PRV gE antibody positivity rates were 25.04% (95% confidence interval [CI], 24.61% to 25.46%) at the animal level and 55.96% (95% CI, 51.68% to 60.18%) at the pig farm level. Variables such as farm geographical division, farm topography, African swine fever (ASF) outbreak, and porcine reproductive and respiratory syndrome virus (PRRSV) control in pig farms were identified as risk factors for farm-level PRV infection. Five significant high-PRV gE seroprevalence clusters were detected in China for the first time, with a time range of 1 December 2017 to 31 July 2019. The monthly average change value of PRV gE seroprevalence was −0.826%. The probability of a monthly PRV gE seroprevalence decrease was 0.868, while an increase was 0.132. IMPORTANCE PRV is a critical pathogen threatening the global swine industry. Our research fills knowledge gaps regarding PRV prevalence, infection risk factors, spatial-temporal clustering of high PRV gE seroprevalence, and the epidemic trend of PRV gE seroprevalence in China in recent years. These findings are valuable for the clinical prevention and control of PRV infection and suggest that PRV infection is likely to be successfully controlled in China.

[1]  Junlong Zhao,et al.  Risk Factors and Spatial-Temporal Analysis of Porcine Reproductive and Respiratory Syndrome Seroprevalence in China Before and After African Swine Fever Outbreak , 2022, Frontiers in Veterinary Science.

[2]  Hongying Chen,et al.  Serological Investigation and Genetic Characteristics of Pseudorabies Virus between 2019 and 2021 in Henan Province of China , 2022, Viruses.

[3]  Junlong Zhao,et al.  Seroprevalence Investigation of Classic Swine Fever Virus Before, During, and After African Swine Fever Virus Outbreak in Some Provinces of China from 2017 to 2021. , 2022, Viral immunology.

[4]  H. Favoreel,et al.  The Attenuated Pseudorabies Virus Vaccine Strain Bartha K61: A Brief Review on the Knowledge Gathered during 60 Years of Research , 2020, Pathogens.

[5]  Aibing Wang,et al.  Current Status and Challenge of Pseudorabies Virus Infection in China , 2020, Virologica Sinica.

[6]  Sidang Liu,et al.  Epidemiological investigation of porcine pseudorabies virus and its coinfection rate in Shandong Province in China from 2015 to 2018 , 2020, Journal of veterinary science.

[7]  Qin Chen,et al.  Risk analysis of African swine fever in Poland based on spatio-temporal pattern and Latin hypercube sampling, 2014–2017 , 2019, BMC Veterinary Research.

[8]  M. Veit,et al.  Interspecies Transmission, Genetic Diversity, and Evolutionary Dynamics of Pseudorabies Virus , 2018, The Journal of infectious diseases.

[9]  Z. Bu,et al.  Replication and virulence in pigs of the first African swine fever virus isolated in China , 2019, Emerging microbes & infections.

[10]  R. S. Soares Magalhaes,et al.  Epidemiology of pseudorabies in intensive pig farms in Shanghai, China: Herd-level prevalence and risk factors. , 2018, Preventive veterinary medicine.

[11]  Qi Xu,et al.  Investigation on pseudorabies prevalence in Chinese swine breeding farms in 2013–2016 , 2018, Tropical Animal Health and Production.

[12]  P. Diggle,et al.  Veterinary Epidemiology: Fourth Edition , 2017 .

[13]  H. Qiu,et al.  Control of swine pseudorabies in China: Opportunities and limitations. , 2016, Veterinary microbiology.

[14]  R. Fite,et al.  Quantitative risk assessment of entry of contagious bovine pleuropneumonia through live cattle imported from northwestern Ethiopia. , 2015, Preventive veterinary medicine.

[15]  B. Martínez-López,et al.  Assessing the Risk of African Swine Fever Introduction into the European Union by Wild Boar. , 2015, Transboundary and emerging diseases.

[16]  Min Hu,et al.  Seroprevalence and risk factors of Mycoplasma suis infection in pig farms in central China. , 2014, Preventive veterinary medicine.

[17]  S. Youngquist,et al.  Part 21: categoric analysis: Pearson chi-square test. , 2013, Air medical journal.

[18]  H. Nauwynck,et al.  Porcine reproductive and respiratory syndrome virus (PRRSV) causes apoptosis during its replication in fetal implantation sites. , 2011, Microbial pathogenesis.

[19]  E. C. Hahn,et al.  Pseudorabies virus in wild swine: a global perspective , 2011, Archives of Virology.

[20]  A. Allepuz,et al.  Exploratory spatial analysis of Aujeszky's disease during four phases of the eradication programme in Catalonia, Spain (2003-2007). , 2008, Preventive veterinary medicine.

[21]  C. Gortázar,et al.  Epidemiological risk factors of Aujeszky’s disease in wild boars (Sus scrofa) and domestic pigs in Spain , 2008, European Journal of Wildlife Research.

[22]  Lisa E. Pomeranz,et al.  Molecular Biology of Pseudorabies Virus: Impact on Neurovirology and Veterinary Medicine , 2005, Microbiology and Molecular Biology Reviews.

[23]  M. Kulldorff,et al.  A Space–Time Permutation Scan Statistic for Disease Outbreak Detection , 2005, PLoS medicine.

[24]  R. W. Humphry,et al.  A practical approach to calculate sample size for herd prevalence surveys. , 2004, Preventive veterinary medicine.

[25]  C. Hengartner,et al.  Complete, Annotated Sequence of the Pseudorabies Virus Genome , 2004, Journal of Virology.

[26]  Olaf Berke,et al.  Spatial relative risk mapping of pseudorabies-seropositive pig herds in an animal-dense region. , 2003, Journal of veterinary medicine. B, Infectious diseases and veterinary public health.

[27]  H. Boshuizen,et al.  Multiple imputation of missing blood pressure covariates in survival analysis. , 1999, Statistics in medicine.

[28]  B. Ripley,et al.  Modern Applied Statistics with S-Plus. , 1996 .

[29]  M.C.M. de Jong,et al.  Transmission of pseudorabies virus within pig populations is independent of the size of the population , 1995 .

[30]  M Kulldorff,et al.  Spatial disease clusters: detection and inference. , 1995, Statistics in medicine.

[31]  H. Bozdogan.  Model selection and Akaike's Information Criterion (AIC): The general theory and its analytical extensions , 1987 .

[32]  E. S. Pearson,et al.  THE USE OF CONFIDENCE OR FIDUCIAL LIMITS ILLUSTRATED IN THE CASE OF THE BINOMIAL , 1934 .

[33]  M. Thrusfield.  Veterinary epidemiology [4th Ed.] , 2018 .

[34]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[35]  S. Martin,et al.  Veterinary Epidemiologic Research , 2009 .

[36]  A. Kleyner,et al.  Monte Carlo Simulation , 2011, Encyclopedia of GIS.

[37]  M. R. Wilson,et al.  A Review of Pseudorabies (Aujeszky's Disease) in Pigs , 2007 .

[38]  Brian D. Ripley,et al.  The car Package , 2006 .

[39]  T. Mettenleiter.  Aujeszky's disease (pseudorabies) virus: the virus and molecular pathogenesis--state of the art, June 1999. , 2000, Veterinary research.

[40]  T. Drew.  A review of evidence for immunosuppression due to porcine reproductive and respiratory syndrome virus. , 2000, Veterinary research.