Prevalence and risk factors of bovine alphaherpesvirus 1 (BoHV-1) in western Pernambuco, BrazilABSTRACT
The study aimed to conduct an epidemiological survey to determine the prevalence and risk factors associated with bovine alphaherpesvirus 1 (BoHV-1) infection in cattle from western Pernambuco State. Serum samples from 369 animals were analyzed, distributed across 19 rural properties in three municipalities: Afrânio, Araripina, and Petrolina. The participating cattle were unvaccinated against the virus, aged two years or older, and belonged to beef and/or dairy herds. Serological diagnosis was performed using the microplate serum neutralization test. Epidemiological questionnaires were applied on each property, gathering information about livestock production characteristics. Statistical analysis included a univariate approach followed by a mixed model with the herd as a random intercept to identify potential risk factors. The prevalence observed in herds and individual animals was 89.5% (17/19) and 43.1% (159/369), respectively. In the univariate analysis, contact with neighboring cattle showed an odds ratio (OR) of 4.42, emphasizing the importance of this variable in the disease’s epidemiology. The detection of seropositive animals in the study area highlights the need to establish control and prevention measures to safeguard the health status of herds in the region.
Keywords
reproductive disease; risk factors; IBR; prevalence; infectious bovine rhinotracheitis
RESUMO
O objetivo da pesquisa foi realizar inquérito epidemiológico para identificar a prevalência e os fatores de risco associados à infecção pelo alfaherpesvírus bovino 1 (BoHV-1) em bovinos do oeste do Estado de Pernambuco. Foram analisadas amostras de soro de 369 animais, distribuídos entre 19 propriedades rurais de três municípios: Afrânio; Araripina; e Petrolina. Os bovinos participantes não eram vacinados contra o vírus, possuíam idade igual ou superior a dois anos e eram de rebanhos de corte e/ou leite. O diagnóstico sorológico foi realizado por meio da técnica de soroneutralização em microplacas. Em cada propriedade foram aplicados questionários epidemiológicos contendo informações sobre as características da exploração pecuária. Foi realizada análise estatística univariada, seguida de um modelo misto, com rebanho como intercepto aleatório para identificação de possíveis fatores de risco. A prevalência encontrada nos rebanhos e nos animais foi de 89,5% (17/19) e de 43,1% (159/369), respectivamente. Na análise univariada, o contato com bovinos vizinhos apresentou uma OR = 4,42, indicando a importância desta variável na epidemiologia da doença. A identificação de animais soropositivos na área de estudo indica que é necessário o estabelecimento de medidas de controle e prevenção, visando proteger o status sanitário dos rebanhos na região de estudo.
Palavras-chave
doença reprodutiva; fatores de risco; IBR; prevalência; rinotraqueíte infecciosa bovina
1. Introduction
The cattle industry is a key sector in the economy of the Brazilian semiarid region, counting on a herd of 27 million cattle (IBGE, 2023). However, livestock production in this region is still characterized by low productivity indices, such as reduced milk yield and extended calving intervals. Additionally, it is predominantly a subsistence or family-based activity (Neves et al., 2011; Clementino et al., 2015).
In this context, infectious agents such as bovine alphaherpesvirus 1 (BoHV-1) contribute to reduced productivity in the sector, leading to decreased milk production, lower reproductive efficiency, and increased herd mortality rates (Rola et al., 2015; Sayers, 2017; Sibhat et al., 2018). The virus is the etiological agent of infectious bovine rhinotracheitis (IBR), infectious pustular vulvovaginitis (IPV), and infectious pustular balanoposthitis (IPB), and it is also associated with cases of abortion, conjunctivitis, and encephalitis (Nandi et al., 2009).
BoHV-1 has a global distribution, with antibodies reported on all continents where livestock production occurs (Raaperi et al., 2014). In Brazil, the virus is widespread across all regions, with an average antibody prevalence of 54.2%. It causes annual economic losses of approximately 48 million USD, primarily due to abortion-related losses (Silva et al., 2021). BoHV-1 infection is associated with various risk factors, including large herd sizes, the use of mechanical milking systems, and uncertified semen (Almeida et al., 2021; Ortiz-González et al., 2022; Karimi et al., 2023).
Understanding the epidemiology of a disease is essential for developing effective viral control and prevention strategies in a given region, as pathogens behave uniquely depending on climate, animal management practices, and production purposes. However, there is a lack of studies on the epidemiology of BoHV-1 in the northeastern semiarid region of Brazil, particularly in the western part of the State of Pernambuco. Therefore, this study aimed to conduct an epidemiological investigation to determine the prevalence and risk factors associated with the presence of anti-BoHV-1 antibodies in cattle herds in western Pernambuco.
2. Material and methods
This study was approved by the Ethics Committee on Animal Use (CEUA) of the Federal University of Vale do São Francisco (UNIVASF), under registration number 0004/260722. The epidemiological survey was conducted in three municipalities in the western part of the State of Pernambuco: Afrânio, Araripina, and Petrolina (Figure 1).
The study area is located in the northeastern semi-arid region, characterized by a maximum annual precipitation of 800 mm, high temperatures, and a rainfall pattern marked by scarcity and irregular distribution. It lies within the Caatinga biome, a type of vegetation adapted to arid conditions but with soils of low productive potential, which poses challenges to agricultural and livestock production (Silva et al., 2010). Despite these constraints, the studied municipalities have a total cattle herd of 62,943 head (IBGE, 2023) and an annual milk production of 7.4 million liters (IBGE, 2017).
Given the large cattle population in the area, sample size was determined according to Thrusfield and Christley (2018), considering a 95% confidence level, a desired absolute precision of 5%, and an expected prevalence of 60%, based on the average prevalence reported in previous studies in the Brazilian semiarid region (Silva et al., 2015; Fernandes et al., 2019; Silva et al., 2019; Haas et al., 2020). A total of 369 animals were sampled from 19 rural properties, selected through non-probabilistic convenience sampling, from August 2022 to January 2023. The sampled cattle were unvaccinated against BoHV-1, aged two years or older, and from beef and/or dairy properties.
To collect serum samples, blood (9 mL) was drawn via puncture of the coccygeal or jugular vein using vacuum collection tubes without anticoagulant. The cattle were restrained using ropes, chutes, and/or squeeze crates, and the puncture site was aseptically prepared with iodinated alcohol. The tubes were labeled and transported in refrigerated isothermal containers to the laboratory. Blood serum was obtained by centrifugation and transferred to sterile microtubes. The samples were stored at −20 °C in the laboratory until analysis.
To identify potential risk factors associated with BoHV-1 infection, a structured questionnaire was applied on each property. The questionnaire covered information regarding location, rearing system, milking type, reproductive management, frequency of cattle purchases, contact with cattle from other properties, veterinary assistance, quarantine practices, presence of other production animals, use of borrowed bulls, and loaning of bulls. Additionally, an individual record was created for each bovine, identifying the animal by name and/or ear tag, sex, breed, and property of origin.
The serological diagnosis of BoHV-1 was performed using the serum neutralization (SN) technique on 96-well microplates, as recommended by the World Organisation for Animal Health (2024). Serum dilutions were prepared in decreasing order of concentration starting from row B, ranging from 1:2 to 1:128, with one column of the microplate allocated for each dilution. Each well received a constant dose of the virus (BoHV-1 LA, 100 TCID50/50µL), except for row A, which served as the negative control for bovine sera. After incubating the virus with the respective sera at 37 °C for 1 hour, 50 µL containing 50,000 MDBK cells were added. Test readings were performed after 72 hours by observing the cytopathic effect. Neutralizing antibody titers were determined as the highest serum dilutions capable of inhibiting viral replication, classified into groups (negative, ≥ 2 and ≤ 8, ≥ 16 and ≤ 64, ≥ 128).
Risk factor analysis was carried out in two stages: univariate analysis and multivariate analysis. In the univariate analysis, each independent variable was cross-tabulated with the dependent variable (serological status of the animal for BoHV-1). Variables with p < 0.2 in the univariate analysis were included in the initial multivariate model. Collinearity among predictor variables was assessed using the variance inflation factor (VIF). Variables with VIF < 5 were subjected to the next analysis, a mixed regression model, which considered BoHV-1 seropositivity as the dependent variable and management variables as explanatory variables. In this mixed regression model, the herd variable was treated as a random effect. A significance level of 5% was adopted for the multivariate analysis. All analyses were performed using SPSS 13.0 for Windows.
3. Results and Discussion
Among the 369 samples analyzed, 159 tested positive for anti-BoHV-1 antibodies, resulting in a seroprevalence of 43.1% (Table 1). This study represents the first record of antibodies against BoHV-1 in the western region of the State of Pernambuco. Since all samples were obtained from unvaccinated cattle, the observed seropositivity indicates prior exposure to the infectious agent.
Prevalence of antibodies against bovine alphaherpesvirus 1 (BoHV-1) in western Pernambuco, 2023.
It should be considered that BoHV-1 infection establishes a latent state in the sensory ganglia of the peripheral nervous system, persisting throughout the host’s lifetime (Ostler & Jones, 2023). The infection can be reactivated under stressful conditions or by the administration of corticosteroids (El-Mayet & Jones, 2024). Consequently, clinically healthy cattle may act as latent carriers, potentially resuming viral transmission.
Serological positivity does not necessarily indicate active infection or the presence of clinical signs. The severity and pathogenesis depend on the virulence of the virus; however, the infection is generally not fatal, and carrier animals often remain asymptomatic, serving as silent transmitters. Nevertheless, secondary bacterial infections can exacerbate the clinical condition (Biswas et al., 2013).
The virus is distributed worldwide, with varying prevalence rates reported across different countries. These include 60.0% in Egypt (Mahmoud & Ali, 2022), 57.5% in Colombia (Ortiz-González et al., 2022), 50.0% in Iran (Karimi et al., 2023), 43.7% in Algeria (Djellata, 2024), 39.53% in Turkey (İnce & Şevik, 2022), 39.5% in Poland (Socha et al., 2022), 31.4% in India (Patil et al., 2022), 30.0% in Ethiopia (Asmare et al., 2023), 21.4% in Ireland (Barrett et al., 2024), 17.4% in Kenya (Kipyego et al., 2020), 14.3% in Australia (Cusack et al., 2021), and 2.7% in Peru (Mendoza-Estela et al., 2024).
Prevalence also varies in the Brazilian semiarid region. In the Agreste region of Pernambuco, studies have reported a seroprevalence of 52.8% in the microregion of Vale do Ipanema (Silva et al., 2019) and 79.5% in the microregion of Garanhuns (Silva et al., 2015). In Paraíba, the prevalence is reported at 64.8% (Fernandes et al., 2019), while in northern Minas Gerais, 48.6% of cattle have anti-BoHV-1 antibodies (Haas et al., 2020). Differences in sample size, geographic characteristics, cattle farming practices, and seasonal variations help explain the discrepancies in prevalence observed in studies conducted in the semiarid region and worldwide.
The herd prevalence found in this study was 89.5% (17/19), which is consistent with other studies in Pernambuco, where prevalence values reached 100.0% (Silva et al., 2015; Silva et al., 2019). In one property, all tested cattle were seropositive, while in two properties, no seropositive animals were identified. This significant variation in infection prevalence among properties, as illustrated in Figure 2, reflects the differences in production methods and environmental conditions specific to each herd.
The presence of antibodies in most herds and the high seroprevalence observed in this and other studies indicate a widespread distribution of BoHV-1 among herds in the Brazilian semi-arid region. The lack of a prevention and control program for BoHV-1 infection in Brazil, combined with low adherence to vaccination in the study area, contributes to the dissemination of the virus. In the municipality of Petrolina, only 3.5% of producers vaccinate against IBR (Neves et al., 2011). Vaccination has been shown to be effective in reducing infection rates in herds (Brock et al., 2020; Sarangi et al., 2021).
Map of the study area with the location of the 19 herds analyzed according to serological results for bovine alphaherpesvirus 1 (BoHV-1).
In the univariate analysis of risk factors, the variables “contact with neighboring cattle” and “technical assistance” were associated with BoHV-1 infection. Contact with cattle from neighboring properties showed an odds ratio (OR) of 4.42 (P = 0.028), highlighting the importance of this variable in the disease’s epidemiology (Table 2).
Univariate analysis of potential risk factors associated with the presence of BoHV-1 seropositive animals, 2023.
In the state of Acre, the lack of veterinary assistance was previously associated with a higher likelihood of seropositivity for BoHV-1 (Arruda et al., 2019). The absence of veterinary assistance leads to lower adoption of biosecurity measures, thereby facilitating the transmission of infectious diseases. Thus, to control the virus in the region, it is essential to develop programs that provide technical support to cattle farmers, particularly those engaged in family farming, who comprise the majority in the study area.
In the multivariate analysis, using a mixed model with the herd as a random intercept, the model’s accuracy was observed to be 69.9%, with a p-value of 0.082 (Table 3). The variables initially identified as associated with the presence of seropositive animals were not confirmed as risk factors. In this study, the presence of seropositive animals was confirmed in 89.5% of the herds, with only two herds having no seropositive animals. This finding underscores the need for studies involving a larger number of herds to develop mixed models that are not affected by the “cluster” effect.
Mixed regression model for variables associated with the presence of BoHV-1 seropositive animals, 2023.
The variable “contact with neighboring animals” was identified as a factor associated with the presence of anti-BoHV-1 antibodies in animals only in the univariate analysis. In the studied properties, this contact typically occurred due to the shared use of Caatinga areas for communal grazing with cattle from other producers or the proximity of cattle through property boundary fences. Pasture sharing has previously been identified as a risk factor for virus transmission in the Ipanema Valley, Pernambuco (Silva et al., 2019), and in Paraíba (Fernandes et al., 2019). BoHV-1 is transmitted via aerosols, making close contact an important transmission route (Nandi et al., 2009). Therefore, increased contact, whether among cattle within the same property or with those from neighboring properties, raises the likelihood of exposure to the pathogen and subsequent infection.
4. Conclusions
The results of this study indicate that BoHV-1 infection is widely disseminated in the studied area, highlighting the need for implementing control measures. The adoption of biosecurity practices is recommended, such as restricting contact between cattle from different properties through the installation of fences along property boundaries. These measures would help maintain the herds’ health status and improve cattle productivity in western Pernambuco.
Acknowledgments
The authors would like to thank the Fundação de Amparo à Ciência e Tecnologia do Estado de Pernambuco (FACEPE) for the grant.
References
-
Almeida, Í. C. D., Almeida, Y. V., Donatele, D. M., Clipes, R. C., Barioni, G., Zanini, M. S., & Filippo, P. A. D. (2021). Seroprevalence and associated factors of infectious bovine rhinotracheitis and bovine viral diarrhea in dairy cows in the Caparaó region, Espírito Santo, Brazil. Ciência Rural, 51(12), Article 20200220. https://doi.org/10.1590/0103-8478cr20200220.
» https://doi.org/10.1590/0103-8478cr20200220 -
Arruda, E. F., Silva, T. I. B., Aragão, B. B., Castro, R. S., & Gomes, Y. A. (2019). Soroprevalence of bovine alphaherpesvirus type 1 (BoHV-1) and risk factors associated with dairy properties of the municipality of Senador Guiomard, Acre, Brazil. Arquivos do Instituto Biológico, 86, Article 1362018. https://doi.org/10.1590/1808-1657001362018.
» https://doi.org/10.1590/1808-1657001362018 -
Asmare, K., Aragaw, K., Sibhat, B., Abayneh, T., Gelaye, E., Getachew, B., & Egan, S. (2023). Seroprevalence and risk factors associated with bovine herpesvirus 1 (BHV-1) infection in dairy cattle in southern and central Ethiopia. Preventive Veterinary Medicine, 217, Article 105959. https://doi.org/10.1016/j.prevetmed.2023.
» https://doi.org/10.1016/j.prevetmed.2023. -
Barrett, D., Lane, E., Lozano, J. M., O’Keeffe, K., & Byrne, A. W. (2024). Bovine Herpes Virus Type 1 (BoHV-1) seroprevalence, risk factor and Bovine Viral Diarrhoea (BVD) co-infection analysis from Ireland. Scientific Reports, 14(1), 867−976. https://doi.org/10.1038/s41598-023-50433-5.
» https://doi.org/10.1038/s41598-023-50433-5 -
Biswas, S., Bandyopadhyay, S., Dimri, U., & H. Patra, P. (2013). Bovine herpesvirus-1 (BHV-1)–a re-emerging concern in livestock: a revisit to its biology, epidemiology, diagnosis, and prophylaxis. Veterinary Quarterly, 33(2), 68−81. https://doi.org/10.1080/01652176.2013.799301.
» https://doi.org/10.1080/01652176.2013.799301 -
Brock, J., Lange, M., Guelbenzu-Gonzalo, M., Meunier, N., Vaz, A. M., Tratalos, J. A., Dittrich, P., Gunn, M., More, S. J., Graham, D., & Thulke, H.-H. (2020). Epidemiology of age-dependent prevalence of Bovine Herpes Virus Type 1 (BoHV-1) in dairy herds with and without vaccination. Veterinary Research, 51(1), Article 124. https://doi.org/10.1186/s13567-020-00842-5.
» https://doi.org/10.1186/s13567-020-00842-5 -
Clementino, I. J., Pimenta, C. R. M., Fernandes, L. G., Bezerra, C. D. S., Alves, C. J., Dias, R. A., Amaku, M., Ferreira, F., Telles, E. O., Gonçalves, V. S. P., Ferreira Neto, J. S., & Azevedo, S. S. (2015). Caracterização da pecuária bovina no Estado da Paraíba, Nordeste do Brasil. Semina: Ciências Agrárias, 36(1), 557−570. https://doi.org/10.5433/1679-0359.2015v36n1p557.
» https://doi.org/10.5433/1679-0359.2015v36n1p557 -
Cusack, P., Bergman, E., Hay, K., & Morton, J. (2020). Serological status of cattle to bovine viral diarrhoea virus and bovine herpesvirus 1 at entry to and exit from Australian feedlot backgrounding facilities. Australian Veterinary Journal, 99(1−2), 20–23. https://doi.org/10.1111/avj.13021.
» https://doi.org/10.1111/avj.13021 -
Djellata, N. (2024). Seroprevalence of infectious bovine rhinotracheitis in aborted cows in Algeria. Veterinarska Stanica, 55(3), 311–316. https://doi.org/10.46419/vs.55.3.2.
» https://doi.org/10.46419/vs.55.3.2 -
El-Mayet, F., & Jones, C. (2024). Stress Can Induce Bovine Alpha-Herpesvirus 1 (BoHV-1) Reactivation from Latency. Viruses, 16(11), 1675–1691. https://doi.org/10.3390/v16111675.
» https://doi.org/10.3390/v16111675 -
Fernandes, L. G., Denwood, M. J., Santos, C. S. A. B., Alves, C. J., Pituco, E. M., Romaldini, A. H. C. N, Stefano, E., Nielsen, S. S. & Azevedo. S. S. (2019). Bayesian estimation of herd-level prevalence and risk factors associated with BoHV-1 infection in cattle herds in the State of Paraíba, Brazil. Preventive Veterinary Medicine, 169, Article 104705. https://doi.org/10.1016/j.prevetmed.2019.104705.
» https://doi.org/10.1016/j.prevetmed.2019.104705 -
Haas, D. J., Barbieri, J. M., Freitas, E. J. P., Oliveira, M. S., Porto, B. R., Rodrigues, R. O., Heinemann, M. B., Almeida, A. C., Lobato, Z. I. P., Dorneles, E. M. S. & Lage, A. P. (2020). Seroprevalence and intercurrence of reproductive pathogens in cattle from family farms in North of Minas Gerais, Brazil. Semina: Ciências Agrárias, 41(1), 145−158. https://doi.org/10.5433/1679-0359.2020v41n1p145.
» https://doi.org/10.5433/1679-0359.2020v41n1p145 -
IBGE − Instituto Brasileiro de Geografia e Estatística. (2017). Censo Agropecuário 2017. https://sidra.ibge.gov.br/tabela/6912#resultado Accessed April 05, 2024.
» https://sidra.ibge.gov.br/tabela/6912#resultado -
IBGE − Instituto Brasileiro de Geografia e Estatística. (2023). Pesquisa Pecuária Municipal 2023. https://sidra.ibge.gov.br/tabela/3939#resultado Accessed September 20, 2024.
» https://sidra.ibge.gov.br/tabela/3939#resultado -
İnce, Ö. B., & Şevik, M. (2022). Risk assessment and seroprevalence of bovine herpesvirus type 1 infection in dairy herds in the inner Aegean Region of Turkey. Comparative Immunology, Microbiology and Infectious Diseases, 80, Article 101741. https://doi.org/10.1016/j.cimid.2021.101741.
» https://doi.org/10.1016/j.cimid.2021.101741 -
Karimi, O., Sani, M. B., Bakhshesh, M., Harofteh, J. Z., & Poormirzayee-Tafti, H. (2023). Prevalence of bovine herpesvirus 1 antibodies and risk factors in dairy cattle of Iran’s central desert. Tropical Animal Health and Production, 55(1), Article 23. https://doi.org/10.1007/s11250-022-03426-x.
» https://doi.org/10.1007/s11250-022-03426-x -
Kipyego, E. S., Gitau, G., Vanleeuwen, J., Kimeli, P., Abuom, T. O., Gakuya, D., Muraya, J., & Makau, D. (2020). Sero-prevalence and risk factors of infectious bovine rhinotracheitis virus (type 1) in Meru County, Kenya. Preventive Veterinary Medicine, 175, Article 104863. https://doi.org/10.1016/j.prevetmed.2019.104863.
» https://doi.org/10.1016/j.prevetmed.2019.104863 -
Mahmoud, H., & Ali, A. (2022). Epidemiological investigation on Bovine alphaherpesvirus 1 and bovine viral diarrhea virus in cattle and camels in southern Egypt. Veterinaria Italiana, 58(4), 399−404. https://doi.org/10.12834/vetit.2361.14459.2.
» https://doi.org/10.12834/vetit.2361.14459.2 -
Mendoza-Estela, J. E., Briones, G., & Vargas-Rocha, L. (2024). Initial Seroprevalence Records of Infectious Agents Implicated in Reproductive Issues in High-altitude Cattle from Two Districts in Cajamarca, Peru. Kafkas Universitesi Veteriner Fakultesi Dergisi, 30(2): 283−288. https://doi.org/10.9775/kvfd.2023.30503.
» https://doi.org/10.9775/kvfd.2023.30503 -
Nandi, S., Kumar, M., Manohar, M., & Chauhan, R. S. (2009). Bovine herpes virus infections in cattle. Animal Health Research Reviews, 10(1), 85–98. https://doi.org/10.1017/s1466252309990028.
» https://doi.org/10.1017/s1466252309990028 -
Neves, A. L. A., Pereira, L. G. R., Santos, R. D.; Araújo, G. G. L.; Carneiro, A. V., Moraes, S. A., Spaniol, C. M. O., & Aragão, A. S. L. (2011). Caracterização dos produtores e dos sistemas de produção de leite no perímetro irrigado de Petrolina/PE. Revista Brasileira de Saúde e Produção Animal, 12(1), 209–223. https://periodicos.ufba.br/index.php/rbspa/article/view/40416/22486
» https://periodicos.ufba.br/index.php/rbspa/article/view/40416/22486 -
Ortiz-González, A. D., Buitrago, H. A. L., Bulla-Castañeda, D. M., Lancheros-Buitrago, D. J., Garcia-Corredor, D. J., Díaz-Anaya, A. M., Tobón-Torreglosa, J. C., Ortiz-Ortega, D. & Pulido-Medellín, M. O. (2022). Seroprevalence and risk factors associated with bovine herpesvirus 1 in dairy herds of Colombia. Veterinary World, 15(6), 1550−1556. https://doi.org/10.14202/vetworld.2022.1550-1556.
» https://doi.org/10.14202/vetworld.2022.1550-1556 -
Ostler, J. B., & Jones, C. (2023). The Bovine Herpesvirus 1 Latency-Reactivation Cycle, a Chronic Problem in the Cattle Industry. Viruses, 15(2), 552−566. https://doi.org/10.3390/v15020552.
» https://doi.org/10.3390/v15020552 -
Patil, S. S., Suresh, K. P., Velankar, A., Shivaranjini, C., Hemadri, D., Hiremath, J., & Jacob, S. S. (2022). Seroprevalence of infectious bovine rhinotracheitis (IBR) in India: a 5-year study. Veterinaria Italiana, 58(3), 339−349. https://doi.org/10.12834/VetIt.2433.16160.1.
» https://doi.org/10.12834/VetIt.2433.16160.1 -
Raaperi, K., Orro, T., & Viltrop, A. (2014). Epidemiology and control of bovine herpesvirus 1 infection in Europe. The Veterinary Journal, 201(3), 249−256. https://doi.org/10.1016/j.tvjl.2014.05.040.
» https://doi.org/10.1016/j.tvjl.2014.05.040 -
Rola, J. G., Larska, M., Grzeszuk, M., & Rola, J. (2015). Association between antibody status to bovine herpesvirus 1 and quality of milk in dairy herds in Poland. Journal of Dairy Science, 98(2), 781−789. https://doi.org/10.3168/jds.2014-8781.
» https://doi.org/10.3168/jds.2014-8781 -
Sarangi, L. N., Tharani, N., Polapally, S., Rana, S. K., Thodangala, N., Bahekar, V. S., Prasad, A., Reddy, R. V. C., Surendra, K. S. N. L, Naidu, G. H., Ponnanna, N. M., & Sharma, G. K. (2021). Infectious bovine abortions: observations from an organized dairy herd. Brazilian Journal of Microbiology, 52, 439−448. https://doi.org/10.1007/s42770-020-00414-x.
» https://doi.org/10.1007/s42770-020-00414-x -
Sayers, R. G. (2017). Associations between exposure to bovine herpesvirus 1 (BoHV-1) and milk production, reproductive performance, and mortality in Irish dairy herds. Journal of Dairy Science, 100(2), 1340–1352. https://doi.org/10.3168/jds.2016-11113.
» https://doi.org/10.3168/jds.2016-11113 -
Sibhat, B., Ayelet, G., Skjerve, E., Gebremedhin, E. Z., & Asmare, K. (2018). Bovine herpesvirus-1 in three major milk sheds of Ethiopia: Serostatus and association with reproductive disorders in dairy cattle. Preventive Veterinary Medicine, 150, 126-132. https://doi.org/10.1016/j.prevetmed.2017.12.019
» https://doi.org/10.1016/j.prevetmed.2017.12.019 -
Silva, B. P. e, Soares, L. B. F., Macêdo, A. A. de, Oliveira, J. M. B. de, Aragão, B. B., Nascimento, S. A. do, & Pinheiro Júnior, J. W. (2019). Soroprevalência e fatores de risco associados ao herpesvírus bovino tipo 1 e ocorrência da infecção pelo vírus da diarreia viral bovina em vacas leiteiras no estado de Pernambuco. Medicina Veterinária (UFRPE), 13(3), 399−405. https://doi.org/10.26605/medvet-v13n3-3302.
» https://doi.org/10.26605/medvet-v13n3-3302 -
Silva, B. P. e, Aragão, B. B., & Pinheiro Junior, J. W. (2021). Economic impacts of Bovine alphaherpesvirus 1 infection in Brazil: Meta-analysis based on epidemiological indicators. Semina: Ciencias Agrarias, 42(6), 3355–3378. https://doi.org/10.5433/1679-0359.2021v42n6p3355.
» https://doi.org/10.5433/1679-0359.2021v42n6p3355 -
Silva, F. B., Oliveira, J. M. B., Batista Filho, A. F. B., Ribeiro, C. P., Pituco, E. M., & Pinheiro Junior, J. W. (2015). Análise soroepidemiológica da infecção pelo herpesvírus bovino tipo 1 (BoHV-1) em bovinos no Estado de Pernambuco. Acta Scientiae Veterinariae, 43, Article 1324. https://www.ufrgs.br/actavet/43/PUB%201324.pdf
» https://www.ufrgs.br/actavet/43/PUB%201324.pdf -
Silva, P. C. G., Moura, M. S. B., Kiill, L. H. P., Brito, L. T. L., Pereira, L. A., Sá, I. B., Correia, R. C., Teixeira, A. H. C., Cunha, T. J. F., & Guimarães Filho, C. (2010). Caracterização do semiárido brasileiro: Fatores naturais e humanos. In I. B. Sá & P. C. G. Silva (Eds.), Semiárido brasileiro: Pesquisa, desenvolvimento e inovação (pp. 18−48). Embrapa Semiárido. https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/861895/1/Semiarido-brasileiro-pesquisa-desenvolvimento-e-inovacao.pdf
» https://www.infoteca.cnptia.embrapa.br/infoteca/bitstream/doc/861895/1/Semiarido-brasileiro-pesquisa-desenvolvimento-e-inovacao.pdf -
Socha, W., Larska, M., Rola, J., & Bednarek, D. (2022). Occurrence of bovine coronavirus and other major respiratory viruses in cattle in Poland. Journal of Veterinary Research, 66(4), 479–486. https://doi.org/10.2478/jvetres-2022-0059
» https://doi.org/10.2478/jvetres-2022-0059 - Thrusfield, M., & Christley, R. (2018). Veterinary epidemiology (4th ed.). Wiley.
-
World Organisation for Animal Health. (2024). Infectious Bovine Rhinotracheitis/Infectious Pustular Vulvovaginitis. In Manual of diagnostic tests and vaccines for terrestrial animals (13th ed.). https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.04.11_IBR_IPV.pdf
» https://www.woah.org/fileadmin/Home/eng/Health_standards/tahm/3.04.11_IBR_IPV.pdf
Edited by
-
Editor:
Mario Celso Sperotto Brum
Publication Dates
-
Publication in this collection
28 Feb 2025 -
Date of issue
2025
History
-
Received
03 Oct 2024 -
Accepted
25 Dec 2024
