1 INTRODUCTION

Bovine viral diarrhea (BVD) is a viral disease that affects cattle and is caused by the bovine viral diarrhea virus (BVDV) (Fray et al., 2000; Hou et al., 2019). BVDV is a member of the Pestivirus genus in the Flaviviridae family, with two species (BVD1 and BVD2) and two biotypes (cytopathic and non-cytopathic) (Al-Kubati et al., 2021; Elhaig et al., 2018).

The disease caused significant financial losses directly through premature culling, reduction in milk production, high moralities, and decrease the reproductive performance as well as indirectly through costs associated with management and eradication programs (Jokar et al., 2021; Rodning et al., 2012; Santman-Berends et al., 2015).

It is primarily transmitted through direct contact with persistently infected (PI) animals which excrete and secret huge amounts of non-cytopathic (NCP) BVDV throughout their lives and cannot produce antibodies to the disease (Bachofen et al., 2013; Fulton, Briggs, et al., 2005; Khodakaram-Tafti & Farjanikish, 2017). In addition, the BVDV can be transmitted indirectly through infected semen or contaminated utensils (Fulton, Ridpath, et al., 2005). The most common natural route for BVDV infection in cattle is the oro-nasal pathway (Akagami et al., 2020).

There are several clinical syndromes caused by BVDV in cattle, including mucosal disease, diarrhea, reproduction disorders (abortion, fetus resorption, stillbirth, mummification of fetus), and hemorrhagic disorders (Dabak et al., 2007; Evermann & Ridpath, 2002; Lunardi et al., 2008).

Moreover, Immunocompromised cattle are a primary source of BVDV infections in herds because they may secrete and excrete the virus into the surrounding environment for a long period of time (Biswas et al., 2013; Fulton, 2013). Consequently, to quickly identify and eradicate persistent carriers in the herds and prevent further economic losses due to BVD, sensitive and precise diagnostic techniques are required (Safarpoor Dehkordi, 2011).

The negative consequences of BVDV infection on the health status of the herd and production may be reduced by effectively controlling and preventing the transmission of the virus, which could be conducted by understanding herd management practices and environmental variables that increase the risk of BVDV infection (Houe, 2003; Moennig et al., 2005).

In Egypt, several studies were conducted and detected PI animals by BVDV among cattle in several governorates in Egypt like Qalyubia (Gabr et al., 2014), Fayoum, and Alexandria (Amin et al., 2014) and Damietta (Atwa et al., 2019).

The diagnostic methods for identifying BVDV infection can be categorized into indirect testing (detect antibodies against BVDV, suggesting a prior exposure) and direct testing (identifying the viral components or virus) (Aragaw et al., 2018). The direct diagnostic methods such as isolation of virus on cell culture, polymerase chain reaction (PCR), and antigen capture ELISA (Dubovi, 2013; Selim et al., 2014; Selim, Manaa, & Khater, 2021). One crucial method for the indirect identification of the virus is the detection of viral-specific antibodies by the use of several serological assays, such as ELISA or virus neutralization test (Lanyon et al., 2014; Selim, Yang, et al., 2018).

Identifying risk factors for infection and understanding the current state of BVDV are crucial for creating and executing disease control and preventive initiatives. The prevalence of BVDV increased in counties that did not implement strict or effective control measures. In Egypt, the prevalence of BVDV-PI was 1.5% (Amin et al., 2014), while it was 6% and 7.5% based on antigen-competitive ELISA and real-time PCR, respectively (Selim, Elhaig, et al., 2018). Despite the use of several vaccines and control programs in Egypt, there has been a sharp rise in financial losses due to clinical or even subclinical BVDV infection.

Therefore, the study aimed to determine the seroprevalence and identify the associated risk factors for BVDV infection in cattle from four Egyptian governorates.

2 MATERIALS AND METHODS

2.2 Study area

The study was conducted from January to December 2023 in four Egyptian governorates: Kafr ElSheikh, Menofia, Alexandria, and Gharbia, all of which are located in northern Egypt, Figure 1.

Kafr ElSheikh, Menofia, and Gharbia governorates situated in the Nile Delta of Egypt have a subtropical desert climate (Classification: BWh) and are located 8–9 m above sea level. The annual temperature in this area is around 23°C and receives 4–5 mm of precipitation annually. In addition, Alexandria has a subtropical desert climate (classification: BWh) and is located 10 m above sea level. The annual temperature is 22°C and around 8.38 mm of precipitation each year. The selected study area is situated between two branches of the Nile and the main activity in these areas is agriculture and animal breeding.

3 RESULTS

Using iELISA test, 124 (18.24%) (95% CI: 15.52–21.32) of the 680 examined serum samples from cattle were positive for BVDV antibodies. There was no significant difference (P > 0.05) between the seroprevalence of BVDV and health status and location. Table 1 shows that the BVDV seropositivity was greater in the Kafr ElSheikh governorate (23.33%) and in cattle with low health status (20%).

Furthermore, there was a significant difference (P < 0.05) in the seroprevalence of BVDV according to age, sex, type of production, introduction of new animals, breeding style, history of abortion, and lactation status. The BVDV seropositivity was relatively higher in females (19.66%, 95% CI: 16.65–23.06), cattle older than 8 years (22.14%. 95% CI: 17.67–27.36), dairy animals (22.65%, 95% CI: 18.88–26.92) and when new animals were introduced to herds (21.39%, 95% CI: 17.72–25.58), Table 1. Interestingly, BVDV seropositivity rose significantly in AI breeding (28.46%), animals with a history of abortion (28.76%), and during the lactation stage (23%).

According to multivariate logistic regression analysis, females were one time (OR = 1.2, 95% CI: 1.11–2.45) more likely than males to get BVDV, and adult animals older than eight years old were three times (OR = 2.6, 95% CI: 1.16–5.97) more likely to contract BVDV infection than young animals, Table 2. Moreover, the introduction of new animals to the herd (OR = 1.4, 95% CI: 1.18–2.90), dairy cattle (OR = 1.9, 95% CI: 1.18–3.03), artificial insemination (OR = 1.3, 95% CI: 1.21–2.54), animals with a history of abortion (OR = 2.6, 95% CI: 1.68–4.06), or animals during lactation (OR = 1.9, 95% CI: 1.12–3.04) were increased the risk of BVDV infection (Table 2).

4 DISCUSSION

Bovine viral diarrhea (BVD) is an infectious disease that affects cattle and other ruminant populations worldwide. BVD causes enormous economic losses in the cattle sector due to its wide variety of clinical symptoms, which include respiratory and gastrointestinal problems, as well as reproductive issues. In Egypt, BVD causes significant economic losses and is widely disseminated among ruminants, despite the implementation of a vaccine program.

The seroprevalence of BVDV in cattle in this study was 18.24% (124/680) with a non-significant difference between studied areas, which comes in accordance with the previously reported rate (18.48%) in cattle from southern Egypt (Mahmoud & Ali, 2022).

The current finding was lower than previous studies which found seroprevalence of 32.6% to 51.9% in Ethiopian dairy cattle, respectively (Aragaw et al., 2018; Asmare et al., 2018; Tesfaye et al., 2021). The current finding is lower than previously reported seroprevalence rates of 19.8% in Kenya (Callaby et al., 2016), 27% in Ecuador (Herrera-Yunga et al., 2018), 36% in Colombia (Ortega et al., 2020), and 40% in Egypt (Selim, Elhaig, et al., 2018).

Conversely, the seroprevalence BVDV rate found in this study was greater than that reported in Ethiopia (11.46%) (Nigussie et al., 2010), Sudan (10.7%) (Saeed et al., 2015), Egypt (10.4%) (Soltan et al., 2015), and Nepal (2.2%) (Manandhar et al., 2018).

The difference in seroprevalences among studies from different countries may be attributed to management practices, study design, size of the herd, animal age, animal's populations, sample size, diagnostic technique, the existence of PI animals, and environmental conditions (Farghali et al., 2022; Houe, 1999; Selim & Abdelhady, 2020; Selim, Alafari, et al., 2022; Selim, Manaa, Alanazi, & Alyousif, 2021; Talafha et al., 2009).

In the current study, there was a strong association between age as a risk factor and BVDV seropositivity. Most studies have identified aging as a risk factor for BVDV seroprevalence (Demil et al., 2021; González-Bautista et al., 2021; Noaman & Nabinejad, 2020). In contrast, the association between age and BVDV seropositivity was not observed by Ortega et al. (2020). Moreover, the risk of BVDV infection increases with age, and the infected animal remains seropositive for life (Erfani et al., 2019; Noaman & Nabinejad, 2020; Radwan et al., 2022; Selim, Attia, et al., 2022; Selim, Megahed, Kandeel, et al., 2021). In addition, the lower seroprevalence in young animals may be due to PI animals being immune to the virus and not producing antibodies detectable by ELISA tests (Gates et al., 2013; Shirvani et al., 2012).

The present results support the previous findings of Karimi et al. (2022), where the health status did not confer as a risk factors for seroprevalence of BVDV. However, Demil et al. (2021) observed that animals with health have a high risk of contracting BVDV infection. This discrepancy in the results might be caused by variations in the methods used to evaluate health status, the layout of the questionnaire, and the biased answers provided by dairy owners (Karimi et al., 2022).

From the results of the present study, it is clear that the introduction of new animals to dairy herds increased the risk of BVD infection, which comes in agreement with the findings of Tadesse et al. (2019). This outcome supports earlier findings that buying breeding cattle, as opposed to storing animals, greatly increases BVDV seropositivity. Moreover, the antibody prevalence will rise dramatically with an increase in both the number of source farms and the number of introduced animals (Guelbenzu-Gonzalo et al., 2021). González-Bautista et al. (2021) found no significant correlation between BVDV seropositivity and cattle introduction into the herd. In addition, the introduction of two importing pregnant animals with a PI calf resulted in the re-infection of the free herd in Germany (Albrecht et al., 2021). Therefore, strict controls on animal trade and migration can minimize new BVDV infections (Scharnböck et al., 2018).

Interestingly, the present findings revealed high BVDV seroprevalence increased with AI breeding which was consistent with the results of González-Bautista et al. (2021). It is essential to emphasize that the utilization of biotechnologies, such as AI, has a direct impact on animal health by mitigating or averting BVD (Martínez-Rodríguez et al., 2021). AI is a protective factor against BVDV in bovine production. However, implementing this technique requires thorough sample analysis, since BVDV remains a possible problem in AI due to semen collection from PI bulls or those with acute-stage of BVDV infections (Arauco Villar & Lozano Salazar, 2018).

Cows with a history of abortion were more likely to be seropositive to BVDV compared to those without a history of reproductive problems, consistent with previous studies that found a higher prevalence of BVDV antibodies in these groups (Asmare et al., 2013; Derdour et al., 2017). In addition, these findings are consistent with previous studies by Thapa et al. (2019) and Derdour et al. (2017), which found a strong association between abortion and BVDV seropositivity.

Furthermore, the present results confirmed the previous findings of Daves (2016), who found that BVDV seropositivity increased significantly in lactating cattle. This might contribute to increasing the risk of BVDV spreading through workers who milked cattle, and contaminated fomites or objects and equipment (Niskanen & Lindberg, 2003).

The present study found that BVDV seroprevalence of 18.28% among Egyptian cattle, leading to a negative impact on the dairy industry and causing severe economic losses. The risk factors analysis revealed that sex, age, introduction of new animal, history of abortion, AI, and lactation increased the risk of BVDV infection in cattle. Consequently, it is imperative to step up the bio-sanitary measures that allow for the reduction or elimination of the virus's presence in the area. Additionally, it is critical to monitor the groups identified as risk factors because they are primarily responsible for the disease's spread and any ensuing harm or effects on the region's livestock industry's ability to compete.

CONFLICT OF INTEREST STATEMENT

There are no conflicts of interest declared by the authors.