Nuo Su1,2†
Qi Wang1,2†
Hong-Ying Liu1
Lian-Min Li1,2Tian Tian1,2Ji-Ying Yin1,2Wei Zheng1,2Qing-Xia Ma1,2Ting-Ting Wang1,2
Ting Li1,2Tie-Lin Yang1,2
Jian-Ming Li1
Nai-Chao Diao1,2
Kun Shi1*
Rui Du1,3,4*- 1College of Chinese Medicine Materials, Jilin Agricultural University, Changchun, China
- 2College of Animal Science and Technology, Jilin Agricultural University, Changchun, China
- 3Laboratory of Production and Product Application of Sika Deer of Jilin Province, Jilin Agricultural University, Changchun, China
- 4Key Laboratory of Animal Production, Product Quality and Security, Ministry of Education, Jilin Agricultural University, Changchun, China
Background: Bovine viral diarrhea is one of the diseases that cause huge economic losses in animal husbandry. Many countries or regions have successively introduced eradication plans, but BVDV still has a high prevalence in the world. This meta-analysis aims to investigate the prevalence and risk factors of BVDV in the world in recent 10 years, and is expected to provide some reference and theoretical basis for BVDV control plans in different regions.
Method: Relevant articles published from 2010 to 2021 were mainly retrieved from NCBI, ScienceDirect, Chongqing VIP, Chinese web of knowledge (CNKI), web of science and Wanfang databases.
Results: 128 data were used to analyze the prevalence of BVDV from 2010 to 2021. BVDV antigen prevalence rate is 15.74% (95% CI: 11.35–20.68), antibody prevalence rate is 42.77% (95% CI: 37.01–48.63). In the two databases of antigen and antibody, regions, sampling time, samples, detection methods, species, health status, age, sex, breeding mode, and seasonal subgroups were discussed and analyzed, respectively. In the antigen database, the prevalence of dairy cows in the breed subgroup, ELISA in the detection method subgroup, ear tissue in the sample subgroup, and extensive breeding in the breeding mode were the lowest, with significant differences. In the antibody database, the prevalence rate of dairy cows in the breed subgroup and intensive farming was the highest, with a significant difference. The subgroups in the remaining two databases were not significantly different.
Conclusion: This meta-analysis determined the prevalence of BVDV in global cattle herds from 2010 to 2021. The prevalence of BVDV varies from region to region, and the situation is still not optimistic. In daily feeding, we should pay attention to the rigorous and comprehensive management to minimize the spread of virus. The government should enforce BVDV prevention and control, implement control or eradication policies according to local conditions, and adjust the policies in time.
1. Introduction
Bovine viral diarrhea virus (BVDV) is the main pathogen of bovine viral diarrhea BVD (1, 2), and it is the main member of flaviviridae and pestivirus genus, which consists of three species: pestivirus A (BVDV-1), pestivirus B (BVDV-2) and pestivirus H (bovine viral diarrhea virus type 3 [Hobi-like pestiviruses)] (WOAH). BVDV-1 contains at least 22 subgenotypes of 1a-1v and BVDV-2 and HoBi-like pestivirus are divided into 4 subtypes (3). Multiple species and genotypes lead to the mutation of BVDV, which brings great obstacles to its prevention and control. BVDV contains two biotypes, and BVDV can be divided into cytopathic type (CP) and non-cytopathic type (NCP) according to whether it causes pathological changes in cultured tissue cells (4). NCP BVDV can infect cows early in embryonic development and produce persistently infected (PI) calves. PI makes it more difficult to control BVDV. It is the main source of infection of BVDV, because it is immune tolerant to infected strains, does not produce antibodies, and is always infected and continuously detoxifies (5). In contrast, the risk of transient infection (TI) transmission is weaker, producing only mild clinical symptoms to the host and expelling the virus into the environment for a short period of time. However, TI damage to the immune system can exacerbate the occurrence of secondary infections, so it remains an important component of BVDV infection (6).
BVDV is widespread in the world and can cause gastrointestinal, respiratory and reproductive diseases. The induced immunosuppression can increase the probability of infection of other diseases (7). BVDV reduces the breeding and growth efficiency of livestock through various ways, increases the mortality rate of young animals and the prevalence rate of reproductive system, respiratory system and gastrointestinal diseases, and causes continuous and serious economic losses to the animal husbandry (8). BVDV can infect cattle, goats, sheep, camels, pigs and other cloven-hoofed animals (9–11). Among them, cattle are the main infection host and source of BVDV, and are most affected by diseases (12). As a major economic animal, cattle are closely related to people's life. According to the survey, the economic impact of BVD ranges from £0 to £552 per cow per year, with a mean impact of £46.50 (13). At the same time, BVDV's pollution to bovine-derived substances further endangers the accuracy of scientific research and the safety of biological products such as vaccines (14). The growing demand for beef and dairy products reminds people to focus on the health of primitive animals and avoid possible economic losses (15). Therefore, it is very important to investigate and control the prevalence of BVDV infection in cattle species. ACVIM's consensus statement clarifies the importance of BVDV control (16). Many countries have also introduced measures to control and purify BVDV. Denmark introduced the BVD eradication plan as early as 1994 (17). Northern Ireland began implementing the BVD AHWNI eradication program in 2013 and the virus positivity declined significantly by 2020 (18). Germany's 6-year mandatory plan has seen a significant decline in the number of PI by 2016, and further removal of the virus is the next challenge (19). Switzerland has had a control program since 2008 and infection rates have dropped significantly by 2020, but PI animals remain the last strong obstacle (20). In 2016–2017, the Indonesian government tried to breed beef cattle by increasing artificial insemination, hoping to reduce the vertical transmission of BVDV (21).
According to the positive rate of BVDV in different species, many articles have been meta-analyzed. Knowing the prevalence of BVDV in time can not only provide data support for the formulation of BVDV prevention and control policies, but also provide technical guidance for practical production.
This paper makes a meta-analysis on the prevalence of BVDV infection among cattle in the world in recent 10 years. Through the summary of the latest data and the thinking caused by eradication plans in different regions, the following questions are addressed: “What should we do to control BVDV? How should the control plan be carried out under different circumstances?”. We hope to observe the effectiveness of current prevention and control measures and provide reference for further prevention and control of BVDV in the future.
2. Materials and methods
2.1. Search strategy
We searched six databases of PubMed, ScienceDirect, Web of Science, CNKI, VIP, and Wanfang, and find articles published in Chinese and English from 2010 to May 20, 2021. Designed to filter prevalence data for all BVDV, the specific search process is as follows:
PubMed search strategy is as follows: According to MeSH terminology, the following keywords were used to search: “Diarrhea Viruses, Bovine Viral,” “Cattle,” and the Boolean operators “OR,” “AND” in the “Keyword/Title/Summary” field alone or in combination.
A: We search for “Cattle” based on MeSH terminology: ((((((((((((((((((((“Cattle”[Mesh]) OR (Cow)) OR (Cows)) OR (Bos indicus)) OR (Zebu)) OR (Zebus)) OR (Holstein Cow)) OR (Cow, Holstein)) OR (Dairy Cow)) OR (Cow, Dairy)) OR (Dairy Cows)) OR (Beef Cow)) OR (Beef Cows)) OR (Cow, Beef)) OR (Bos grunniens)) OR (Yak)) OR (Yaks)) OR (Bos taurus)) OR (Cow, Domestic)) OR (Domestic Cow)) OR (Domestic Cows).
B: We search for “Diarrhea Viruses, Bovine Viral” based on MeSH terminology: (((((((((((“Diarrhea Viruses, Bovine Viral”[Mesh]) OR (Bovine Viral Diarrhea Viruses)) OR (Bovine Pestivirus)) OR (Bovine Pestiviruses)) OR (Pestiviruses, Bovine)) OR (Bovine Diarrhea Virus)) OR (Bovine Diarrhea Viruses)) OR (Diarrhea Virus, Bovine)) OR (Diarrhea Viruses, Bovine)) OR (Virus, Bovine Diarrhea)) OR (Viruses, Bovine Diarrhea)) OR (Diarrhea Virus, Bovine Viral).
C: We used the Boolean operators “OR” for the entry terms and “AND” for the MeSH terms. (((((((((((((((((((((“Cattle”[Mesh]) OR (Cow)) OR (Cows)) OR (Bos indicus)) OR (Zebu)) OR (Zebus)) OR (Holstein Cow)) OR (Cow, Holstein)) OR (Dairy Cow)) OR (Cow, Dairy)) OR (Dairy Cows)) OR (Beef Cow)) OR (Beef Cows)) OR (Cow, Beef)) OR (Bos grunniens)) OR (Yak)) OR (Yaks)) OR (Bos taurus)) OR (Cow, Domestic)) OR (Domestic Cow)) OR (Domestic Cows)) AND ((((((((((((“Diarrhea Viruses, Bovine Viral”[Mesh]) OR (Bovine Viral Diarrhea Viruses)) OR (Bovine Pestivirus)) OR (Bovine Pestiviruses)) OR (Pestiviruses, Bovine)) OR (Bovine Diarrhea Virus)) OR (Bovine Diarrhea Viruses)) OR (Diarrhea Virus, Bovine)) OR (Diarrhea Viruses, Bovine)) OR (Virus, Bovine Diarrhea)) OR (Viruses, Bovine Diarrhea)) OR (Diarrhea Virus, Bovine Viral)).
Use advanced search in ScienceDirect and Web of Science databases to improve the accuracy of your results, enter subject terms “cattle,” “Diarrhea Viruses, Bovine Viral,” “prevalence” and select research articles to search. The VIP database was searched for articles by selecting the subject headings “bovine” and “bovine viral diarrheal mucosal disease” or “bovine” and “bovine viral diarrhea virus.” Wanfang and CNKI search strategies are: The theme words “bovine” and “bovine viral diarrhea mucosal disease” or: “bovine” and “bovine viral diarrhea virus” or “bovine” and “BVDV” were selected.
In order to collect comprehensive data as much as possible, Google Academic will further search the related articles of the collected articles.
2.2. Inclusion criteria and exclusion criteria
Eligible articles are screened according to the inclusion exclusion criteria below.
Inclusion criteria:
(1) Study on the prevalence of BVDV infection;
(2) Literature between 2010 and 2021.5.20;
(3) The species is cattle and the source is clear;
(4) The type of article is experimental research article;
(5) Literature published in Chinese or English.
Exclusion criteria:
(1) Repetitive articles;
(2) Articles that cannot be downloaded;
(3) Study animals were vaccinated or model animals;
(4) Research data is not clear;
(5) Sample size <30.
2.3. Data extraction
Import the search database results into the EndNote (EndNote X 9.3.3) reference manager software (Clarivate analysis, Philadelphia, Pennsylvania, USA) for screening, delete duplicate articles, and then two reviewers further screen according to the article title and abstract. Obtain key data information from all relevant studies, including the first author, sampling year, country, mainland, sample type, detection method, variety, season, health status, age, gender and breeding mode. Microsoft ® Excel ® 2019 MSO (16.0.14228.20216) 32 is used to sort and compile the data mentioned above.
2.4. Quality assessment
The level of proposal evaluation, formulation and evaluation methods determines the quality of selected literature. The scoring standard includes the following four aspects, whether it is random sampling, sampling time, whether the sampling method is detailed, whether the detection method is detailed, and whether there are more than four factors. “Yes” is 1 point, and the maximum is 5 points. Based on the above standards, the article is divided into three grades 0–1, 2–3, 4–5, respectively.
2.5. Statistical analysis
Under the guidance of PRISMA 2020, the article strictly follows its requirements and completes the systematic evaluation and meta-analysis (Supplementary material 1).
R software 4.0.0 is used to compile and calculate data. Sensitivity analyses were performed in different possible ways for all included studies, and bias tests were done by looking at funnel graphs (22). Egger's test and trim and fill analysis further illustrate whether bias occurs (23). Bias is indicated when the funnel chart is asymmetrical or when the Egger test p < 0.05. Q- test (X2 and p representation) was used to evaluate the heterogeneity among the studies, and the forest map was used for visual analysis. The degree of heterogeneity was further evaluated by I2 (24). The higher the I2, the greater the heterogeneity. The code in R for meta-analysis is in Supplementary material 2. Factors investigated in the subgroup analysis included sampling year (before 2017, after 2017), season, health status (healthy, clinically symptomatic), age (<6 months, >6 months), country, region, test method, sample origin, breed (beef cattle, dairy cows, dairy meat dual-use, breeding cattle), sex, breeding pattern (intensive, extensive).
3. Results
3.1. Flow chart and results of literature screening
A total of 5,549 eligible articles were obtained. Seven hundred four duplicate articles were deleted, and 4,500 articles were further screened according to the title, abstract, and Year of publication. Further screening according to the inclusion and exclusion criteria, 15 articles on vaccination were deleted, 2 sample sources were unclear, 10 article data were unclear, 20 data errors were used, 2 articles were used the same data, 4 non-epidemiological investigative articles, 134 non-sampling years, 17 articles with a sample size of <30, 32 articles that could not be queried, and a total of 109 articles were included. Nineteen articles were added to Google Academic, including 128 articles in total. The specific flow chart is shown in Figure 1.
Figure 1. Flow diagram of eligible studies for searching and selecting.
3.2. Studies included
Through literature screening, 128 studies were eligible for the meta-analysis. Among them, there were 77 articles on detecting antibodies and 51 articles on detecting antigens. Studies were identified from 19 countries worldwide, including 10 countries in Asia, two in North America, two in South America, two in Europe and three in Africa (Supplementary Figure 1).
There are a total of 51 antigen detection articles, including 27 articles of 4–5 points and 24 articles of 2–3 points (Table 1). A total of 46,211 cattle were tested, and 3,488 BVDV-positive cattle were tested, with a positive infection rate of 15.74% (95% CI: 11.35–20.68 3,488/46,211, Table 2). Among the regional subgroups, Europe had the highest positive rate with a positive rate of 23.27% (95% CI: 0.00–89.41, Table 2), followed by the Asia positivity rate of 16.75% (95% CI: 11.27–23.04, Table 2), The lowest is 0.32% (95% CI: 0.20–0.46, Table 2) in North America. Spain (59.40%, 95% CI: 50.91–67.62, Supplementary Table 1) has the highest antigen-positive rate among all countries and India has the lowest positive rate. The positivity rate after 2017 was higher than before 2017. The positive rate of ear tissue in the test samples was the lowest, with a positive rate of 0.48% (95% CI: 0.05–1.20, Table 2), which was significantly different. Diary cows had the lowest positive rate of infection, with a positive rate of 11.43% (95% CI: 6.61–17.32, Table 2), which was significantly different. In the health condition subgroup, the rate of BVDV infection with clinical symptoms was higher than that of clinically healthy cattle. Summer infection rate was lowest, with a positive rate of 4.17% (95% CI: 0.12–12.59, Table 2), Spring positivity rate was highest at 21.33% (95% CI: 0.82–57.99, Table 2). ELISA had the lowest positive rate among the test methods, with a positive rate of 6.94% (95% CI: 2.12–14.16, Table 2), which was significantly different. The positive rate in adult cattle is higher than that in calves. Extensive culture mode had the lowest rate of infection, with a positive rate of 1.11% (95% CI: 0.00–5.86, Table 2), which was significantly different.
Table 1. Included studies of Bovine viral diarrhea virus infection of cattle in the word.
Table 2. Antigen prevalence of Bovine viral diarrhea virus of cattle in the word.
A total of 77 articles were published on the detection of BVDV antibodies, including 43 articles with 4–5 points and 34 articles with 2–3 points (Table 3). A total of 55,349 samples were tested, of which 24,585 were positive, and the positive rate was 42.77% (95% CI: 37.01–48.63, Table 4). South America had the highest prevalence in the regional subgroup, with a positivity rate of 76.4% (95% CI: 72.06–80.50, Table 4, Supplementary Table 2) followed by North America, Africa, Europe, and Asia. Infection rates have decreased after 2017 compared to before 2017. Dairy cattle had the highest prevalence rate, with a positive rate of 48.68% (95% CI: 39.19–58.22, Table 4), which was significantly different. In the health condition subgroup, the infection rate of clinically healthy cattle was relatively low, with a positive rate of 43.80% (95% CI: 26.57–61.83, Table 4). The positive rate is relatively high in summer 60.16% (95% CI: 48.92–70.89, Table 4) and winter 63.44% (95% CI: 35.15–87.45, Table 4). The positive rate for cows is lower than that of bulls, and the positive rate of calves is lower than that of adult cattle. Intensive has the highest prevalence of all culture models, with a positive rate of 50.35% (95% CI: 42.93–57.76, Table 4).
Table 3. Included studies of Bovine viral diarrhea virus infection of cattle in the word.
Table 4. Antibody prevalence of Bovine viral diarrhea virus of cattle in the word.
3.3. Meta-analysis based on detected antigen
In antigen detection, a total of 46,211 cattle were tested, and 3,488 BVDV-positive cattle were tested, with a positive infection rate of 15.74% (95% CI: 11.35–20.68, Figure 2). PFT conversion rate and random effect model (χ2 = 0.0566, I2 = 99%, P = 0.00) were used (Table 5). The egger test result is t = 6.5574, p = 6.975e−08 (Supplementary Table 3, Figure 3). The funnel diagram shows that there is bias (Figure 4). The trim and fill analysis are used to correct the bias, a total of 22 articles were corrected, and the adjusted prevalence rate was 2.01% (95% CI:0.40–4.64). The results of sensitivity analysis show that the results of meta-analysis are reliable (Table 6).
Figure 2. Forest plot of bovine viral diarrhea virus antigen prevalence in the world study conducted 2010–2021 (decetion antigen).
Table 5. Normal distribution test for the normal rate and the different conversion of the normal rate.
Figure 3. Egger's test for publication bias (decetion antigen).
Figure 4. Funnel plot with pseudo 95% confidence interval limits for the examination of publication bias (decetion antigen).
Table 6. Sensitivity analysis (decetion antigen).
3.4. Meta-analysis based on detected antibody
In antibody detection, a total of 55,349 samples were tested, of which 24,585 were positive, and the positive rate was 42.77% (95% CI: 37.01–48.63, Figure 5). PFT conversion rate and random effect model(χ2 = 0.0664, I2 = 100%, P = 0.00, Table 7) were used. The egger test result is t = 0.68873, p = 0.4935 (Supplementary Table 4, Figure 6). The funnel diagram shows that there is bias (Figure 7). The data from the trim and fill analysis showed that no trimming performed, and the data unchanged, meaning there may be no significant publication bias. The results of sensitivity analysis show that the results of meta-analysis are reliable (Table 8).
Figure 5. Forest plot of bovine viral diarrhea virus antibody prevalence in the world study conducted 2010–2021 (decetion antibody).
Table 7. Normal distribution test for the normal rate and the different conversion of the normal rate.
Figure 6. Egger's test for publication bias (decetion antibody).
Figure 7. Funnel plot with pseudo 95% confidence interval limits for the examination of publication bias (decetion antibody).
Table 8. Sensitivity analysis (decetion antibody).
4. Discussion
BVDV is one of the most important bovine infectious diseases with global animal health and economic impacts. BVDV infection will not only cause huge economic losses to the breeding industry, but also in animal research and medical industry related serum, vaccines and other biological not infected with BVDV but contaminated with BVDV, which has a huge economic impact (150). BVDV can be spread in many ways. BVDV is widely transmitted, not only through direct contact, but also through various excreta, contaminated materials, etc (151). However, vertical transmission plays an important role in its epidemiology and pathogenesis. PI calves produced by pregnant cows through vertical transmission are the main source of infection of the disease, and they continue to be infected and carry BVDV pathogens throughout their lives. PI cattle are the main host of the virus. A large number of viruses are excreted from urine, feces, excrement, milk and semen, causing serious obstacles to the control of the disease.
The article searched all articles on the epidemiology of bovine BVDV in 2010–2021. The meta-analysis included 128 articles. Through the analysis, it is expected to investigate the latest data on the global prevalence of BVDV and provide data support for the prevention and control of BVDV. The detection of BVDV is usually divided into the detection of antigens and the detection of antibodies. A positive antigen represents the current prevalence of animals carrying BVDV pathogens, making it clear that the virus is spreading and harming the population. Positive antibody indicates infection, vaccine immunization or transient infection. As individuals immunized with vaccine are excluded, positive antibody in the article can be considered as being infected by virus. Both have important guiding significance for the description of the BVDV epidemic.
In the regional subgroup, there were fewer test samples in Europe, possibly due to large-scale vaccinations in Europe and not included in the study; On the other hand, it may be due to the fact that many European countries have eradicated BVDV or the prevalence rate has dropped to 1.5% (152). Examples include Denmark, Norway, Sweden and Finland (153). Switzerland, Austria and Germany are in the late or final stages of eradicating BVDV, followed by plans to eradicate BVDV in the Netherlands, Ireland and Poland (19). Control measures in several countries are mainly aimed at the clearance of PI animals. As early as 1990, a non-vaccination program in the Scandinavian countries was implemented to eliminate BVDV, which was planned to detect and remove PI animals based on ear groove samples (154). The Swiss clearance program restricts action mainly on pregnant cattle and directly tests for antigenic and viral genomes (155). Ireland's clearance program focuses on monitoring ear groove samples from newborn calves (156). PI animals are immune to BVDV and are unable to develop specific antibodies against it, which increases the obstacle to virus clearance and is also the main source of infection of the disease (157). And the mutagenicity of the virus itself, as well as the infection of cp BVDV from the outside world, has developed into a fatal mucosal disease, causing serious harm to the herd (158). There is evidence that when PI animals disappear, population virus transmission is largely stopped. However, the impact of removing only PI without considering TI is still debatable. There are cases where BVDV will persist for 6 years without PI mavericks (159). The successful implementation of a BVDV control plan should consider the impact of both modes of infection. In the process of removing PI, the prevalence rate should be monitored at the same time, and TI animals should be monitored in a timely manner. While the prevalence of PI animals varies from region to region in terms of legal support, it took nearly 10 years for all countries to reach the final stages of the control plan (160, 161). The long-term implementation of the plan also suggests that in order to successfully complete the purification, strict policies, strict management, and a high degree of prevention awareness of practitioners are required.
In the regional subgroups, the low prevalence rate in North America and the high prevalence rate in South America and South America may result in a small number of articles and be unrepresentative due to the limitations of search. There is no data on antigen testing in Africa, while the prevalence of antibody testing remains high. This also reminds us that although many African countries have carried out surveillance and culling of BVDV, it will take a long time to eliminate BVDV. Asia has the largest literature and the infection rate remains high, with no significant differences in regional subgroups. The high infection rate in Asia may be due to the lack of a sound control plan and a surge in herd numbers due to the rapid development of the cattle industry. From the measures in different regions, we can find that the control plan in Poland suggests that it is very important to control the possible risk of virus transmission if the eradication plan is to be successful. From the German plan, it can be found that voluntary policies are not enough to achieve freedom from disease, and the initial implementation of voluntary policies eventually leads to mandatory plans (19). The control plan of the Netherlands points out that in areas where BVDV has been eradicated, the increase of susceptible animals makes the area more affected by BVDV, so timely detection should be carried out to reduce the possibility of transmission of BVDV (162). Monitoring plays an important role in reducing the spread of BVDV, and the comprehensiveness of the sample survey is critical to the success of the eradication plan (20). It can be concluded from the control and eradication plans implemented in different countries and regions that the identification and isolation of PI animals is the key to the eradication plan, and vaccination and appropriate safety measures are the basic methods of the control plan (163). Therefore, countries and areas that have implemented eradication plans should conduct timely and regular prevalence surveys. Other areas should implement corresponding eradication plans as soon as possible.
Due to different control measures in different regions, a subgroup analysis of time for global BVDV antigen testing and antibody testing found that the prevalence after 2017 did not decrease significantly compared with the prevalence before 2017. Previous articles have analyzed that in the global region, the prevalence of PI showed a downward trend from 1982 to 2016, while the level of antibody prevalence was relatively stable (164). Our data also shows that the prevalence of antigens and antibodies has remained relatively stable since 2017. It is suggested that we should improve the corresponding eradication policy and give certain time and patience to eliminate pathogens. BVDV still has a high infection rate, and this high spread may be due to the lack of complete prevention and control measures for BVDV, the most important reason being the failure to detect and eliminate PI animals (151). In addition, the lack of commercial vaccines and reasonable and effective prevention and control programs is one of the reasons for the high prevalence of BVDV (27). Commercial transportation, fertilization of breeding cattle, and the introduction of new herds are all indispensable factors in the spread of disease, hindering the eradication of BVDV. Therefore, it is important to improve the monitoring of BVDV and introduce relevant control measures (151, 165).
In the breed subgroup, the antibody test results were the highest among dairy cattle, with significant difference. On the one hand, it may be due to the long service period of dairy cows, which have more opportunities to contact with pathogens. Studies have also confirmed that the positive rates of tuberculosis, brucellosis and bovine leukemia virus in dairy cows are higher than those in beef cattle (165, 166). On the other hand, compared with beef cattle, there may be more contact between cows and milkers, and the cross-infection among different cows is more intensive during milking, which leads to more opportunities for virus contact and greater risk of infection (142). Among the antigen test results, the positive rate of dairy cows was the lowest, and the difference was significant. Perhaps this is because the harm of antigen-positive cows to dairy cows is more intuitive, such as decreased milk yield, stillbirth, abortion, etc (12, 167, 168), and the production performance of dairy cows needs higher health, so antigen-positive cows are eliminated in time (169–171). For different breeds of cattle, different control measures should be taken according to different economic uses and lifestyles, and strict management should be taken to reduce the prevalence of BVDV.
Age has long been considered the most common influencing factor associated with infection rates (172). The data in the article show that the prevalence of adult cattle is higher than that of calve, and there is no significant difference. Many studies have also pointed out that the prevalence of adult cattle is higher than that of calves as a factor of age (74, 149, 173). This may be due to the longer survival time of adult cattle, a higher chance of exposure to the virus, and a higher probability of infection (141). In addition, antibody prevalence in calves is much higher than antigen prevalence, possibly due to the fact that calves can obtain colostrum antibodies from the mother (174). For calves, whether they are PI cattle carrying antigens should be detected in time, and eliminated in time to prevent the spread of infection. Adult cattle should have a reasonable detection system and a sound management system to reduce the chance of contact with the virus and reduce the prevalence of the disease.
The survey data of the article shows that the prevalence rate is relatively high in winter and spring, no matter for antigen detection or antibody detection. This may be due to the breeding season in spring and winter. It has been reported that in winter and spring, both male and female animals have strong reproductive performance, which is more conducive to cattle breeding (175, 176). The spread of BVDV in the breeding process led to the birth of more PI positive calves, further promoting the increase of the positive rate. The prevalence of BVDV antibody is still high in summer. It may be that the PI animals produced continuously expel viruses to the external environment, leading to the expansion of infection. Some literature points out that there is no antiviral drug to prevent the spread of BVDV in the farm at present, and the spread of the virus can only be prevented by isolating PI animals or vaccinating (177). Therefore, BVDV detection should be done well in the breeding season to reduce the production of PI animals and control the spread of BVDV from the source.
Many articles point out that gender does not have a large influence on infection rates, and bulls are just as susceptible as cows (74). The results of this survey show that there is no significant difference, which is consistent with other research results. Investigation samples of cows are much larger than those of bulls, possibly due to the fact that bulls are mostly used as beef cattle and female cows are used for milk production and reproductive purposes. Female cattle are more affected by the disease. Since PI calves born of cow infection during the first trimester of pregnancy are the main source of infection of the disease, cow test samples are collected in antigen testing to prevent the birth of PI cattle. Therefore, the prevention and control of PI cattle can be screened for antigens from pregnant cows.
In the introduction of BVDV 2018, the diagnosis of BVDV includes nucleic acid detection of QPCR, antigen antibody detection of ELISA, IHC, VN and virus isolation. PCR method can almost meet all purposes of detection, including making group animals free from infection, individual animals free from infection before moving, promoting the implementation of eradication policy, confirmation of clinical cases and detection of infection rate. PCR detection method has the advantages of convenience, rapidity and large sample size. The ELISA method is not applicable to animals with acute infection. IHC is mainly for diagnostic investigation. VN and virus isolation are usually used in laboratory research. It can be seen in the antigen detection data that the positive rate of PCR test is higher than the positive rate of ELISA test. There have also been reports of low sensitivity and accuracy of ELISA testing compared to PCR (178). Young animals can also obtain BVDV antibodies from the milk of female animals, thereby reducing the detection rate of ELISA antigens. This is consistent with the findings of this paper. VN has the highest detection rate, but it is difficult to detect, the sample detection volume is small, and it is generally not used in epidemiological investigations (28). In epidemiological investigations, antibody testing mostly chooses the rapid and inexpensive ELISA test, while the antigen test chooses a more sensitive PCR test (179).
The results of the survey show that most of the antibody test samples are derived from serum, and the test is relatively mature. The feces positivity rate was highest among the antigen-tested samples, followed by blood samples and ear tissue sample. The ear tissue sample is significantly different from other samples, and its low prevalence rate may be due to the fact that the sample was collected from the area where BVDV purification was carried out. Feces samples and blood samples can reflect the prevalence of infection. Feces sample collection is more convenient, the harm to cattle is small, but there is a possibility of cross-infect; Stress may occur on cattle during blood sample collection; Ear tissue samples are often used for the removal of PI cattle under the purification policy of various regions. For the detection of BVDV in cattle, the most appropriate samples shall be taken according to local conditions to make the detection results comprehensive and correct (180).
Breeding mode has always been a key factor affecting BVDV infection. An article survey shows that the low prevalence of grazing and breeding is due to the low density of grazing and breeding (40). However, some data show that the prevalence of intensive farming is low, and some studies show that grazing and breeding have the opportunity to contact more pathogens. Studies have pointed out that although BVDV cannot be transmitted by flies, flies have been shown to carry the BVDV pathogen (181). In the breeding mode subgroup, the positive rate of intensive culture was higher than that of extensive culture. On the one hand, there may be errors in monitoring the infection rate due to the difficulty in sampling free range animals. On the other hand, the virus may spread widely due to the high density of intensive farming. In addition, BVDV is introduced and spread through contaminated houses, water tanks, feeds and feeding equipment (182).
When BVDV infection occurs, the clinical symptoms of acute infected animals usually include temperature rise to 40°C, diarrhea, oral erosion, etc. There are few or no clinical symptoms observed in other infections (183). Mucosal diseases induced by BVDV do not show clinical symptoms within 1 week. After 1 week, severe diarrhea, dehydration, anorexia, and lethargy will occur, and death will occur 1 week after clinical symptoms (184). Due to the low incidence of acute infection and mucosal disease, BVDV infection will not lead to obvious clinical infection, or only non-specific clinical symptoms and immunosuppression (6). The immunosuppression will be secondary to other pathogenic infections, which may cause a series of clinical symptoms and endanger the health level of livestock (185). Through the division of clinical health, the results showed that the prevalence rate of cattle with clinical symptoms was higher than that of clinical healthy cattle, indicating that regular detection of cattle health was also an important way to prevent and control infection. Therefore, whether or not having a sound management system is the key to affecting the infection rate of the intensive breeding industry. A reasonable and perfect management system can greatly reduce the spread of virus.
Through our meta-analysis, we found that the prevalence of BVDV in the world is still very high. In the areas where the eradication plan is implemented, attention should still be paid to controlling the possible transmission risk of the virus. In terms of time span, the control and elimination of BVDV requires the joint efforts of all countries and regions to develop reasonable and effective prevention and control programs to eliminate PI animals. At the same time, the elimination of BVDV requires a certain degree of patience, timely grasp the epidemic situation, and improve the prevention and control policy. Different control measures should be taken for different breeds of cattle, and strict management policies are required to reduce BVDV infection. After calves are born, they should be tested for antigen in time to reduce the birth of PI cattle. BVDV detection and elimination should be done well in winter and spring breeding seasons. For cows, it is necessary to timely detect whether there is antigen infection before pregnancy to prevent the production of PI cattle. The ear tissue samples selected for antigen monitoring are more accurate, VN detection method has a higher accuracy, while PCR detection method has a wide detection range and a large sample detection volume. Generally, ELISA is used to detect serum samples. In raising cattle, attention should be paid to the cleanliness and hygiene of the breeding environment.
To sum up, based on the epidemiological situation of BVDV in different areas, the eradication and prevention policies should be formulated and revised in time. Meanwhile, it is necessary to strengthen the awareness of herders to diseases and increase the awareness of veterinary and other related professionals to prevent and control BVDV. Our meta-analysis still has some limitations. The main reasons are as follows: 1. Due to the choice of language and database, it was not included in all studies. 2. The data cannot be downloaded or excluded from the inclusion and exclusion criteria. 3. Many countries do not have perfect testing procedures and do not test all cattle.
Data availability statement
The original contributions presented in the study are included in the article/Supplementary material, further inquiries can be directed to the corresponding authors.
Author contributions
RD and KS: idea and concept. NS: writing and editing of the manuscript. RD: funding. H-YL, L-ML, QW, and KS: revision of the manuscript. Q-XM, T-TW, WZ, and T-LY: collection and extraction of data. TT and J-YY: database establishment. TL, N-CD, QW, and J-ML: data analysis. All the authors contributed to the editing of the manuscript and approved the final manuscript.
Funding
This work was supported by the National Natural Science Foundation of China (No. 31672577).
Acknowledgments
We thank the scientists and personnel of the College of Animal Science and Technology, Jilin Agricultural University, and the College of Chinese Medicine Materials, Jilin Agricultural University, for their collaboration.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.
Supplementary material
The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fvets.2022.1086180/full#supplementary-material
Abbreviations
BVDV, Bovine viral diarrhea virus; PRISMA, Preferred reporting items for systematic reviews and meta-analyses.
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Keywords: bovine viral diarrhea virus, cattle, meta-analysis, antigen prevalence, antibody prevalence, risk factors
Citation: Su N, Wang Q, Liu H-Y, Li L-M, Tian T, Yin J-Y, Zheng W, Ma Q-X, Wang T-T, Li T, Yang T-L, Li J-M, Diao N-C, Shi K and Du R (2023) Prevalence of bovine viral diarrhea virus in cattle between 2010 and 2021: A global systematic review and meta-analysis. Front. Vet. Sci. 9:1086180. doi: 10.3389/fvets.2022.1086180
Received: 03 November 2022; Accepted: 22 December 2022;
Published: 17 January 2023.
Edited by:
Yasser Mahmmod, Higher Colleges of Technology, United Arab EmiratesReviewed by:
Ahmed N. F. Neamat-Allah, Zagazig University, EgyptAndrea Verna, Instituto de Innovación para la Producción Agropecuaria y el Desarrollo Sostenible (IPADS), Argentina
Vahid Rahmanian, Jahrom University of Medical Sciences, Iran
Copyright © 2023 Su, Wang, Liu, Li, Tian, Yin, Zheng, Ma, Wang, Li, Yang, Li, Diao, Shi and Du. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Kun Shi, 
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†These authors have contributed equally to this work